Original article
Molecular detection of tick-borne pathogens harbored by ticks collected from livestock in the Xinjiang Uygur Autonomous Region, China

https://doi.org/10.1016/j.ttbdis.2020.101478Get rights and content

Abstract

Ticks carry and transmit a wide range of pathogens (bacteria, viruses, and protozoa) that are of importance to humans and animals globally. However, information about the tick-borne pathogens harbored by ticks in the Xinjiang Uygur Autonomous Region (XUAR), northwestern China, is scarce. This study investigated the occurrence of tick species of domestic animals and tick-borne pathogens by using morphological molecular identification and sequence analysis in Turpan, Qitai, Altay, Hejing, Nileke, and Zhaosu counties (XUAR). A total of 5822 adult ticks (females and males) from 12 tick species were identified from 5 animal species (cattle, goats, sheep, camels, and horses) in 6 counties in the XUAR. Collected tick species included Dermacentor marginatus (24.7 %), Dermacentor nuttalli (20.8 %), Hyalomma anatolicum (13.7 %), Dermacentor niveus (13.1 %), Haemaphysalis punctata (10.7 %), Dermacentor silvarum (7.1 %), Dermacentor pavlovskyi (3.9 %), Hyalomma asiaticum (2.2 %), Rhipicephalus pumilio (1.9 %), Rhipicephalus sanguineus sensu lato (0.7 %), Rhipicephalus turanicus (0.6 %), and Hyalomma asiaticum kozlovi (0.6 %). Furthermore, 750 partially engorged adult ticks (females and males), including H. anatolicum (250), D. nuttalli (250), and D. marginatus (250), were individually separated according to species and sampling site, used for DNA extraction, and then screened for tick-borne pathogens. The most common pathogen was Rickettsia raoultii (36.80 %), followed by Brucella sp. (26.2 %), Anaplasma ovis (22.4 %), Babesia caballi (14.8 %), Theileria equi (8.7 %), and Theileria ovis (8.5 %). The sequencing of 6 genes showed a 96–100 % nucleotide identity between the sequences in this study and those deposited in GenBank. This study provides a scientific reference for the prevention and control of tick-borne diseases in the XUAR.

Introduction

Ticks carry and transmit a wide range of pathogens (bacteria, viruses, and protozoa) that are of importance to humans and animals globally. Furthermore, new pathogens have been identified from ticks (Mansfield et al., 2017; Qin et al., 2014). Therefore, in the temperate zone, ixodid ticks are usually estimated to be the most important vectors of pathogens (Jongejan and Uilenberg, 2004). China has approximately 9.6 million square kilometers of land area. More than 117 tick species, seven genera, and more than 30 emerging tick-borne pathogens (TBPs) have been identified in China (Chen et al., 2010; Fang et al., 2015; Zhuang et al., 2018).

The Xinjiang Uygur Autonomous Region (XUAR) covers one-sixth of China’s land, borders eight countries, and has complex climates, including temperate continental arid, semi-arid, and warm temperate continental arid (Li et al., 2019; Zhang et al., 2016). The XUAR is surrounded by multiple land forms, such as the Gobi Desert, valleys, mountains, grasslands, and plateaus. Additionally, this region is halfway along the old Silk Road between eastern Asia and Europe, so international livestock trade is frequent (Li et al., 2019; Takada et al., 2011). Six tick genera, including Dermacentor, Hyalomma, Rhipicephalus, Haemaphysalis, Ixodes, and Argas, and 14 tick species have been identified in the XUAR. Rhipicephalus turanicus, Dermacentor niveus, Hyalomma asiaticum, and Dermacentor marginatus were identified as dominant (Sheng et al., 2019).

Brucellosis, Lyme borreliosis, Q fever, Crimean–Congo hemorrhagic fever, anaplasmosis, rickettsioses, babesiosis, and theileriosis have been investigated previously in China (Li et al., 2019; Wang et al., 2019; Wu et al., 2013; Yang et al., 2018). Brucellosis agents, namely Brucella melitensis, B. abortus, and B. suis, are common in China (Zhang et al., 2008; Zhong et al., 2011). Wang et al. (2018) also reported that Brucella was detected in adult D. marginatus. Lyme borreliosis is the most common vector-borne infectious disease transmitted by the bite of borrelia-infected ticks (Steere et al., 2016). Wang et al., 2015) reported that Borrelia burgdorferi sensu lato was isolated from adult H. asiaticum, D. marginatus, and Rhipicephalus sanguineus sensu lato in China (Wang et al., 2015). Q fever, a worldwide zoonosis caused by Coxiella burnetii, also appears to be widespread in China (Wu et al., 2013). Nineteen tick species were reported to carry C. burnetii in China (Du, 2016). Crimean-Congo hemorrhagic fever (CCHF), caused by the CCHF virus (CCHFV), is widely distributed in more than 30 countries in Africa, Asia, Eastern Europe, and the Middle East. CCHFV was first discovered in Xinjiang, China, and called Xinjiang hemorrhagic fever in 1965. This disease is highly pathogenic, with a fatality rate of 5–30 %, and has been reported in more than 9 provinces in China (Sun et al., 2014).

