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Molecular prevalence of Coxiella burnetii in milk in Iran: a systematic review and meta-analysis

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Abstract

Q fever is a major zoonotic disease in the world. The aim of this meta-analysis was to estimate the prevalence of Coxiella burnetii in animal milk in Iran. We systematically reviewed the literature to identify eligible studies from January 2008 to June 2016 in English or Farsi (Persian) databases. We extracted the molecular prevalence of C. burnetii in milk from cows, goats, sheep, and camels in Iran. The total prevalence of C. burnetii in cow milk was 15.09% (95% CI 11.08–19.10) by PCR methods. The highest and lowest prevalence of Q fever agent were seen in the East Azerbaijan (25.55%) and Khorasan-Razavi (4.22%) provinces, respectively. The molecular prevalence of C. burnetii in goat milk was 7.80% (95% CI 3.54–12.07%). The provinces of Qom (0%) and Lorestan (44.71%) had the lowest and the highest frequency of C. burnetii infection in goat’s milk, respectively. Total prevalence of C. burnetii in sheep milk was 3.79% (95% CI 0.72–6.87%). The highest frequency of C. burnetii in sheep milk was detected in the Khorasan-Razavi province (34.78%). The frequency of C. burnetii in camel milk was 1.43%. High infection of C. burnetii in milk is an important health problem in Iran, amplified by the traditional preparations of dairy products.

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References

  • Abbasi S, Farzan R, Momtaz H (2011) Molecular detection of Coxiella burnetii in goat bulk milk samples in some provinces of Iran African Journal of Biotechnology 10:18513–18515

    Article  CAS  Google Scholar 

  • Ahmadizadeh C, Moosakhani F, Jamshidian M (2015) Detection and Identification of Coxiella burnetii in Milk Cattles of Tehran Province Advances in Bioresearch 6

  • Alipour Z (2011) The prevalence of Q fever in dairy cows referred to the veterinary hospital in Ahvaz by ELISA and polymerase chain reaction. Shahid Chamran University

  • Amin W, Ahmed S (2009) Detection of Coxiella burnetii in bovine milk samples using polymerase chain reaction Assiut Veterinary Medical Journal 55:23–31

    Google Scholar 

  • Anderson A et al. (2013) Diagnosis and management of Q fever—United States, 2013: recommendations from CDC and the Q Fever Working Group MMWR Recomm Rep 62:1–30

    PubMed  Google Scholar 

  • Angelakis E, Raoult D (2010) Q fever Veterinary microbiology 140:297–309

    Article  CAS  PubMed  Google Scholar 

  • Bond K et al. (2016) One Health approach to controlling a Q fever outbreak on an Australian goat farm Epidemiology and infection 144:1129–1141

    Article  CAS  PubMed  Google Scholar 

  • Borji S, Jamshidi A, Khanzadi S, Razmyar J (2014) Detection of Coxiella burnetii and sequencing the IS1111 gene fragment in bulk tank milk of dairy herds Iranian Journal of Veterinary Science and Technology 6:21–28

    Google Scholar 

  • Cerf O, Condron R (2006) Coxiella burnetii and milk pasteurization: an early application of the precautionary principle? Epidemiology and Infection 134:946–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cisak E, Zając V, Sroka J, Sawczyn A, Kloc A, Dutkiewicz J, Wójcik-Fatla A (2017) Presence of Pathogenic Rickettsiae and Protozoan in Samples of Raw Milk from Cows, Goats, and Sheep Foodborne Pathogens and Disease 14:189–194

    Article  CAS  PubMed  Google Scholar 

  • Dijkstra F et al. (2012) The 2007–2010 Q fever epidemic in The Netherlands: characteristics of notified acute Q fever patients and the association with dairy goat farming FEMS Immunology & Medical Microbiology 64:3–12

    Article  CAS  Google Scholar 

  • Eldin C, Angelakis E, Renvoisé A, Raoult D (2013) Coxiella burnetii DNA, but not viable bacteria, in dairy products in France The American journal of tropical medicine and hygiene 88:765–769

    Article  PubMed  PubMed Central  Google Scholar 

  • Eldin C et al. (2017) From Q fever to Coxiella burnetii infection: a paradigm change Clinical microbiology reviews 30:115–190

    Article  PubMed  Google Scholar 

  • Esmaeili S, Golzar F, Ayubi E, Naghili B, Mostafavi E (2017) Acute Q fever in febrile patients in northwestern of Iran PLoS neglected tropical diseases 11:e0005535

