Elsevier

Acta Tropica

Volume 206, June 2020, 105443
Acta Tropica

Coxiella burnetii in camels (Camelus dromedarius) from Algeria: Seroprevalence, molecular characterization, and ticks (Acari: Ixodidae) vectors

https://doi.org/10.1016/j.actatropica.2020.105443Get rights and content

Highlights

  • The high Q fever seroprevalence among camels was associated with: geographic location, age class and season.

  • Camels were low level of Coxiella burnetii in blood, with transient and low level of bacteremia especially in chronic stage of infection.

  • Although the arid conditions, Hyalomma tick species could facilitate the transmission of Coxiella burnetii among dromedary herds.

  • The genotype of Algerian strain clustered with several strains of C. burnetii isolated from ticks, cattle, and human.

Abstract

Q fever is a widespread zoonotic disease caused by Coxiella burnetii that most commonly infects not only a variety of mammals but also arthropods and in particularly ticks. The aim of this study was to detect C. burnetii infection in camels including ixodid ticks using serological and molecular assays. Between July 2018 to June 2019, blood samples from 184 male and female camels (Camelus dromedarius) were collected from 3 regions of South–East Algeria and serum samples were tested for antibodies against Coxiella burnetii using indirect enzyme-linked immunosorbent assay (ELISA) kit. The positive sera and a total of 60 ticks were tested by quantitative PCR (qPCR) for detection of C. burnetii with primers and probes specific to the transposon-like repetitive region (IS1111 gene). Positive samples were genotyped by amplification and sequencing of partial sequences based on the IS1111 gene.

The seroprevalence of antibodies against C. burnetii was 75.5%. Statistical analysis pointed out three potential risk factors associated with Q fever infection: geographic location, age class and season. No positive DNA of camel blood sample was observed. However, five Hyalomma dromedarii, one H. impeltatum and one H. excavatum tick species were detected positive for Coxiella burnetii DNA by qPCR, with an overall prevalence rate of 11.66% (7/60). The revealed Algerian strains by phylogenetic and comparative analysis of the IS1111 nucleotide sequences were clustered with several pathogenic C. burnetii strains isolated from ticks, human, and cattle located in Tunisia, Greece and in some Mediterranean countries, respectively. The study results clearly indicate that camels and their ticks in Algeria may play an important role as a reservoir for C. burnetii and can be considered as a significant source of Q fever transmission to other animal species and humans.

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.

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