Isolation, biotyping and antimicrobial susceptibility of Campylobacter isolates from raw milk in Erbil city, Iraq


Submitted: 30 September 2019
Accepted: 11 December 2019
Published: 11 March 2021
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This study aimed to determine the prevalence and antimicrobial sensitivity of Campylobacter species in raw milk sold at retail vending in Erbil city. Three hundred and fifty (350) samples were aseptically collected from retail raw milk shops between January and June 2019. For isolation of Campylobacter spp., samples were cultured on selective media and tested for biotype and antimicrobials susceptibility by disk diffusion assay. The overall prevalence of Campylobacter spp. was 12.6%. Campylobacter jejuni was significantly prevalent (65.9%) among other Campylobacter species. Antimicrobial susceptibility testing showed complete sensitivity to tetracycline, rifampicin, and neomycin. On the other hand, total resistance to ampicillin and trimethoprim was observed. Strikingly, as low as 56.8% and 72.7% of isolates are still sensitive to the drugs of choice in campylobacteriosis treatment; ciprofloxacin and erythromycin respectively. This resistance pattern of Campylobacter found in this study is critically alarming owing to the insusceptibility to the aforementioned antibiotics commonly used as the drugs of choice for campylobacteriosis treatment. Increase in Campylobacter prevalence in raw milk was associated with warm season. These levels prevalence and resistance worth further investigations and effective countermeasures owing to potential public health hazards.


Al-Dulaimi FM, 2013. Prevalence of Campylobacter species in faeces of children and poultry meats in Dhamar province. MSc thesis, Sana’a University, Yemen.

Al-Rawe AM, Al-Taee GAM, 2005. Biotyping some Campylobacter jejuni isolates and their sensitivity to common antibiotics. Rafidain J Sci 16:31–8.

Al-Zailay FMA, 2017. Epidemiological study on campylobacteriosis in human and cow raw milk at Dhamar governorate, Yemen. MSc thesis, Thamar University, Yemen.

Backert S, Tegtmeyer N, Cróinín TÓ, Boehm M, Heimesaat MM, 2017. Human campylobacteriosis. In: Klein G, editor. Campylobacter: Features, Detection, and Prevention of Foodborne Disease. Academic press, London, pp 1–25. DOI: https://doi.org/10.1016/B978-0-12-803623-5.00001-0

Barakat AM, Sobhy MM, El Fadaly HA, Rabie NS, Khalifa NO, Hassan E, Kotb M, Amin Girh Z, Sedeek D, Zaki M, 2015. Zoonotic hazards of campylobacteriosis in some areas in Egypt. Life Sci J 12:9–14.

Bianchini V, Borella L, Benedetti V, Parisi A, Miccolupo A, Santoro E, Recordati C, Luini M, 2014). Prevalence in bulk tank milk and epidemiology of Campylobacter jejuni in dairy herds in Northern Italy. Appl Env Microbiol, 80:1832–1837. DOI: https://doi.org/10.1128/AEM.03784-13

Bolton DJ, 2015. Campylobacter virulence and survival factors. Food Microbiol 48:99–108. DOI: https://doi.org/10.1016/j.fm.2014.11.017

Burakoff A, Brown K, Knutsen J, Hopewell C, Rowe S, Bennett C, Cronquist A, 2018. Outbreak of fluoroquinolone-resistant Campylobacter jejuni infections associated with raw milk consumption from a Herdshare Dairy - Colorado, 2016. MMWR 67:146–148. DOI: https://doi.org/10.15585/mmwr.mm6705a2

Castrodale LJ, Gerlach RF, Xavier CM, Smith BJ, Cooper MP, Mclaughlin JB, 2013. Sharing milk but not messages: campylobacteriosis associated with consumption of raw milk from a cow-share program in Alaska, 2011. J Food Prot 76:744–747. DOI: https://doi.org/10.4315/0362-028X.JFP-12-329

Chlebicz A, Śliżewska K, 2018. Campylobacteriosis, salmonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: a review. Int J Env Res Public Health 15: 863. https://doi.org/10.3390/ijerph15050863 DOI: https://doi.org/10.3390/ijerph15050863

Chukwu, MO, Luther King Abia ALK, Ubomba-Jaswa E, Obi L, Dewar JB, 2019. Characterization and phylogenetic analysis of campylobacter species isolated from paediatric stool and water samples in the Northwest province, South Africa. Int J Env Res Public Health 16: 2205. https://doi.org/10.3390/ijerph16122205 DOI: https://doi.org/10.3390/ijerph16122205

CLSI (Clinical and Laboratory Standards Institute), 2011. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. M100-S21. Wayne, Pennsylvania.

