Coxiella burnetii and Borrelia spp. in peripheral blood of dromedary camels in Fars, Iran: molecular characterization, hematological parameters, and acute-phase protein alterations

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Veterinary Clinical Pathology, Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

2 Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

3 Department of Food Hygiene and Public Health, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

Abstract

Background: Dromedary camels (Camelus dromedarius) are raised in extremely strict ecological conditions of deserts. Camels are vulnerable to many zoonotic infections. There are limited data on the occurrence of Q fever and borreliosis in camels, in Iran. Aims: The current study was focused on the occurrence of Coxiella burnetii and Borrelia spp. infection in the blood samples of Iranian camels using molecular assays. Effect of the presence of these infections on various hematological factors and some acute-phase proteins (Hp, a1AGP, SAA) were also investigated. Methods: Blood samples were collected from 113 clinically healthy camels to investigate the presence of the infections using nested PCR. Moreover, the sequence of positive samples was analyzed phylogenetically. Routine haematological tests were performed and the concentrations of acute-phase proteins were measured in serum using enzyme immunoassay. Results: PCR result showed that 6.19% (95% CI: 2.53-12.35%) (7/113) of camels were positive for C. burnetii. In addition, sequencing results of the corresponding gene of the outer membrane protein (com1) revealed two different genotypes of C. burnetii agent in camels from Southern Iran. In the PCR assay, Borrelia spp. DNA was not detected in the samples. No significant difference was observed in hematological parameters or acute-phase proteins between positive and negative Q fever camels except for mean corpuscular hemoglobin (MCH) and red cell distribution width (RDW). Conclusion: Clinically healthy camels might be very important reservoirs of zoonotic pathogens. Q fever is not considered a notifiable disease in camels of Iran, and clinical cases may scarcely be recognized by the healthcare system. Due to a lack of adequate information, additional studies on the molecular epidemiology and clinical pathology aspects of C. burnetii infection in Iran are needed.