    Article  PubMed  PubMed Central  Google Scholar 

  • Etemadfar L (2016) Investigetion of Coxiella brunetti in raw milk and unpasteurized traditional dairy products in shopping centers in the city of Khorramabad, Lorestan Province. Lorestan University

  • Fretz R, Schaeren W, Tanner M, Baumgartner A (2007) Screening of various foodstuffs for occurrence of Coxiella burnetii in Switzerland International journal of food microbiology 116:414–418

    Article  CAS  PubMed  Google Scholar 

  • Gale P, Kelly L, Mearns R, Duggan J, Snary EL (2015) Q fever through consumption of unpasteurised milk and milk products–a risk profile and exposure assessment Journal of Applied Microbiology 118:1083–1095

    Article  CAS  PubMed  Google Scholar 

  • García-Pérez A, Astobiza I, Barandika J, Atxaerandio R, Hurtado A, Juste R (2009) Short communication: investigation of Coxiella burnetii occurrence in dairy sheep flocks by bulk-tank milk analysis and antibody level determination Journal of dairy science 92:1581–1584

    Article  CAS  PubMed  Google Scholar 

  • Georgiev M et al. (2013) Q fever in humans and farm animals in four European countries, 1982 to 2010 Eurosurveillance 18:1–13

  • Ghalyanchi Langeroudi A, Babkhani N, Zolfaghari MR, Majidzadeh Arbadili K, Morovvati A, Soleimani M (2013) Detection of Coxeilla brunetii in bulk tank milk samples from dairy bovine farms using nested-PCR in Qom, Iran, 2011 Iranian Journal of Veterinary Medicine 7:207–211

    CAS  Google Scholar 

  • Ghasemian R, Mostafavi E, Esmaeili S, Najafi N, Arabsheybani S (2016) A Survey of Acute Q Fever among Patients with Brucellosis-Like and Atypical Pneumonia Symptoms Who Are Referred to Qaemshahr Razi Hospital in Northern Iran (2014–2015) Global Journal of Health Science 9:225–232

    Article  Google Scholar 

  • Guatteo R, Beaudeau F, Berri M, Rodolakis A, Joly A, Seegers H (2006) Shedding routes of Coxiella burnetii in dairy cows: implications for detection and control Veterinary research 37:827–833

    Article  PubMed  Google Scholar 

  • Guatteo R, Seegers H, Taurel A-F, Joly A, Beaudeau F (2011) Prevalence of Coxiella burnetii infection in domestic ruminants: a critical review Veterinary microbiology 149:1–16

    Article  PubMed  Google Scholar 

  • Gyuranecz M et al. (2012) Prevalence of Coxiella burnetii in Hungary: screening of dairy cows, sheep, commercial milk samples, and ticks Vector-Borne and Zoonotic Diseases 12:650–653

    Article  PubMed  Google Scholar 

  • Haghi F, Zeighami H, Naderi G, Samei A, Roudashti S, Bahari S, Shirmast P (2015) Detection of major food-borne pathogens in raw milk samples from dairy bovine and ovine herds in Iran Small Ruminant Research 131:136–140

    Article  Google Scholar 

  • Hirai A et al. (2005) Investigation of Coxiella burnetii contamination in commercial milk and PCR method for the detection of C. burnetii in egg Shokuhin eiseigaku zasshi Journal of the Food Hygienic Society of Japan 46:86–92

    Article  CAS  PubMed  Google Scholar 

  • Jaydari A, Khademi P, Lorestani S, Maleki S (2014) Development of Nested-PCR method for detection coxiella bruneti in goat milk samples Iranian Journal of Public Health 43:171

    Google Scholar 

  • Kargar M, Rashidi A, Doosti A, Ghorbani-Dalini S, Najafi A (2013) Prevalence of Coxiella burnetii in bovine bulk milk samples in southern Iran Comparative clinical pathology 22:331–334

    Article  Google Scholar 

  • Kargar M, Rashidi A, Doosti A, Najafi A, Ghorbani-Dalini S (2015) The Sensitivity of the PCR Method for Detection of Coxiella burnetii in the Milk Samples Zahedan Journal of Research in Medical Sciences 17

  • Karimian A, Mahzounieh M, Ebrahimi Kahrizsangi A (2016) Genomic detection of Coxiella burnetii in bulk tank milk samples by Nested-PCR method in Shahrekord, Iran Pajoohandeh Journal 21:52–57

    Google Scholar 

  • Khademi P (2014) Genomic detection of Coxiella burnetii (Q fever) in cow's milk and goat farms Khorramabad. Shahrekord University