EFSA (European Food Safety Authority), 2017. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016. Europ Food Saf Agen J 15. https://doi.org/10.2903/j.efsa.2017.5077 DOI: https://doi.org/10.2903/j.efsa.2017.5077

Elmalı M, Can HY, 2019. Antimicrobial susceptibility and virulence-associated genes in Campylobacter isolates from milk and wastewater in Hatay, Turkey. Ciência Rural 49. https://doi.org/10.1590/0103-8478cr20180227 DOI: https://doi.org/10.1590/0103-8478cr20180227

Evans MR, Roberts RJ, Ribeiro CD, Gardner D, Kembrey D, 1996. A milk-borne Campylobacter outbreak following an educational farm visit. Epidemiol Infect 117:457–462. DOI: https://doi.org/10.1017/S0950268800059112

Heuvelink AE, van Heerwaarden C, Zwartkruis-Nahuis A, Tilburg JJ, Bos MH, Heilmann FG, Hofhuis A, Hoekstra T, de Boer E, 2009. Two outbreaks of campylobacteriosis associated with the consumption of raw cows’ milk. Int J Food Microbiol 134:70–74. DOI: https://doi.org/10.1016/j.ijfoodmicro.2008.12.026

Ibrahim JN, Eghnatios E, El Roz A, Fardoun T, Ghssein G, 2019. Prevalence, antimicrobial resistance and risk factors for campylobacteriosis in Lebanon. J Infect Developing Countries 13:11–20. DOI: https://doi.org/10.3855/jidc.10729

Isabel R, 2019. Campylobacter jejuni bacteremia in a patient with asplenia and enteritis. IDCases 17, e00555. https://doi.org/10.1016/J.IDCR.2019.E00555 DOI: https://doi.org/10.1016/j.idcr.2019.e00555

Jorgensen F, Ellis-Iversen J, Rushton S, Bull SA, Harris SA, Bryan SJ, Gonzalez A, Humphrey TJ. (2011). Influence of season and geography on Campylobacter jejuni and C. coli subtypes in housed broiler flocks reared in Great Britain. Appl Env Microbiol 77:3741–3748. DOI: https://doi.org/10.1128/AEM.02444-10

Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM, 2015. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 28:687–720. DOI: https://doi.org/10.1128/CMR.00006-15

Kanaan MH, 2018. Biotyping and resistotyping of Campylobacter isolates recovered from frozen chicken meat sold in Baghdad province. Int J Sci Res 7:304–306.

Kashoma IP, Kassem II, John J, Kessy BM, Gebreyes W, Kazwala RR, Rajashekara G, 2016. Prevalence and antimicrobial resistance of Campylobacter isolated from dressed beef carcasses and raw milk in Tanzania. Microb Drug Resist 22:40–52. DOI: https://doi.org/10.1089/mdr.2015.0079

Kazemeini H, Valizade Y, Parsaei P, Nozarpour N, Rahimi E, 2011. Prevalence of Campylobacter species in raw bovine milk in Isfahan, Iran. Middle-East J Sci Res 5:664–666.

Korlath JA, Osterholm MT, Judy LA, Forfang JC, Robinson RA, 1985. A Point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152:592–596. DOI: https://doi.org/10.1093/infdis/152.3.592

Levine MM, Kotloff KL, Nataro, JP, Muhsen K, 2012. The Global Enteric Multicenter Study (GEMS): Impetus, rationale, and genesis. Clin Infect Dis 55:S215–S224. DOI: https://doi.org/10.1093/cid/cis761

Longenberger AH, Palumbo AJ, Chu AK, Moll ME, Weltman A, Ostroff SM, 2013. Campylobacter jejuni infections associated with unpasteurized milk—multiple states, 2012. Clin Infect Dis 57:263–266. DOI: https://doi.org/10.1093/cid/cit231

Luangtongkum T, Jeon B, Han J, Plummer P, Logue CM, Zhang Q, 2009. Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol, 4:189–200. DOI: https://doi.org/10.2217/17460913.4.2.189

MacFaddin JF, 2000. Biochemical Tests for the Identification of Medical Bacteria. 3rd ed. Lippincott, Williams & Wilkins Co, Philadelphia, PA, USA.

Mahmood MS, Hussain I, Arshad MI, Ali S, Aktar M, Khan A, Mahmood F, 2009. Seasonal prevalence of Campylobacter species in milk and milk products in Pakistan. Pak J Zool Suppl Ser 9:227-231.