Keywords


Abdali, F; Hosseinzadeh, S; Berizi, E and Shams, S (2018). Prevalence of Coxiella burnetii in unpasteurized dairy products using nested PCR assay. Iran. J. Microbiol., 10: 220-226.
Abdullah, HHAM; Hussein, HA; El-Razik, KhAA; Barakat, AMA and Soliman, YA (2019). Q fever: A neglected disease of camels in Giza and Cairo Provinces, Egypt. Vet. World. 12: 1945-1950.
Afzal, M and Sakkir, M (1994). Survey of antibodies against various infectious disease agents in racing camels in Abu Dhabi, United Arab Emirates. Rev. Sci. Tech. OIE., 13: 787-792.
Alanazi, AD; Abdullah, S; Helps, C; Wall, R; Puschendorf, R; ALHarbi, SA; Abdel-Shafy, S and Shaapan, RM (2018). Tick-borne pathogens in ticks and blood samples collected from camels in Riyadh province, Saudi Arabia. Int. J. Zool. Res., 14: 30-36.
Ali, SF; Ibrahim, EM and Jake, JEl (2016). Molecular and serological studies on Coxiella burnetii in camels at Marsa Matrouh governorate in Egypt. J. Am. Sci., 12: 77-82.
Bahari, AA; Azami, S; Goudarztalejerdi, A; Karimi, S; Esmaeili, S; Chomel, BB and Sazmand, AR (2021). Focus: zoonotic disease: molecular detection of zoonotic pathogens in the blood and tissues of camels (Camelus dromedarius) in Central Desert of Iran. Yale J. Biol. Med., 94: 249-258.
Barlozzari, G; Sala, M; Iacoponi, F; Volpi, C; Polinori, N; Rombolà, P; Vairo, F; Macrì, G and Scarpulla, M (2020). Cross-sectional serosurvey of Coxiella burnetii in healthy cattle and sheep from extensive grazing system in central Italy. Epidemiol. Infect., 148: 1-8.
Benaissa, MH; Ansel, S; Mohamed-Cherif, A; Benfodil, K; Khelef, D; Youngs, CR and Ait-Oudhia, K (2017). Seroprevalence and risk factors for Coxiella burnetii, the causative agent of Q fever in the dromedary camel (Camelus dromedarius) population in Algeria. Onderstepoort J. Vet. Res., 84: 1-7.
Bunikis, J; Garpmo, U; Tsao, J; Berglund, J; Fish, D and Barbour, AG (2004). Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology. 150: 1741-1755.
CDC (The Centers for Disease Control and Prevention) (2022). Lyme disease, Why is CDC concerned about Lyme disease?. https://www.cdc.gov/lyme/why-is-cdc-concerned-about-lyme-disease.html.
Devaux, CA; Omar Osman, I; Million, M and Raoult, D (2020). Coxiella burnetii in dromedary camels (Camelus dromedarius): A possible threat for humans and livestock in North Africa and the Near and Middle East?. Front. Vet. Sci., 7: e 558481.
Doosti, A; Arshi, A and Sadeghi, M (2014). Investigation of Coxiella burnetii in Iranian camels. Comp. Clin. Path., 23: 43-46.
Eckstein, S; Ehmann, R; Gritli, A; Rhaiem, MB; Yahia, HB; Diehl, M; Wölfel, R; Handrick, S; Moussa, MB and Stoecker, K (2022). Viral and bacterial zoonotic agents in dromedary camels from Southern Tunisia: A sero-prevalence study. Microorganisms. 10: e727.
El Tigani Ahmed, ETA; Blanda, V; Abdelwahab, GE; Hammadi, ZMA; Habeeba, S; Khalafalla, AI; Alhosani, MA; La Russa, F; Migliore, S; Torina, A; Loria, GR and Al Muhairi, SS (2021). Molecular investigation on tick-borne hemoparasites and Coxiella burnetii in dromedary camels (Camelus dromedarius) in Al Dhafra Region of Abu Dhabi, UAE. Animals. 11: e666.
Erbas, G; Parin, U; Kirkan, S; Savasan, S; Yüksel, HT and Balat, G (2018). Molecular identification of tick-borne zoonotic bacteria in one humped camel (Camelus dromedarius). J. Camel Pract. Res., 25: 89-92.
Gagaoua, M; Dib, AL and Bererhi, EH (2022). Recent advances in dromedary camels and their products. Animals. 12: e162.
Ghaemi, M; Sharifiyazdi, H; Heidari, F; Nazifi, S and Ghane, M (2019). ‘Candidatus Bartonella dromedarii’ in the dromedary camels of Iran: Molecular investigation, phylogenetic analysis, hematological findings, and acute-phase proteins quantitation. Vet. Microbiol., 237: e108404.
