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Review

Diversity and Distribution of Theileria Species and Their Vectors in Ruminants from India, Pakistan and Bangladesh

by
Jehan Zeb
1,2,
Baolin Song
1,
Muhammad Umair Aziz
1,
Sabir Hussain
1,
Riaz Zarin
3 and
Olivier Sparagano
1,*
1
Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong SAR, China
2
Department of Zoology, Abdul Wali Khan University Mardan, Mardan 23200, Pakistan
3
Elementary & Secondary Education Department Government of Khyber Pakhtunkhwa, Chitral 17200, Pakistan
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(2), 82; https://doi.org/10.3390/d14020082
Submission received: 28 December 2021 / Revised: 19 January 2022 / Accepted: 19 January 2022 / Published: 25 January 2022
(This article belongs to the Special Issue 2021 Feature Papers by Diversity’s Editorial Board Members)
Browse Figures
Versions Notes

Abstract

:
Tropical theileriosis, caused by the apicomplexan hemoparasite of the genus Theileria, is a major constraint to livestock production in various parts of world, including South Asia. Several studies have been carried out over the last five decades; however, comprehensive information in this region regarding the diversity and distribution of Theileria is lacking. Therefore, keeping in mind the economic importance of theileriosis, we have systematically reviewed the current knowledge about Theileria spp. diversity and distribution affecting cattle, water buffaloes, goats and sheep in three countries included India, Pakistan and Bangladesh of the Indian sub-continent. The data collected indicated that the microscopic method is the widely used method for evaluating Theileria species in the three countries from 1970 to 2021. This is the first study in this region to compile a comprehensive knowledge about the diversity and distribution of Theileria. Our study revealed the existence of 11 different species of Theileria, including Theileria spp. Theleria annulata, T. orientalis, T. mutans, T. velifera circulating in cattle and buffalo while T. annulata, T. lestoquardi, T. luwenshuni T. ovis, Theileria spp. and T. lestoquardi-like spp., were infecting goats and sheep from various regions of India, Pakistan and Bangladesh. We find that T. annulata can be found in both small and large ruminants and is widely distributed in the different regions of India, Pakistan and Bangladesh. In addition, our analysis revealed that the existence of possible tick vectors of the genera Hyalomma, Haemophysalis, Rhipicephalus and Amblyomma may be responsible for the diverse and wide distribution of different Theileria species. However, the competence of these tick vectors for different Theileria species still need to be explored. Therefore, further studies are needed to bridge this gap and to improve the health and production of livestock and reduce economic losses due to theileriosis in India, Pakistan and Bangladesh. Furthermore, we selected representative 18S rRNA sequences for T. annulata from the different regions to infer phylogenetic relationship. Phylogenetic analysis of the selected isolates clustered in different clades which might be due to the variation in a hypervariable region of 18S rRNA. The outcome of this analysis is expected to provide a coherent and integrated framework about the different Theileria species prevailing in these countries and contribute to improving the surveillance and control plans of various Theileria species in the region.