In China, six species of Anaplasma, namely Anaplasma marginale, A. ovis, A. phagocytophilum, A. centrale, A. capra, and A. platys, were investigated in animals and 20 tick species (Goff et al., 1993; Hou et al., 2019; Shi et al., 2020; Zhang, 2014). According to Guo et al. (2016), several Rickettsia species, including R. raoultii, R. heilongjiangii, R. sibirica, R. slovaca, R. massiliae, R. conorii, Rickettsia sp. XY99, and R. parkeri, are present in China. However, Rickettsia sibirica sibirica and Rickettsia sp. XY99, which cause tick bite fever in humans, are the most common (Dong et al., 2014; Li et al., 2016).

Equine piroplasmosis (EP; Babesia caballi and Theileria equi), a tick-borne disease of horses, is commonly detected in D. nuttalli, D. silvarum, D. niveus, and H. anatolicum adult ticks in China (Wu et al., 2013; Song et al., 2018b). Like EP, theileriosis of sheep caused by T. ovis has been detected in adult H. anatolicum and H. qinghaiensis ticks (Li et al., 2011; Niu et al., 2009; Shu et al., 2001).

Although several reports have illustrated the characterization or diversity of tick species in the XUAR (Sheng et al., 2019), information about pathogens carried or transmitted by XUAR ticks remains insufficient (Li et al., 2011; Niu et al., 2009; Shu et al., 2001). Therefore, this study was carried out with the objective of characterizing the pathogens carried or transmitted by tick species collected from cattle, goats, sheep, camels, and horses in the XUAR

Section snippets

Tick collection

All of the 5822 ticks (females and males) in this study were collected while they were feeding on asymptomatic healthy animals (cattle, goats, sheep, camels, and horses) that were collected from 6 counties (19 sampling spots) in Xinjiang, China, namely Turpan (GC), Qitai (QT), Altay (AL), Hejing (HJ), Nileke (NL), and Zhaosu (ZS) (Fig. 1a). The microclimate, GPS coordinates, host animals, and altitude of the sampling areas are shown in Supplementary Table 1. Briefly, ticks were collected by

Tick species identification based on morphology

A total of 5822 ticks were collected from cattle (123), sheep (72), horses (113), and camels (10). Identification by morphological observation revealed that the 5822 adult ticks belong to four tick genera, namely Dermacentor, Hyalomma, Rhipicephalus, and Haemaphysalis. Twelve species were identified: Dermacentor marginatus (24.7 %), D. nuttalli (20.8 %), Hyalomma anatolicum (13.7 %), D. niveus (13.1 %), Haemaphysalis punctata (10.7 %), D. silvarum (7.1 %), D. pavlovskyi (3.9 %), H. asiaticum

Discussion

Information on the genetic diversity and transmission of TBPs in hard ticks is limited, especially in the XUAR (Lu et al., 2013). In this study, 12 species of adult ticks collected in 6 counties were investigated via morphological identification, and samples of the three most common ticks were molecularly identified. Then we conducted a pathogen survey of the three most common ticks (H. anatolicum, D. nuttalli, and D. marginatus). Three bacteria and three protozoa with veterinary and/or public

Credit authorship statement

Yongchang Li: Methodology, Validation, Statistical analysis the results, Writing-Original Draft, Writing-Review & Editing. Xiuxiu Wen: Validation, Statistical analysis the results, Writing-Review & Editing. Min Li: Investigation, Writing-Review & Editing. Paul Franck Adjou Moumouni: Developed the project and the study protocol, Edited and revised the manuscript. Eloiza May Galon: Edited and revised the manuscript. Qingyong Guo: Investigation, Recorded samples’ data. Mohamed Abdo Rizk:

Acknowledgments

This study was supported by grants from the Japan Society for the Promotion of Science (JSPS) Core-to-Core Program and the National Natural Science Foundation of China-Regional Science Foundation (31660711). We are grateful to the farmers for their cooperation and the state veterinarians for helping with tick-sample collection in the field.

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