Gumi, B; Firdessa, R; Yamuah, L; Sori, T; Tolosa, T; Aseffa, A; Zinsstag, J and Schelling, E (2013). Seroprevalence of brucellosis and Q-fever in Southeast Ethiopian pastoral livestock. J. Vet. Sci. Med. Diagn., 2: e4172.
Hassani, M (2021). Camel abortion status in Iran-A mini review. SVU Int. J. Vet. Sci., 4: 19-24.
Helmy, N (2000). Seasonal abundance of Ornithodoros (O.) savignyi and prevalence of infection with Borrelia spirochetes in Egypt. J. Egypt. Soc. Parasitol., 30: 607-619.
Heydari, AA; Mostafavi, E; Heidari, M; Latifian, M and Esmaeili, S (2021). Q fever endocarditis in Northeast Iran. Case Rep. Infect. Dis., 28: e5519164.
Holloway, P; Gibson, M; Nash, S; Holloway, T; Cardwell, J; Abu Basha, E; Al Omari, B; Mangtani, P and Guitian, J (2022). A cross-sectional study of Q fever in camels: risk factors for infection, the role of small ruminants and public health implications for desert-dwelling pastoral communities. Zoonoses Public Hlth., 70: 238-247.
Horton, KC; Wasfy, M; Samaha, H; Abdel-Rahman, B; Safwat, S; Abdel Fadeel, M; Mohareb, E and Dueger, E (2014). Serosurvey for zoonotic viral and bacterial pathogens among slaughtered livestock in Egypt. Vector Borne Zoonot., 14: 633-639.
Hussain, S; Saqib, M; Ashfaq, K and Sindhu, Z (2022). Effect of subclinical coxiellosis (Q fever) on selected hematological and serum biochemical variables of naturally infected camels. Pakistan. J. Zool., 54: 2623-2627.
Hussain, S; Saqib, M; El-Adawy, H; Hussain, MH; Jamil, T; Sajid, MS; Alvi, MA; Ghafoor, M; Tayyab, MH and Abbas, Z (2022). Seroprevalence and molecular evidence of Coxiella burnetii in dromedary camels of Pakistan. Front. Vet. Sci., 9: e908479.
Hussein, MF; Alshaikh, MA; Al-Jumaah, RS; GarelNabi, A; Al-Khalifa, I and Mohammed, OB (2015). The Arabian camel (Camelus dromedarius) as a major reservoir of Q fever in Saudi Arabia. Comp. Clin. Path., 24: 887-892.
Hussein, MF; Alshaikh, M; El-Rab, MO; Aljumaah, RS; El Nabi, AR and Bagi, AM (2008). Serological prevalence of Q fever and chlamydiosis in camels in Saudi Arabia. J. Anim. Vet. Adv., 7: 685-688.
Janati, MH; Mohammadi, GH; Mejrzad, J and Azizzadeh, M (2017). Investigation of Coxiella burnetii infection in camel population of northeast of Iran with qPCR. J. Appl. Anim. Res., 6: 9-14.
Janati Pirouz, H; Mohammadi, G; Mehrzad, J; Azizzadeh, M and Nazem Shirazi, MH (2015). Seroepidemiology of Q fever in one-humped camel population in northeast Iran. Trop. Anim. Health Prod., 47: 1293-1298.
Jarelnabi, AA; Alshaikh, MA; Bakhiet, AO; Omer, SA; Aljumaah, RS; Harkiss, GD; Mohammed, OB and Hussein, MF (2018). Seroprevalence of Q fever in farm animals in Saudi Arabia. Biomed. Res., 29: 895-900.
Khalili, M; Naderi, HR; Salehnia, N and Abiri, Z (2016). Detection of Coxiella burnetii in acute undifferentiated febrile illnesses (AUFIs) in Iran. Trop. Doct., 46: 221-224.
Khoobdel, M; Jafari, A; Telmadarraiy, Z; Sedaghat, M and Bakhshi, H (2021). Tick-borne pathogens in Iran: A meta-analysis. Asian Pac. J. Trop. Med., 14: 486-504.
Li, K; Luo, H and Shahzad, M (2018). Epidemiology of Q-fever in goats in Hubei province of China. Trop. Anim. Health Prod., 50: 1395-1398.
Mentaberre, G; Gutiérrez, C; Rodríguez, NF; Joseph, S; González-Barrio, D; Cabezón, O; de la Fuente, J; Gortazar, C and Boadella, M (2013). A transversal study on antibodies against selected pathogens in dromedary camels in the Canary Islands, Spain. Vet. Microbiol., 167: 468-473.
Mohabbati Mobarez, A; Bagheri Amiri, F and Esmaeili, S (2017). Seroprevalence of Q fever among human and animal in Iran: A systematic review and meta-analysis. PLoS Neglect. Trop. Dis., 11: e0005521.
