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.

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

Ixodes ticks transmit Theileria and Anaplasma species to a wide range of animals. The spreading of ticks and tick-borne pathogens has been attributed to transhumant herds, and research on these uninvestigated issues has been neglected in many countries, including Pakistan. Recently, we used internal transcribed spacer (ITS) and 16S ribosomal DNA partial sequences to genetically characterize Ixodes kashmiricus ticks and their associated Rickettsia spp. However, the data on its cox1 sequence and associated Theileria spp. and Anaplasma spp. are missing. This study aimed to genetically characterize I. kashmiricus based on the cox1 sequence and their associated Theileria spp. and Anaplasma spp. The I. kashmiricus ticks were collected from small ruminants: sheep (Ovis aries) and goats (Capra hircus) of transhumant herds in district Shangla, Dir Upper and Chitral, Khyber Pakhtunkhwa (KP), Pakistan. Out of 129 examined hosts, 94 (72.87%) (56 sheep and 38 goats) were infested by 352 ticks, including adult females (175; 49.7%) followed by nymphs (115; 32.7%) and males (62; 17.6%). For molecular analyses, 121 ticks were subjected to DNA isolation and PCR for the amplification of the cox1 sequence for I. kashmiricus, 18S rDNA for Theileria spp. and 16S rDNA sequences for Anaplasma spp. The obtained cox1 sequence showed 89.29%, 88.78%, and 88.71% identity with Ixodes scapularis, Ixodes gibbosus, and Ixodes apronophorus, respectively. Phylogenetically, the present cox1 sequence clustered with the Ixodes ricinus complex. Additionally, the 18S rDNA sequence showed 98.11% maximum identity with Theileria cf. sinensis and 97.99% identity with Theileria sinensis. Phylogenetically, Theileria spp. clustered with the T. cf. sinensis and T. sinensis. In the case of Anaplasma spp., the 16S rDNA sequence showed 100% identity with Anaplasma capra and phylogenetically clustered with the A. capra. PCR-based DNA detection targeting the amplification of groEL and flaB sequences of Coxiella spp. and Borrelia spp., respectively, was unsuccessful. This is the first phylogenetic report based on cox1 and new locality records of I. kashmiricus, and the associated T. sinensis-like and A. capra. Significant tick surveillance studies are needed in order to determine the epidemiology of Ixodes ticks and their associated pathogens.

First Detection of Theileria sinensis-like and Anaplasma capra in Ixodes kashmiricus: With Notes on cox1-Based Phylogenetic Position and New Locality Records

Tick-borne Rickettsia spp. have long been known as causative agents for zoonotic diseases. We have previously characterized Rickettsia spp. in different ticks infesting a broad range of hosts in Pakistan; however, knowledge regarding Rickettsia aeschlimannii in Haemaphysalis and Hyalomma ticks is missing. This study aimed to obtain a better understanding about R. aeschlimannii in Pakistan and update the knowledge about its worldwide epidemiology. Among 369 examined domestic animals, 247 (66%) were infested by 872 ticks. Collected ticks were morphologically delineated into three genera, namely, Rhipicephalus, Hyalomma, and Haemaphysalis. Adult females were the most prevalent (number ₌ 376, 43.1%), followed by nymphs (303, 34.74%) and males (193, 22.13%). Overall, genomic DNA samples of 223 tick were isolated and screened for Rickettsia spp. by the amplification of rickettsial gltA, ompA, and ompB partial genes using conventional PCR. Rickettsial DNA was detected in 8 of 223 (3.58%) ticks including nymphs (5 of 122, 4.0%) and adult females (3 of 86, 3.48%). The rickettsial gltA, ompA, and ompB sequences were detected in Hyalomma turanicum (2 nymphs and 1 adult female), Haemaphysalis bispinosa (1 nymph and 1 adult female), and Haemaphysalis montgomeryi (2 nymphs and 1 adult female). These rickettsial sequences showed 99.71–100% identity with R. aeschlimannii and phylogenetically clustered with the same species. None of the tested Rhipicephalus microplus, Hyalomma isaaci, Hyalomma scupense, Rhipicephalus turanicus, Hyalomma anatolicum, Rhipicephalus haemaphysaloides, Rhipicephalus sanguineus, Haemaphysalis cornupunctata, and Haemaphysalis sulcata ticks were found positive for rickettsial DNA. Comprehensive surveillance studies should be adopted to update the knowledge regarding tick-borne zoonotic Rickettsia species, evaluate their risks to humans and livestock, and investigate the unexamined cases of illness after tick bite among livestock holders in the country.