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

Marinou I, Bersimis S, Ioannidis A, Nicolaou C, Mitroussia-Ziouva A, Legakis NJ, Chatzipanagiotou S, 2012. Identification and antimicrobial resistance of Campylobacter species isolated from animal sources. Front Microbiol 3:58. https://doi.org/10.3389/fmicb.2012.00058 DOI: https://doi.org/10.3389/fmicb.2012.00058

Medeiros D, Hofmann L, 2002. Isolation of thermophilic Campylobacter from food, MFLP-46. Ottawa, Canada.

Modi S, Brahmbhatt MN, Chatur YA, Nayak JB, 2015. Prevalence of Campylobacter species in milk and milk products, their virulence gene profile and antibiogram. Vet World 8:1–8. DOI: https://doi.org/10.14202/vetworld.2015.1-8

Mughal, M. H. (2018). Campylobacteriosis: a global threat. Biomed J Sci Tech Res 11:001–005. DOI: https://doi.org/10.26717/BJSTR.2018.11.002165

Mungai EA, Behravesh CB, Gould LH, 2015. Increased outbreaks associated with nonpasteurized milk, United States, 2007-2012. Emerg Infect Dis 21:119–122. DOI: https://doi.org/10.3201/eid2101.140447

Nachamkin I, Fitzgerald C, 2015. Campylobacter and Arcobacter. In: Jorgensen JH, Pfaller MA, eds. Manual of Clinical Microbiology, 11th edn. ASM press, Washington DC, pp 998–1012. DOI: https://doi.org/10.1128/9781555817381.ch56

Omara ST, Fadaly HA, Barakat AMA, 2015. Public health hazard of zoonotic Campylobacter jejuni reference to Egyptian regional and seasonal variations. Res J Microbiol 10:343–354. DOI: https://doi.org/10.3923/jm.2015.343.354

Patrick ME, Christiansen LE, Wainø M, Ethelberg S, Madsen H, Wegener HC, 2004. Effects of climate on incidence of Campylobacter spp. in humans and prevalence in broiler flocks in Denmark. Appl Env Microbiol 70:7474–7480. DOI: https://doi.org/10.1128/AEM.70.12.7474-7480.2004

Porter IA, Reid TMS, 1980. A milk-borne outbreak of Campylobacter infection. J Hyg 84:415–419. DOI: https://doi.org/10.1017/S0022172400026942

Rahimi E, Sepehri S, Momtaz H, 2013. Prevalence of Campylobacter species in milk and dairy products in Iran. Evue Med Vet 164:283–288.

Salihu MD, Junaidu AU, Magaji AA, Rabiu ZM, 2010. Study of Campylobacter in raw cow milk in Sokoto state, Nigeria. Br J Dairy Sci 1:1–5.

Schielke A, Rosner BM, Stark K, 2014. Epidemiology of campylobacteriosis in Germany – insights from 10 years of surveillance. BMC Infect Dis 14:30. DOI: https://doi.org/10.1186/1471-2334-14-30

Shen Z, Wang Y, Zhang Q, Shen J, 2018. Antimicrobial resistance in Campylobacter spp. Microbiol Spec 6. https://doi.org/10.1128/microbiolspec.ARBA-0013-2017 DOI: https://doi.org/10.1128/microbiolspec.ARBA-0013-2017

Weltman A, Longenberger AH, Moll M, Johnson L, Martin J, Beaudoin A, 2013. Recurrent outbreak of Campylobacter jejuni infections associated with a raw milk dairy — Pennsylvania, April–May 2013. Retrieved from https://stacks.cdc.gov/view/cdc/54694

WHO. (2018). Campylobacter. Retrieved September 25, 2019, from https://www.who.int/news-room/fact-sheets/detail/campylobacter

Zelenáková L, Ziarovská J, Kozelová D, Mura L, Lopasovský L, Bobková A, Zajác P, Capla J, Tináková K, 2012. Campylobacteriosis: importance of strengthening surveillance and reported foodborne disease control within European Union. J Microbiol Biotechnol Food Sci, 1:855-867

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Almashhadany DA. Isolation, biotyping and antimicrobial susceptibility of <em>Campylobacter</em> isolates from raw milk in Erbil city, Iraq. Ital J Food Safety [Internet]. 2021 Mar. 11 [cited 2024 Apr. 25];10(1). Available from: https://www.pagepressjournals.org/ijfs/article/view/8589

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