Mohammadpour, R; Champour, M; Tuteja, F and Mostafavi, E (2020). Zoonotic implications of camel diseases in Iran. Vet. Med. Sci., 6: 359-381.
Mohammed, OB; Jarelnabi, AA; Aljumaah, RS; Alshaikh, MA; Bakhiet, AO; Omer, SA; Alagaili, AN and Hussein, MF (2014). Coxiella burnetii, the causative agent of Q fever in Saudi Arabia: molecular detection from camel and other domestic livestock. Asian Pac. J. Trop. Med., 7: 715-719.
Moradnejad, P; Esmaeili, S; Maleki, M; Sadeghpour, A; Kamali, M; Rohani, M; Ghasemi, A; Bagheri Amiri, F; Pasha, HR; Boudagh, S; Bakhshandeh, H; Naderi, N; Ghadrdoost, B; Lotfian, S; Dehghan Manshadi, SA and Mostafavi, E (2019). Q fever endocarditis in Iran. Sci. Rep., 9: e15276.
Muema, J; Nyamai, M; Wheelhouse, N; Njuguna, J; Jost, C; Oyugi, J; Bukania, Z; Oboge, H; Ogoti, B and Makori, A (2022). Endemicity of Coxiella Burnetii infection among people and their livestock in pastoral communities in Northern Kenya. Heliyon. 8: e11133.
Nokhodian, Z; Ataei, B; Feizi, A; Moradi, A; Yaran, M and Ghaffari Hoseini, S (2018). Detection of Coxiella burnetii and risk factors for infection in ruminants in a central county of Iran. Vet. Microbiol., 222: 7-10.
Rahimi, E; Doosti, A; Ameri, M; Kabiri, E and Sharifian, B (2010). Detection of Coxiella burnetii by nested PCR in bulk milk samples from dairy bovine, ovine, and caprine herds in Iran. Zoonoses Public Hlth., 57: e38-e41.
Reza, N; Durrani, AZ; Saleem, MH; Sheikh, AA; Usman, M; Mujahid, Q; Iqbal, MZ and Rizwan, M (2021). Seroprevalence of Borrelia burgdorferi sensu lato in camel (Camelus dromedarius) in Punjab, Pakistan. Pakistan. J. Zool., 64: e1987.
Ruiz-Fons, F; González-Barrio, D; Aguilar-Ríos, F; Soler, AJ; Garde, JJ; Gortázar, C and Fernández-Santos, MR (2014). Infectious pathogens potentially transmitted by semen of the black variety of the Manchega sheep breed: Health constraints for conservation purposes. Anim. Reprod. Sci., 149: 152-157.
Sazmand, A; Harl, J; Eigner, B; Hodžić, A; Beck, R; Hekmatimoghaddam, S; Mirzaei, M; Fuehrer, HP and
Joachim, A
(2019). Vector-borne bacteria in blood of camels in Iran: new data and literature review. Comp. Immunol. Microbiol. Infect. Dis., 65: 48-53.
Schelling, E; Diguimbaye, C; Daoud, S; Nicolet, J; Boerlin, P; Tanner, M and Zinsstag, J (2003). Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in Chad. Prev. Vet. Med., 61: 279-293.
Selmi, R; Mamlouk, A; Ben Yahia, H; Abdelaali, H; Ben Said, M; Sellami, K; Daaloul-Jedidi, M; Jemli, MH and Messadi, L (2018). Coxiella burnetii in Tunisian dromedary camels (Camelus dromedarius): Sero-prevalence, associated risk factors and seasonal dynamics. Acta Trop., 188: 234-239.
Usman, M; Durrani, AZ; Mehmood, N; Saleem, MH and Chaudhry, M (2022). Prevalence of Borrelia burgdorferi sensu lato in pet dogs and associated ticks in Pakistan. Pakistan. J. Zool., 50: 1-10.
Weck, BC; Serpa, MCA; Labruna, MB and Muñoz-Leal, S (2022). A novel genospecies of Borrelia burgdorferi sensu lato associated with cricetid rodents in Brazil. Microorganisms. 10: e204.
Woldehiwet, Z (2004). Q fever (coxiellosis): epidemiology and pathogenesis. Res. Vet. Sci., 77: 93-100.
Zhai, B; Niu, Q; Liu, Z; Yang, J; Pan, Y; Li, Y; Zhao, H; Luo, H and Yin, H (2018). First detection and molecular identification of Borrelia species in Bactrian camel (Camelus bactrianus) from Northwest China. Infect. Genet. Evol., 64: 149-155.
Zhang, GQ; Nguyen, SV; To, H; Ogawa, M; Hotta, A; Yamaguchi, T; Kim, HJ; Fukushi, H and Hirai, K (1998). Clinical evaluation of a new PCR assay for detection of Coxiella burnetii in human serum samples. J. Clin. Microbiol., 36: 77-80.