First report of spotted fever group Rickettsia aeschlimannii in Hyalomma turanicum, Haemaphysalis bispinosa, and Haemaphysalis montgomeryi infesting domestic animals: updates on the epidemiology of tick-borne Rickettsia aeschlimannii

Simple Summary Ticks are chelicerate arthropods that feed on blood and infest all vertebrates except fish and transmit different disease-causing agents including Rickettsia spp. to domestic and wild animals as well as humans. In the present study, we aimed to molecularly screen and genetically characterize Rickettsia spp. in various tick species infesting camels, sheep, and goats from five districts (Kohat, Dera Ismail Khan, Lower Dir, Bajaur, and Mansehra) of Khyber Pakhtunkhwa province, Pakistan. A total of 8/148 (5.4%) ticks, including four Hyalomma turanicum, two Haemaphysalis cornupunctata, one Haemaphysalis montgomeryi, and one Haemaphysalis bispinosa, were found positive for Rickettsia sp. The phylogenetic analysis of detected Rickettsia sp. based on three genetic markers (gltA, ompA, and ompB) revealed 100% identity with Rickettsia raoultii, clustered with its corresponding species reported in China, Russia, USA, Turkey, Denmark, Austria, Italy, and France. Further comprehensive studies on molecular and serosurveillance of various Rickettsia spp. in different ticks should be conducted in the region to understand the zoonotic threats due to these pathogens. Abstract Ticks are hematophagous ectoparasites that transmit different pathogens such as Rickettsia spp. to domestic and wild animals as well as humans. Genetic characterizations of Rickettsia spp. from different regions of Pakistan are mostly based on one or two genetic markers and are confined to small sampling areas and limited host ranges. Therefore, this study aimed to molecularly screen and genetically characterize Rickettsia spp. in various tick species infesting camels, sheep, and goats. All the collected tick specimens were morphologically identified, and randomly selected tick species (148) were screened molecularly for the detection of Rickettsia spp. by amplifying three rickettsial DNA fragments, namely, the citrate-synthase gene (gltA), outer-membrane protein A (ompA), and outer-membrane protein B (ompB). After examining 261 hosts, 161 (61.7%) hosts were found infested by 564 ticks, including 287 (50.9%) nymphs, 171 (30.3%) females, and 106 (18.8%) males in five districts (Kohat, Dera Ismail Khan, Lower Dir, Bajaur, and Mansehra). The highest occurrence was noted for Hyalomma dromedarii (number = 72, 12.8%), followed by Haemaphysalis sulcata (n = 70, 12.4%), Rhipicephalus turanicus (n = 64, 11.3%), Rhipicephalus microplus (n = 55, 9.7%), Haemaphysalis cornupunctata (n = 49, 8.7%), Hyalomma turanicum (n = 48, 8.5%), Hyalomma isaaci (n = 45, 8.0%), Haemaphysalis montgomeryi (n = 44, 7.8%), Hyalomma anatolicum (n = 42, 7.5%), Haemaphysalis bispinosa (n = 38, 6.7%), and Rhipicephalus haemaphysaloides (n = 37, 6.6%). A subset of 148 ticks were tested, in which eight (5.4%) ticks, including four Hy. turanicum, two Ha. cornupunctata, one Ha. montgomeryi, and one Ha. bispinosa, were found positive for Rickettsia sp. The gltA, ompA, and ompB sequences revealed 100% identity and were phylogenetically clustered with Rickettsia raoultii reported in China, Russia, USA, Turkey, Denmark, Austria, Italy, and France. Additionally, various reports on R. raoultii from Palearctic and Oriental regions were summarized in this study. To the best of our knowledge, this is the first report regarding genetic characterization and phylogenetic analysis of R. raoultii from Pakistan. Further studies to investigate the association between Rickettsia spp. and ticks should be encouraged to apprise effective management of zoonotic consequences.