1. Introduction

Tick-borne diseases (TBDs) are considered to be one of the main threats to the ruminants’ health in both tropical and sub-tropical regions of the world, representing a serious obstacle to livestock farming. Several TBDs cause significant economic losses associated with high mortality rate and decreased production output in domestic livestock worldwide [1,2]. Among these, theileriosis is considered one of the significant tick-borne diseases and a major constraint in the growth of the livestock business in many areas of the world [3,4] (Ica et al., 2007; Jenkins 2018). It causes severe morbidity and mortality in livestock, reducing meat and milk production, leading to significant economic losses each year worldwide. The estimated range of economic losses due to theileriosis is 5–25% of the total farm losses worldwide [5]. Resource-poor farming communities are at a greater risk due to the lack of systematic acaricide use and limited access to veterinary health care centers leading to a high mortality rate in untreated animals [6,7].
The lifecycle of Theileria parasites in the ruminant host and tick vector has been reviewed [8,9]. Shortly, the lifecycle of Theileria is completed in two stages i.e., the vertebrate host stage (asexual reproduction) and tick vector stage (sexual reproduction). The lifecycle begins when an infected tick bites and transmits sporozoites into vertebrate hosts during blood-feeding, where it may transform into schizonts [10]. Subsequently, upon releasing from the infected leukocytes, the merozoites may infect host erythrocytes (RBCs) and then develop into piroplasms. Further multiplication of the piroplasms (merogony) takes place in the RBCs [11]. In non-transforming Theileria, merogony has been observed in RBCs [12]. Finally, the tick acquires blood-stage Theileria parasites including the gametes, when they feed on an infected host. Sexual reproduction of the gametes occurs in the midgut of the competent vector tick species, where, during meiosis, genetic recombination occurs [13,14]. In this way, Theileria parasites’ transmission occurs trans-stadially by the tick vectors, and therefore, the known transmission vectors may be 2- or 3-host tick species [9]. The modified form of life cycle of Theileria species is shown in Figure 1.
Theileria is distributed worldwide and is a significant cause of disease in livestock in tropical and subtropical regions of the world, including Asia. The most pathogenic and economically important Theileria species infecting large ruminants (Cattle; Bos Taurus and Bos indicus, and water buffalo; Bubalus bubalis) are T. annulata, which causes Tropical theileriosis (TT) or Mediterranean theileriosis, T. parva, which causes East Coast fever (ECF), and T. mutans, which causes benign theileriosis and T. orientalis, (T. orientalis/buffeli group), which causes Oriental theileriosis (OT) or Theileria-associated bovine anemia (TABA). However, on the other hand, T. lestoquardi, which causes malignant ovine theileriosis (MOT) T. uilenbergi and T. luwenshuni are the most pathogenic species of economic significance infecting small ruminants (goats; Capra aegagrus hircus and sheep; Ovis aries), T. taurotragi, and T. ovis, mostly cause asymptomatic infections in livestock [2,15]. Depending upon the Theileria species, different tick vector species of the genera Hyalomma, Rhipicephalus, Haemaphysalis, and Amblyomma are involved in disease transmission [16].
Different diagnostic techniques are used for the detection of Theileria. Most widely used and standard techniques are Giemsa-stained blood smears and lymph node needle biopsy smears. These methods are more useful in acutely infected animals than the chronically infected carriers due to the low level of parasitaemia. Furthermore, species-specific identification based on Giemsa staining is difficult as most Theileria piroplasms share morphological identity except for T. parva, T. annulata and T. velifera. Similarly, schizonts cannot always be detected in the superficial lymph nodes during the disease time. In addition, these methods need more field investigation [15,17]. As an alternative, a serological method for detecting parasites antibodies has been developed. However, these methods may only detect previous exposure to the infection as compared to the current one due to its poor sensitivity and specificity [15,18]. New advanced techniques such as next-generation genomic resources have been adapted to overcome these limitations of traditional gross parasitological diagnostic techniques. Different piroplasm species can be differentiated based on variations in the hyper-variable region of 18S rDNA sequence [19,20,21,22,23,24,25]. For the amplification of the 18S region, various PCR methods like reverse line blot (RLB)-PCR, quantitative PCR (qPCR) and multiplex PCR have been described to [19,26,27,28].
The seasonal fluctuations have been found as one of the important risk factors that affect the distribution of this parasite. There are several species of this parasite, and they have substantial differences in their ecoepidemiology in significant parts of the Asian countries including India, Pakistan and Bangladesh. In addition, lack of proper management practices in these areas may lead to heavy economic losses [29,30,31]. Keeping in view the importance of the above discussion, the present review data related to the Theileria species diversity infecting ruminant species and distribution concerning its tick vectors in specific region of the Asia including India, Pakistan and Bangladesh. The outcome of this analysis is expected to provide an integrated scientific baseline for future vaccination programs and other control measures either at the pathogen or vector level.

2. Materials and Methods

2.1. Study Protocol

In this review study, we systemically reviewed the relevant articles published on Theileria in small and large ruminants in the three important countries from the livestock perspectives of South Asia, including India, Pakistan and Bangladesh as shown in Figure 2. The different studies were divided into various zones based on administrative and geomorphic features such as India divided into five zones viz Central, North, East, North-east, West, South, while Pakistan divided into four provinces such as Punjab, Khyber Pakhtunkhwa, Sindh and Balochistan and FATA and Bangladesh was divided into six zones like Central, South Eastern, North Central, Northern, and Western.

2.2. Literature Search Strategy

Our procedure was based on searching different databases such as PubMed, Science Direct, Springer, Scopus, Google Scholar and Web of Science for retrieving relevant articles published in these three countries, which mainly focused on the time period from 1970 to 2021. Furthermore, to back trace the past years published articles on Theileria, all collected peer- reviewed articles, and references cited from the retrieved studies were searched again. Different terms such as Theileria, tick borne pathogens, Theileria vectors, tick vectors, large ruminants, small ruminants, and region of the concerned country were used for retrieving data.

