First molecular survey of tick-borne protozoan and bacterial pathogens in the questing tick population in Bangladesh

Uday Kumar Mohanta; S M Abdullah; Al-Wasef; Boniface Chikufenji; Zhuowei Ma; Hang Li; Shimaa Abd El-Salam El-Sayed; Moaz M Amer; Thanh Thom Do; Saiful Islam; Tilak Chandra Nath; Yongchang Li; Rika Umemiya-Shirafuji; Qingyong Guo; Xuenan Xuan

doi:10.1016/j.actatropica.2024.107244

First molecular survey of tick-borne protozoan and bacterial pathogens in the questing tick population in Bangladesh

Acta Trop. 2024 May 18:256:107244. doi: 10.1016/j.actatropica.2024.107244. Online ahead of print.

Authors

Affiliations

¹ National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080‒8555, Hokkaido, Japan; Department of Microbiology and Parasitology, Sher‒e‒Bangla Agricultural University, Sher‒e‒Bangla Nagar, Dhaka, 1207, Bangladesh.
² Department of Microbiology and Parasitology, Sher‒e‒Bangla Agricultural University, Sher‒e‒Bangla Nagar, Dhaka, 1207, Bangladesh.
³ National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080‒8555, Hokkaido, Japan.
⁴ National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080‒8555, Hokkaido, Japan; Department of Biochemistry and Chemistry of Nutrition, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.
⁵ Department of Parasitology, Sylhet Agricultural University, Tilagor, Sylhet, 3100, Bangladesh.
⁶ National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080‒8555, Hokkaido, Japan; Laboratory of Parasitology, College of Veterinary Medicine, Xinjiang Agricultural University, Urumqi 830011, Xinjiang, PR China.
⁷ Laboratory of Parasitology, College of Veterinary Medicine, Xinjiang Agricultural University, Urumqi 830011, Xinjiang, PR China.
⁸ National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro 080‒8555, Hokkaido, Japan. Electronic address: gen@obihiro.ac.jp.

PMID: 38762942
DOI: 10.1016/j.actatropica.2024.107244

Abstract

Questing ticks carry various tick-borne pathogens (TBPs) that are responsible for causing tick-borne diseases (TBDs) in humans and animals around the globe, especially in the tropics and sub-tropics. Information on the distribution of ticks and TBPs in a specific geography is crucial for the formulation of mitigation measures against TBDs. Therefore, this study aimed to survey the TBPs in the questing tick population in Bangladesh. A total of 2748 questing hard ticks were collected from the pastures in Sylhet, Bandarban, Sirajganj, Dhaka, and Mymensingh districts through the flagging method. After morphological identification, the ticks were grouped into 142 pools based on their species, sexes, life stages, and collection sites. The genomic DNA extracted from tick specimens was screened for 14 pathogens, namely Babesia bigemina (AMA-1), Babesia bovis (RAP-1), Babesia naoakii (AMA-1), Babesia ovis (18S rRNA), Theileria luwenshuni (18S rRNA), Theileria annulata (Tams-1), Theileria orientalis (MPSP), Anaplasma marginale (groEL), Anaplasma phagocytophilum (16S rRNA), Anaplasma bovis (16S rRNA), Anaplasma platys (16S rRNA), Ehrlichia spp. (16S rRNA), Rickettsia spp. (gltA), and Borrelia (Bo.) spp. (flagellin B) using genus and species-specific polymerase chain reaction (PCR) assays. The prevalence of the detected pathogens was calculated using the maximum likelihood method (MLE) with 95 % confidence interval (CI). Among 2748 ixodid ticks, 2332 (84.86 %) and 416 (15.14 %) were identified as Haemaphysalis bispinosa and Rhipicephalus microplus, respectively. Haemaphysalis bispinosa was found to carry all the seven detected pathogens, while larvae of R. microplus were found to carry only Bo. theileri. Among the TBPs, the highest detection rate was observed in A. bovis (20/142 pools, 0.81 %, CI: 0.51-1.20), followed by T. orientalis (19/142 pools, 0.72 %, CI: 0.44-1.09), T. luwenshuni (9/142 pools, 0.34 %, CI: 0.16-0.62), B. ovis (4/142 pools, 0.15 %, CI: 0.05 - 0.34) and Bo. theileri (4/142 pools, 0.15 %, CI: 0.05-0.34), Ehrlichia ewingii (3/142 pools, 0.11 %, CI: 0.03-0.29), and Babesia bigemina (1/142, 0.04 %, CI: 0.00 - 0.16). This study reports the existence of T. luwenshuni, E. ewingii, and Bo. theileri in Bangladesh for the first time. The novel findings of this study are the foremost documentation of transovarian transmission of B. bigemina and E. ewingii in H. bispinosa and also provide primary molecular evidence on the presence of E. ewingii and Bo. theileri in H. bispinosa. Therefore, this study may shed light on the circulating TBPs in ticks in the natural environment and thereby advocate awareness among physicians and veterinarians to control and prevent TBDs in Bangladesh.

Keywords: Bangladesh; Questing tick population; T. luwenshuni, E. ewingii, Bo. theileri; Tick-borne pathogens.