Molecular Survey of Rickettsia raoultii in Ticks Infesting Livestock from Pakistan with Notes on Pathogen Distribution in Palearctic and Oriental Regions

Tick-borne bacteria of the genera Rickettsia and Coxiella cause several emerging veterinary and human infectious diseases. Ticks of the genus Hyalomma are medically important vectors due to their potential role in the transmission of pathogens to vertebrate hosts. There is an inadequate knowledge on tick-borne Rickettsia spp. and Coxiella spp. in ticks infesting transhumant camels in Pakistan. In this study, we conducted a molecular survey for screening of Rickettsia spp. and Coxiella spp. in ticks infesting camels. Seven hard tick species including Hyalomma dromedarii, Hyalomma anatolicum, Hyalomma scupense, Hyalomma isaaci, Hyalomma turanicum, Hyalomma asiaticum, and Rhipicephalus sanguineus s.l were confirmed on camels in three distinct physiographic regions of Khyber Pakhtunkhwa, Pakistan. A subset of morphologically identified ticks were subjected to molecular assays for the genetic characterization of ticks and the detection and genetic characterization of Rickettsia and Coxiella species using standard genetic markers. Ticks screened for pathogens resulted in the detection of Rickettsia aeschlimannii and Candidatus Rickettsia shennongii and Coxiella burnetii. The molecular analysis further reveals the presences of an undetermined Rickettsia aeschlimannii-like species, that is making a distinct phylogenetic clade with R. aeschlimannii. The detection of pathogens in camel ticks poses potential health hazards as these ticks frequently bites humans. Molecular screening of Rickettsia spp. and Coxiella spp. associated with camel ticks is a preliminary step toward the surveillance of evaluating their zoonotic threats in the region. 

Molecular detection of Rickettsia aeschlimannii, Candidatus Rickettsia shennongii, Rickettsia sp. and Coxiella burnetii in ticks collected from camels

Despite high diversity in the Oriental region, ticks of the genus Haemaphysalis have been neglected regarding their genetic data and vector potential. This study aimed to genetically characterize three species of the genus Haemaphysalis: Haemaphysalis cornupunctata, Haemaphysalis kashmirensis, and Haemaphysalis montgomeryi infesting goats and sheep, and Rickettsia spp. associated with these tick species in the Hindu Kush Himalayan range of Pakistan. Altogether, 834 ticks were collected by examining 120 hosts including goats (64/120, 53.3%) and sheep (56/120, 46.6%), in which 86 (71.6%) hosts were found to be tick-infested. The morphologically identified ticks were subjected to DNA extraction and PCR for the amplification of partial 16S rDNA and cox fragments. Rickettsia spp. associated with the collected ticks were detected through the amplification of gltA, ompA and ompB partial fragments. The 16S rDNA of H. cornupunctata and H. montgomeryi showed a maximum identity of 100% with the sequences of the same species, whereas the 16S rDNA of H. kashmirensis showed the highest identity of 93–95% with Haemaphysalis sulcata. The cox sequence of H. montgomeryi displayed 100% identity with the same species. In comparison, the cox sequences of H. cornupunctata and H. kashmirensis showed maximum identities of 87.65–89.22% with Haemaphysalis punctata and 89.34% with H. sulcata, respectively. The gltA sequence of Rickettsia sp. from H. kashmirensis showed the highest identity of 97.89% with Rickettsia conorii subsp. raoultii, while the ompA and ompB fragments from the same DNA samples revealed 100% and 98.16% identity with Rickettsia sp. and “Candidatus Rickettsia longicornii”, respectively. Another gltA sequence amplified from H. montgomeryi ticks showed 100% identity with Rickettsia hoogstraalii, while the attempts to amplify ompA and ompB for R. hoogstraalii were unsuccessful. In the phylogenetic tree, the 16S rDNA of H. cornupunctata clustered with the corresponding species while its cox clustered with H. punctata. Both 16S rDNA and cox sequences of H. kashmirensis clustered with H. sulcata. The gltA sequence of Rickettsia sp. was clustered individually in the spotted fever (SF) group of Rickettsia, while the gltA sequence of R. hoogstraalii was clustered with the same species in the transition group of Rickettsia. In the SF group, the rickettsial ompA and ompB sequence clustered with undetermined Rickettsia sp. and “Candidatus Rickettsia longicornii”, respectively. This is the earliest study regarding the genetic characterization of H. kashmirensis. This study indicated that ticks belong to the genus Haemaphysalis have the potential of harboring and/or transmitting Rickettsia spp. in the region.

/pdf/phylogenetic-position-of-haemaphysalis-kashmirensis-and-1w94uhyu.pdf

Phylogenetic Position of Haemaphysalis kashmirensis and Haemaphysalis cornupunctata, with Notes on Rickettsia spp.

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Phylogenetic Position of Haemaphysalis kashmirensis and Haemaphysalis cornupunctata, with Notes on Rickettsia spp.