2.3. Data Extraction and Qualitative Assessment

The diversity and distribution studies were analyzed carefully and reviewed systematically before initiating the data entry process onto predesigned Microsoft Excel 2010 sheets. To further maximize the accuracy, the extracted information compiled in Microsoft Excel 2010 by the author (JZ) was screened to remove repeated studies. After the data were entered, another author (OS) checked the dataset thoroughly to avoid errors, duplications and to further enhance the quality of extracted data.
Furthermore, all studies regarding Theileria/theileriosis conducted on large (cattle and buffaloes) and small ruminants (goats and sheep) in the region were selected for analysis. Five key pieces of information was extracted from the literature: (1) Theileria species and possible tick vectors detection (2) region, state or location of the study, (3) time of the study conducted, (4) study type and (5) studies that have used the standard methodology of confirmatory tests including blood smear examination with different staining methods, molecular methods by different PCRs, and serological diagnosis.
During the first step of screening, 410 articles, including n = 250 from India, n = 130 from Pakistan and n = 30 from Bangladesh were retrieved. Following the data retrieval step, the data were compiled in Microsoft Excel 2010 and all the duplicated studies n = 60 were removed from further screening while n = 130 theses and full length papers which were not available online were also excluded. In addition, all the irrelevant data and papers (n = 75) published in a language other than English were also removed. To further enhance the quality assessment, we removed the conference proceedings, which were not available with full text. Finally, a total of 136 were identified to be eligible for data analysis which included n = 67, n = 56 and n = 13 from India, Pakistan and Bangladesh, respectively (Figure 3). The studies were carried out between 1975 and 2021, and were grouped in three different periods: (1) 1975–2010, (2) 2011–2015, (3) 2016–2021, and were differentiated between molecular and direct diagnostic tests, as shown in Figure 4 and Figure 5.

2.4. Phylogenetic Analysis and Evolutionary Divergence

Representative sequences with accession numbers were selected from the previously published studies and were used for phylogenetic and evolutionary (genetic) divergence analysis. The sequences selected from the different regions of India were included, MF287947.1 (Central India), MF287920.1, (West India), MF287949.1 (Eastern India), MF287937.1 T_annulata South India and MF287934.1 (North India) while sequences with accession numbers from Pakistan are included JQ743631.1 (Pakistan), JQ743636.1, (Pakistan), MW046053.1 (Pakistan) and MW046054.1 (Pakistan). The phylogenetic tree of the selected T. annulata isolates was inferred using the 18S rRNA genetic marker. Phylogenetic analyses were conducted with a Tamura 3-parameter (T92 + G) Model using MEGA version 7.0 [32]. CLUSTAL W alignment was performed to align the selected sequences retrieved from the GenBank. The neighbor-joining algorithm was used to establish the phylogenetic analysis. Bootstrap values were obtained with 1000 replicates.

3. Results and Discussion

3.1. Diversity and Distribution of Theileria Species Infecting Livestock

A general overview of the Theileria species identified in the three countries is depicted in the Table 1. We have collected the data regarding different species of Theileria infecting livestock i.e., large (cattle & buffalo) and small ruminants (goats & sheep) conducted in the different geographical regions of the three selected countries of South Asia. Our analysis revealed that different species of Theileria in these countries circulating in large ruminants include T. annulata, T. orientalis T. mutans, T. Ovis and T. velifera and Theileria spp., while in small ruminants, the different species of Theileria reported were T. annulata, T. lestoquardi, T. luwenshuni T. ovis, Theileria spp. and T. lestoquardi-like spp. from various geographical locations of India, Pakistan and Bangladesh. Among these, the most common and widespread species circulating in all ruminants is T. annulata.

3.2. Diversity and Distribution of Theileria Species Infecting Livestock in the Different Regions of India

Theileria species reported from different regions of India are listed in Table 2. According to the data collected, only one species of Theileria reported in cattle and buffalo from the central region of India is T. annulata, [33,34] while, on the other hand, in Eastern India, two species of Theileria. (T. mutans & T. velifera) were identified; however, no Theileria species were reported in small ruminants from these two regions [35,36]. Furthermore, Theileria species identified in the large ruminants from South India included Theileria spp., T. annulata [37,38,39] and new T. orientalis genotype [40,41,42,43], whereas, in East and North East India, trans placental transmission of T. annulata in young borne calves and its detection in tick Hy. anatolicum has been identified [44,45]. In the case of small ruminants, T. lestoquardi was identified molecularly. T. luwenshuni & T. ovis [46,47,48] were detected in South India while only T. luwenshuni has been recorded in the East and Northeast region of India [49,50]. Furthermore, Theileria spp., [51] T. annulata, [52,53,54,55,56,57] and T. orientalis [58] were detected to be circulating in cattle and buffalo while T. annulata, [59], Theileria spp. [60] and T. luwenshuni [61,62,63] were found infecting goats and sheep (small ruminants) from West Bangal and North India. The difference in the distribution of diversity of various Theileria species in different regions may be attributed to various factors such as competent vector tick species, geo-climatic conditions favoring different vector tick species growth, lack of education of farmers, and improper use of acaricidal use.