  • Khademi P, Mahzounieh M, Koutamehr ME (2014a) Genomic detection of Coxiella burnetii (Q fever agent) in cattles milk samples in animal farms Bonab township. Iran Iranian journal of public health 43:292

    Google Scholar 

  • Khademi P, Mahzounieh MR, Kahrizsangi AE, Shdravan E (2014b) Genomic detection of Coxiella burnetii in goat milk samples in animal farms Khorramabad Township, Iran Pajoohandeh Journal 19:162–168

    Google Scholar 

  • khademi p, Jaydari A, Esmaeili Koutamehr M (2015) Genomic detection of Coxiella burnetii in cattle milk samples by Nested-PCR method, Iran Iranian Journal of Medical Microbiology 9:69–72

    Google Scholar 

  • Khalifa NO, Elhofy FI, Hanan A, Sobhy MM, Agag M (2016) Seropervelance and Molecular Detection of Coxiella burnetii Infection in Sheep, Goats and Human in Egypt Journal Of Microbiology, Biotechnology And Food Science 2:1–7

    Google Scholar 

  • Khalili M, Diali HG, Mirza HN, Mosavi SM (2015) Detection of Coxiella burnetii by PCR in bulk tank milk samples from dairy caprine herds in southeast of Iran Asian Pacific Journal of Tropical Disease 5:119–122

    Article  CAS  Google Scholar 

  • Khalili M, Naderi HR, Salehnia N, Abiri Z (2016) Detection of Coxiella burnetii in acute undifferentiated febrile illnesses (AUFIs) in Iran Tropical doctor:0049475515624855

  • Khanzadi S, Jamshidi A, Razmyar J, Borji S (2014) Identification of Coxiella burnetii by touch-down PCR assay in unpasteurized milk and dairy products in North-East of Iran Iranian Journal of Veterinary Medicine 8:15–19

    Google Scholar 

  • Kim SG (2005) Coxiella burnetii in Bulk Tank Milk Samples, United States-Emerging Infectious Disease 11:619–621

  • Loftis AD, Priestley RA, Massung RF (2010) Detection of Coxiella burnetii in commercially available raw milk from the United States Foodborne pathogens and disease 7:1453–1456

    Article  PubMed  Google Scholar 

  • Lorestani S, Jaydari A, Maleki S, Khademi P (2016) Genomic detection of Coxiella burnetii in cattle milk samples by Nested-PCR method, Iran Journal of Food Science and Technology 56:165–171

    Google Scholar 

  • Mobarez AM, Amiri FB, Esmaeili S (2017) Seroprevalence of Q fever among human and animal in Iran; A systematic review and meta-analysis PLoS neglected tropical diseases 11:e0005521

    Article  Google Scholar 

  • Mohammed OB et al. (2014) Coxiella burnetii, the causative agent of Q fever in Saudi Arabia: molecular detection from camel and other domestic livestock Asian Pacific Journal of Tropical Medicine 7:715–719

    Article  CAS  Google Scholar 

  • Nasehfar A, Bonyadian M, Boroujeni RK, Esfahani MM, Kazemeini H, Shahraki MM (2015a) Prevalence of Coxiella Burnetii by Nested PCR in Bovine Bulk Milk Samples in Central Zone of Iran American Advances Journal of Biological Sciences 1:10–13

    Google Scholar 

  • Nasehfar A, Bonyadian M, Boroujeni RK, Esfahani MM, Kazemeini H, Shahraki MM (2015b) Real-Time PCR-Based Detection of Coxiella Burnetii in Bovine Bulk Milk Samples in Iran American Advances Journal of Biological Sciences 1:14–17

    Google Scholar 

  • Öngör H, Cetinkaya B, Karahan M, Acik MN, Bulut H, Muz A (2004) Detection of Coxiella burnetii by immunomagnetic separation-PCR in the milk of sheep in Turkey Veterinary record 154:570–572

    Article  PubMed  Google Scholar 

  • Parker NR, Barralet JH, Bell AM (2006) Q fever The Lancet 367:679–688

  • Petruzzelli A, Amagliani G, Micci E, Foglini M, Di Renzo E, Brandi G, Tonucci F (2013) Prevalence assessment of Coxiella burnetii and verocytotoxin-producing Escherichia coli in bovine raw milk through molecular identification Food control 32:532–536

    Article  CAS  Google Scholar 

  • Rahimi E (2014) Detection of Coxiella burnetii in ovine bulk milk samples in Fars, Khuzestan, Ghom and Kerman provinces using PCR assay Veterinary Journal

