Coxiella burnetii in camels (Camelus dromedarius) from Algeria: Seroprevalence, molecular characterization, and ticks (Acari: Ixodidae) vectors
Introduction
The world population of dromedary camel is about 30 million, with highest numbers in Africa and the Middle East. The camels are common in arid areas as beasts of load and production animals for meat and milk. Several infectious diseases are known to affect camels. Consequently, a consumption and contact with these camels represent a significant point source or vector for zoonotic disease transmission to humans and other animals (Zhu et al., 2019).
Coxiella burnetii, the causative agent of Q fever, is a zoonotic and strictly intracellular bacterium that belongs to the gamma subdivision of Proteobacteria in the Order of Legionellales and Coxiellaceae family (Bielawska-Drozd et al., 2013). Human infection most frequently occurs from inhalation of contaminated aerosols, through direct contact with milk, urine, feces, amniotic fluid or aborted tissues, or semen of infected animals, and tick bites (Anderson et al., 2013). A wide variety of vertebrate and invertebrate hosts can be infected with C. burnetii including wild and domestic mammals, marine mammals, birds, reptiles and arthropods (Babudieri, 1959). Among mammals, cattle, sheep and goats are the main reservoirs and frequent source of human infection by C. burnetii (Eldin et al., 2017). However, any infected animal has the potential to transmit the pathogen (Janati et al., 2015; Vanderburg et al., 2014), as suggested by Vanderburg et al. (2014) that contact with camels was associated with human Q fever across Africa. Coxiella burnetii is among the most widespread zoonotic pathogens infectious in camels (Hussein et al., 2015). Very high prevalence of Q fever antibodies was reported in the sera of camels from almost all parts of the Middle East, North and East Africa (Selmi et al., 2018; Zhu et al., 2019). Only few serological data for seroprevalence of Q fever are available regarding camel populations in Algeria (Benaissa et al., 2017) since most investigations have focused on sheep, goats and cows (Agag et al., 2016; Derdour et al., 2017; Khaled et al., 2016; Menadi et al., 2019; Rahal et al., 2018).
Coxiella burnetii has been isolated in more than 40 hard and at least 14 soft tick species, suggesting that these arthropods play a role in the transmission of the bacterium (Eldin et al., 2017). In addition, ticks are considered the natural primary reservoirs of C. burnetii as they maintain the infection in domestic animals (Norlander, 2000). Ticks can transmit C. burnetii by bite or exposure to infected excreta expelled by ticks onto the skin of the animal host at the time of feeding (Babudieri, 1959; Hartzell et al., 2008; Norlander, 2000; Oyston et al., 2011). Also, most soft and hard ticks transmit C. burnetii transstadially and transovarially to their offspring (Babudieri, 1959; Balashov et al., 1973). Thus, it has been suggested that there is an increase in the virulence of C. burnetii after passage through ticks (Cutler et al., 2007). Coxiella burnetii multiplies in the gut or stomach of ticks, resulting in heavy loads of viable organisms that are excreted with feces, saliva and coxal fluid (Maurin et al., 1999; Norlander, 2000) which in turn play an important role in the spread of C. burnetii in the environment (Mediannikov et al., 2010).
The molecular epidemiology of C. burnetii from different bioclimatic areas of Algeria has been rarely investigated in animals (particularly from camels) and their infesting ticks (Abdelkadir et al., 2019; Leulmi et al., 2016). Therefore, the aims of this study were detection and genetic characterization of the C. burnetii strain occurring in blood and ticks harvested in camels from Algeria.
Section snippets
Study area
This study was conducted from three provinces (Ouargla, El Oued and Biskra) located at 33°31′41.88″ N 4°36´11.05″ (Fig. 1). These provinces have been classified as arid areas characterized by long, hot summers and short winters. Camels in these regions are a livestock intended for the production of meat and milk, as well as for transportation of supplies and people. In addition, these provinces are considered one of the most significant camel rearing areas in Algeria with increasingly trade
Seroprevalence of C. burnetii by enzyme-linked immunosorbent assays (ELISA)
The 184 collected sera were tested for IgG antibodies against Coxiella burnetii using ELISA. The seroprevalence of antibodies against C. burnetii was (75.54%). Geographic location (P = 0.045), age class (P<0.001) and season (P = 0.011) positively correlated with increased risk of Q fever infection (Table 1).
