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Molecular evidence of tick-borne hemoprotozoan-parasites (Theileria ovis and Babesia ovis) and bacteria in ticks and blood from small ruminants in Northern Algeria

https://doi.org/10.1016/j.cimid.2016.11.008Get rights and content

Highlights

Abstract

Using qPCR, standard PCR and/or sequencing, we investigated the presence of tick-associated microorganisms in ticks and blood from sheep and goats from Souk Ahras, Algeria.

Borrelia theileri, was detected in (7/120, 5.8%) blood from sheep and (13/120, 10.8%) goats. Anaplasma ovis was screened in (38/73, 52%) Rhipicephalus bursa and (5/22, 22.7%) R. turanicus and in (74/120, 61.7%), (65/120, 54.2%) blood of sheep and goats respectively.

Coxiella burnetii tested positive in R. bursa (4/73, 5.5%) and (7/120, 5.8%) blood of sheep and (2/120, 1.7%) goats. Theileria ovis was detected in (50/147, 34%) R. bursa and (3/22, 13.6%) R. turanicus and in (64/120, 53.3%) blood of sheep and (25/120, 20.8%) goats. Babesia ovis was screened positive in (23/147, 15.6%) R. bursa and (7/48, 14.6%) R. turanicus.

Our findings expand knowledge about the repertoire of tick-borne microorganisms present in ectoparasites and/or the blood of small ruminants in Algeria.

Introduction

Small ruminants are an important source of meat and milk in Algeria and play a vital role in food security. Sheep predominate, at around 80% of total livestock. They are amongst the major economically important livestock in Algeria with about 27 million head in 2014 [1], [2]. Goat populations also play an important role in the livelihood of resource-poor farmers and represent around 4 million head [2]. Sheep and goats are exposed to several health problems and their productivity is thought to be greatly reduced due to infectious diseases and parasitic diseases [2], [3], [4], [5].

Vector-borne diseases represent a large proportion of these infectious diseases, which are caused by a multitude of pathogens transmitted by arthropod vectors [6]. Ticks were the first arthropods to be established as vectors of pathogens [7] that can transmit them to humans [8]. They are considered to be the second biggest vectors of pathogens after mosquitoes [9] and the most important vectors of disease-causing pathogens in animals [10]. There are about 900 species of ticks described so far [11], most of which are responsible for the transmission of a huge variety of micro-organisms, including viruses, bacteria and parasites [12].

Theileria spp. and Babesia spp., the causative agents of theileriosis and babesiosis, respectively, are among the most economically important hemoparasitic tick-borne diseases in ruminants worldwide [13]. In the past, most attention has been given to bovine-infecting piroplasmosis, and most tick-borne diseases in small ruminants have received less consideration [14]. However, because of the socio-economic impact in a number of countries, interest has recently increased in sheep and goat piroplasmosis [14]. The Theileria species infecting small ruminants are Theileria ovis, T. lestoquardi, T. luwenshuni, T. uilenbergi, T. recondita and T. separata [15], [16]. Small ruminants are also affected by Babesia ovis, B. motasi, B. crassa, B. foliata, B. taylori, Babesia sp. (China) and Babesia sp. (Xinjiang) [17].

Likewise, a vast number of tick-related bacteria have been identified in the past 25 years [18], including borrelioses [19], anaplasmosis [20], Q fever [21] and tick-borne rickettsial diseases [18]. In recent years, the prevalence of tick-borne bacterial diseases has dramatically increased and emerged throughout the world [22].

Spirochaete Borrelia theileri has been identified in the blood of various domestic mammals including ongulates, mainly cattle and small ruminants in tropical and subtropical regions of Africa, where the genus Boophilus (Rhipicephalus) was recognized as vector [23]. The clinical signs of infection in ruminants and other animals remain mild and variable, but usually include fever and anemia [24].

Anaplasma ovis is an erythrocytic anaplasma that parasitizes red blood cells [25] and may cause mild to severe disease in sheep and other ruminants [26]. A. ovis is transmitted primarily by Rhipicephalus bursa ticks [27].

In addition, Coxiella burnetii, the causative agent of Q fever, is recognized as a worldwide highly infectious zoonotic intracellular bacterium [28]. C. burnetii is able to infect various species of domestic mammals, including small ruminants and humans [29].

In this study, we aimed to update the occurrence and repertoire of tick-borne parasitic and bacterial diseases in Algeria by using molecular-based methods.

Section snippets

Study areas, tick collection and blood sampling

This cross-sectional study was carried out on ticks and blood from sheep and goats on 12 sites (Table 1) through the province of Souk Ahras in the Northeastern of Algeria, (36° 17′ 15″ N 7° 57′ 15″ E). Souk Ahras is surrounded by wooded mountains and is ​​1000 m above sea level. It is an extension of the Telli Atlas mountains. It has a semi-humid climate characterized by a hot summer and a cold, wet winter with rainfall averaging 850 mm per year, the bulk of which is seen between October and

Tick identification and sample collection

A total of 910 ticks were collected from sheep (627/910, 68.9%) and goats (283/910, 31.1%) from the province of Souk Ahras. Two tick species were identified among overall collected ticks: Rhipicephalus bursa (545/627, 86.9%) and Rhipicephalus turanicus (82/627, 13.1%), collected from 120 sheep and R. bursa (262/283, 92.6%) and R. turanicus (21/283, 7.4%), collected from 120 goats. From all the ticks collected, a convenient sample of 95 ticks sampled on sheep (73 R. bursa and 22 R. turanicus)

Discussion

This investigation reports the first direct evidence of tick-borne haemoprotozoan-parasites (Theileria ovis and Babesia ovis) and bacteria (Anaplasma ovis, Borrelia theileri and Coxiella burnetii) in ticks (R. bursa and/or R. turanicus) and blood from small ruminants (sheep and goats) in Souk Ahras, Northern Algeria.

In our study, the presence of DNA from pathogens in ticks and blood collected from small ruminants was screened using a validated method consisting of double qPCR assays and/or

Conflict of interests

The authors declared that they have no competing interests.

Authors' contributions

AA contributed to arthropod and blood collections, performed DNA extractions, qPCRs, sequencing and first drafted the paper. HL helped with the experiments, contributed to the manuscript, analyzed the data, coordinated the study and identified arthropods. AB contributed to conceiving, designing and coordinating the study. DR Contributed reagents/materials/analysis tools and analyzed the data. PP conceived, designed and coordinated experiments. All authors read and approved the final manuscript.

Acknowledgements

This work was carried out thanks to the support of the A*MIDEX project (no. ANR-11-IDEX-0001-02) funded by the French Government’s “Investissements d’Avenir” program, managed by the French National Research Agency (ANR).

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