First report on tick-borne pathogens detected in ticks infesting stray dogs near butcher shops

Abid Ali; Shafi Ullah; Muhammad Numan; Mashal M Almutairi; Abdulaziz Alouffi; Tetsuya Tanaka

doi:10.3389/fvets.2023.1246871

First report on tick-borne pathogens detected in ticks infesting stray dogs near butcher shops

Front Vet Sci. 2023 Sep 18:10:1246871. doi: 10.3389/fvets.2023.1246871. eCollection 2023.

Authors

Abid Ali¹, Shafi Ullah¹, Muhammad Numan¹, Mashal M Almutairi², Abdulaziz Alouffi³, Tetsuya Tanaka⁴

Affiliations

¹ Department of Zoology, Abdul Wali Khan University Mardan, Mardan, Pakistan.
² Department of Pharmacology and Toxicology, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia.
³ King Abdulaziz City for Science and Technology, Riyadh, Saudi Arabia.
⁴ Laboratory of Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima, Japan.

Abstract

Public health is a major concern for several developing countries due to infectious agents transmitted by hematophagous arthropods such as ticks. Health risks due to infectious agents transmitted by ticks infesting butcher-associated stray dogs (BASDs) in urban and peri-urban regions have been neglected in several developing countries. To the best of the authors' knowledge, this is the first study assessing public health risks due to ticks infesting BASDs in Pakistan's urban and peri-urban areas. A total of 575 ticks (390 from symptomatic and 183 from asymptomatic BASDs) were collected from 117 BASDs (63 symptomatic and 54 asymptomatic); the ticks belonged to 4 hard tick species. A subset of each tick species' extracted DNA was subjected to polymerase chain reaction (PCR) to amplify the 16S rDNA and cox1 sequences of the reported tick species, as well as bacterial and protozoal agents. The ticks' 16S rDNA and cox1 sequences showed 99-100% identities, and they were clustered with the sequence of corresponding species from Pakistan and other countries in phylogenetic trees. Among the screened 271 ticks' DNA samples, Anaplasma spp. was detected in 54/271 (19.92%) samples, followed by Ehrlichia spp. (n = 40/271, 14.76%), Rickettsia spp. (n = 33/271, 12.17%), Coxiella spp. (n = 23/271, 4.48%), and Hepatozoon canis (n = 9/271, 3.32%). The obtained sequences and phylogenetic analyzes revealed that the pathogens detected in ticks were Ehrlichia minasensis, Ehrlichia sp., Hepatozoon canis, Coxiella burnetii, Coxiella sp., Anaplasma capra, Anaplasma platys, Anaplasma sp., Rickettsia massiliae, "Candidatus Rickettsia shennongii" and Rickettsia aeschlimannii. Tick-borne pathogens such as E. minasensis, H. canis, A. capra, A. platys, and R. aeschlimannii, were detected based on the DNA for the first time in Pakistan. This is the first report on public health risks due to ticks infesting BASDs. These results not only provided insights into the occurrence of novel tick-borne pathogens in the region but also revealed initial evidence of zoonotic threats to both public health and domestic life.

Keywords: butcher; one-health; pathogens; stray dogs; ticks.

Grants and funding

The researchers supporting project number (RSP2023R494), King Saud University, Riyadh, Saudi Arabia. This work was supported by JSPS KAKENHI Grant Numbers JP20KK0154 and JP22H02522, and JSPS Bilateral Program (Grant number JPJSBP120239937).