Significant difference was noted according to geographic location. The highest prevalence rates in camels were 90% for Biskra compared to 84.6% and 65.7% for Ouargla and El Oued,
Discussion
In the present survey, the overall seroprevalence was determined to be 75.54% among camels. These results are in agreement to those obtained in the same regions (71.2%) by Benaissa et al. (2017). Other camel serological investigations carried out in some African and Asian countries, including Egypt, Iran, Kenya, Tunisia, Saudi Arabia, Chad and Ethiopia, ranged from 16% to 90% (Browne et al., 2017; Hussein et al., 2008, 2015; Janati et al., 2015; Jarelnabi et al., 2018; Klemmer et al., 2018;
CRediT authorship contribution statement
Meriem Bellabidi: Investigation, Methodology, Formal analysis, Resources, Validation, Writing - original draft, Writing - review & editing. Mohammed Hocine Benaissa: Investigation, Methodology, Formal analysis, Resources, Validation, Writing - original draft, Writing - review & editing. Samia Bissati-Bouafia: Writing - original draft. Zoubir Harrat: Resources, Writing - original draft. Karima Brahmi: Conceptualization, Resources, Writing - original draft. Tahar Kernif: Conceptualization,
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We would like to thank Dr. Felix Mba Medie for English correction, Division of Infectious Diseases, Department of Medicine, Duke University School of Medicine, Durham, North Carolina, United States of America.
References (53)
- et al.
Presence of Rickettsia aeschlimannii, 'Candidatus Rickettsia barbariae' and Coxiella burnetii in ticks from livestock in northwestern Algeria
Ticks Tick-borne. Dis.
(2019) - et al.
Q fever
J Infect
(2007) - et al.
Population dynamics of ticks infesting the one-humped camel (Camelus dromedarius) in central Tunisia
Ticks Tick-borne. Dis.
(2013) - et al.
Q fever: epidemiology, diagnosis, and treatment
Mayo Clin. Proc.
(2008) - et al.
Vector-borne rickettsioses in North Africa
Infect. Dis. Clin North Am.
(2012) - et al.
Serological and molecular evidence of q fever among small ruminant flocks in Algeria
Comput. Immunol. Microbiol. Infect. Dis.
(2016) - et al.
Coxiella burnetii, the causative agent of Q fever in Saudi Arabia: molecular detection from camel and other domestic livestock
Asian Pac. J. Trop. Med.
(2014) Q fever epidemiology and pathogenesis
Microb. Infect.
(2000)- et al.
Diagnosis of Coxiella burnetii-related abortion in Italian domestic ruminants using single-tube nested PCR
Vet. Microbiol.
(2006) - et al.
Genotyping of Coxiella burnetii detected in placental tissues from aborted dairy cattle in the north of Algeria
Comp Immunol. Microbiol. Infect. Dis.
(2018)
Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in CHAD
Prev. Vet. Med.
Molecular detection and genetic characterization of the potentially pathogenic Coxiella burnetii and the endosymbiotic candidatus Midichloria mitochondrii in ticks infesting camels (Camelus dromedarius) from Tunisia
Microb. Pathog.
Coxiella burnetii in Tunisian dromedary camels (Camelus dromedarius): seroprevalence, associated risk factors and seasonal dynamics
Acta Trop.
Impact of IS1111 insertion on the MLVA genotyping of Coxiella burnetii
Microb. Infect.
Molecular and immunological characterization of Hyalomma dromedarii and Hyalomma excavatum (Acari: Ixodidae) vectors of Q fever in camels
Vet. World
Seroprevalence of Q fever in cows in Bejaia area (Algeria)
Rev. Elev. Med. Vet. Pays Trop.
Diagnosis and management of Q fever–United States, 2013: recommendations from CDC and the Q fever working group
MMWR Recomm. Rep
The genus Hyalomma: VII. Redescription of all parasitic stages of H. (Euhyalomma) dromedarii and H. (E.) schulzei (Acari: Ixodidae)
J. Med. Entomol.
Q fever: a zoonosis
Adv. Vet. Sci.
Bloodsucking arthropods and rickettsiae
Sci. Leningr
Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters
J. Parasitol.
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.
Q fever–selected issues
Ann Agric. Environ. Med
Study of Ixodidae on camels in southwest Algeria, Adrar region [in French]
Ann. Méd. Vét.
Serosurvey of Coxiella burnetii (Q fever) in dromedary camels (Camelus dromedarius) in Laikipia county
Kenya. Zoonoses. Public Health
Prevalence of the main infectious causes of abortion in dairy cattle in algeria
J. Vet. Res.
Cited by (27)
Molecular detection and MST genotyping of Coxiella burnetii in ruminants and stray dogs and cats in Northern Algeria
2024, Comparative Immunology, Microbiology and Infectious DiseasesTick-borne pathogens in camels: A systematic review and meta-analysis of the prevalence in dromedaries
2024, Ticks and Tick-borne DiseasesCoxiella and Q fever
2023, Molecular Medical Microbiology, Third EditionSeroprevalence of Q fever among ewes and associated risk factors in Ain Defla region, North-central Algeria
2022, Comparative Immunology, Microbiology and Infectious DiseasesCitation Excerpt :ELISA, IFA, or CFT can be used, but ELISA methods are recommended to detect antibodies against C. burnetii in animals [3]. To date, very limited studies on the seroprevalence of Q fever in animals have been carried out in Algeria: small ruminants [10–14], cattle [15–17], camels [18,19] and horses [20]. Moreover, to the best of our knowledge, there is no epidemiological data on Q fever in the province of Ain Defla.