  • Rahimi E, Doosti A, Ameri M, Kabiri E, Sharifian B (2010) Detection of Coxiella burnetii by nested PCR in bulk milk samples from dairy bovine, ovine, and caprine herds in Iran Zoonoses and public health 57:e38-e41

    Article  CAS  PubMed  Google Scholar 

  • Rahimi E, Ameri M, Karim G, Doosti A (2011) Prevalence of Coxiella burnetii in bulk milk samples from dairy bovine, ovine, caprine, and camel herds in Iran as determined by polymerase chain reaction Foodborne pathogens and disease 8:307–310

    Article  CAS  PubMed  Google Scholar 

  • Rahmde S, Azimzadeh N, Poormontaseri M, Hosseinzadeh S (2014) Prevalence of Q fever in dairy cattle based on bulk-milk analysis, in Shiraz Iranian Journal of Public Health 43:208

  • Raoult D (2012) Chronic Q fever: expert opinion versus literature analysis and consensus Journal of Infection 65:102–108

    Article  PubMed  Google Scholar 

  • Rodolakis A (2009) Q Fever in dairy animals Annals of the New York Academy of Sciences 1166:90–93

  • Rodolakis A et al. (2007) Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds Journal of Dairy Science 90:5352–5360

    Article  CAS  PubMed  Google Scholar 

  • Sargeant J et al. (2016) Methods and processes of developing the Strengthening the Reporting of Observational Studies in Epidemiology–Veterinary (STROBE-Vet) statement Zoonoses and public health 63:651–661

    Article  CAS  PubMed  Google Scholar 

  • Van den Brom R, Van Engelen E, Luttikholt S, Moll L, Van Maanen K, Vellema P (2012) Coxiella burnetii in bulk tank milk samples from dairy goat and dairy sheep farms in The Netherlands in 2008 Veterinary Record 170:310

    Article  PubMed  Google Scholar 

  • Van den Brom R, Van Engelen E, Roest H, van der Hoek W, Vellema P (2015) Coxiella burnetii infections in sheep or goats: an opinionated review Veterinary microbiology 181:119–129

    Article  PubMed  Google Scholar 

  • Van Engelen E, Schotten N, Schimmer B, Hautvast J, Van Schaik G, van Duijnhoven Y (2014) Prevalence and risk factors for Coxiella burnetii (Q fever) in Dutch dairy cattle herds based on bulk tank milk testing Preventive veterinary medicine 117:103–109

    Article  PubMed  Google Scholar 

  • Vandenbroucke JP et al. (2007) Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration PLoS Medicine 4:e297

    Article  PubMed  PubMed Central  Google Scholar 

  • Yaghmaie F, Esmaeili S, Francis SA, Mostafavi E (2015) Q fever endocarditis in Iran: A case report Journal of infection and public health 8:498–501

    Article  PubMed  Google Scholar 

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Acknowledgments

This study has been approved and supported by Tarbiat Modares University. Also, we would like to express our gratitude to Dr Fahimeh Bagheri Amiri (specialist in epidemiology) for her help in study design and data analysis.

Funding

This work was supported financially by Tarbiat Modarres University (Tehran, Iran) as a PhD thesis and Iranian National Scientific Foundation (INSF; Contracted No. 91004716).

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Authors and Affiliations

  1. Department of Bacteriology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

    Saber Esmaeili & Ashraf Mohabati Mobarez

  2. Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

    Mohammad Khalili

  3. Department of Epidemiology and Biostatics, Pasteur Institute of Iran, Tehran, Iran

    Ehsan Mostafavi

  4. National Reference Laboratory of Plague, Tularemia and Q Fever, Research Centre for Emerging and Reemerging Infectious Diseases, Pasteur Institute of Iran, Akanlu, Kabudar-Ahang, Hamadan, Iran

    Ehsan Mostafavi

  5. Rajaie Cardiovascular Medical and Research Center, Iran University of Medical Sciences, Tehran, Iran

    Pardis Moradnejad

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  1. Saber Esmaeili
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  2. Ashraf Mohabati Mobarez
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  3. Mohammad Khalili
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  4. Ehsan Mostafavi
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Correspondence to Ashraf Mohabati Mobarez.

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Esmaeili, S., Mohabati Mobarez, A., Khalili, M. et al. Molecular prevalence of Coxiella burnetii in milk in Iran: a systematic review and meta-analysis. Trop Anim Health Prod 51, 1345–1355 (2019). https://doi.org/10.1007/s11250-019-01807-3

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