3.3. Possible Tick Vectors for Theileria Species in India

The diverse array of Theileria species in the region may be due to different tick vectors infesting livestock, which is shown in Table 3. Several studies have reported different vector tick species from different regions of India included R. microplus Hae. Bispinosa Hy. truncatum Hy. dromedarii Hy. anatolicum R. Sanguineous [70,78,99]. It may be assumed that the presence of different species of Theileria circulating in large and small ruminants may be linked to the presence of a wide variety of these tick vectors in the particular area as these ticks have the potential to transmit various Theileria species reported from other parts of the world [100,101]. For example, it has been found in Uttar Pradesh that H. anatolicum and R. appenticulatus could play a vector role in the T. annulata and T. lestoquardi transmission in large and small ruminants, respectively [64]. Similarly, Hy anatolicum and R. microplus Hy. m. isaaci have been identified to transmit T. annulata in cattle, while, in buffalo, Hy. anatolicum may be the only vector transmitting T. buffeli (T. orientalis). On the other hand, Hy. anatolicum and Haemaphysalis are widely distributed in different regions of India [64,102], which may transmit various species of Theileria such as T. lestocardi (hirci) and other Theileria species in goats and sheep. Recently, in India, some studies have also confirmed the role of various tick species such as R. microplus, Hy. anatolicum and Hae. bispinosa in the transmission of T. orientalis [70,78]. Similar reports have been observed in Africa [103]. Besides the above-mentioned tick species, Hy. detritum, Hy. dromedarii, and Hy. lusitanicum can also be the potential vectors for the transmission of this pathogen in different hosts [9].

3.4. Diversity and Distribution of Theileria Species in Different Regions of Pakistan

Theileria species that have been reported in different provinces of Pakistan are listed in Table 4. Approximately three different species of Theileria, including Theileria spp., T. annulata and T. orientalis have been reported in cattle and buffalo from different places of the Punjab province. Among these, the predominant and widely distributed pathogen is T. annulata, which many authors have reported across the province either microscopically or molecularly [104,105,106,107]. In addition to T. annulata, other Theileria species such as T. orientalis [108,109,110] and Theileria spp. have also been identified recently [111,112,113]. On the other hand, different species of Theileria identified in small ruminants (goats and sheep) from various geographic areas of Punjab included Theileria spp. and T. annulata, [114,115,116] T. ovis and T. ovis, T. lestoquardi, [115,117,118,119]. In Khyber Pakhtunkhwa province, several studies from different areas investigated that T. annulata is the only species circulating in cattle and buffalo [101,120,121,122]; however, diverse species of Theileria such as T. annulata, T. lestoquardi, T. luwenshuni T. ovis and Theileria spp. have been identified in goats and sheep [123,124,125,126]. Theileria spp. and T. annulata were identified in cattle and buffalo from Sindh and Balochistan Province [116,127]. No single study has reported Theileria species infecting ruminants from Sindh province; however, in Balochistan and FATA, different species Theileria identified from small ruminants include T. annulata, T. ovis and T. lestoquardi [7,107,116]. Some studies were carried out in the adjoining areas of two provinces and reported different species of Theileria; for example, in a study Ghafar et al. [128] interestingly identified T. lestoquardi-like spp., T. orientalis and T. annulata from the ticks collected from the cattle and buffalo in different agro-ecological zones of Punjab and Sindh Province, while, on the other hand, Durrani et al. [129] and Karim et al. [130] identified T. ovis and T. annulata in small and large ruminants from the different regions of Punjab and Khyber Pakhtunkhwa, respectively.

3.5. Tick Vectors for Transmission of Theileria in Pakistan

In Pakistan, different studies have reported a wide variety of tick species from various geographical areas as shown in Table 5. In these studies, different tick species have been identified, which may be due to different prevailing conditions in the country such as seasonal fluctuation, relative humidity, temperature, association and lifestyle of different species of animals, lack of education in farmers, and farm management practices which may favor tick growth and survival. In the current study, existence of a wide variety of Theileria species may be due to the presence of different tick vectors, which may possibly play a role in the transmission of these pathogens. Common genera which may be possibly involved in the transmission of these pathogens include Hyalomma, Rhipicephalus and Haemaphysalis. Several studies have reported different tick species across the country such as Hy. hussaini, Hy. scupense, Hy. anatolicum, Hy. scupense, Hy. excavatum, R. microplus, R. sanguineus [105,123,138,155,156,157,158]. These ticks may have the capacity to transmit different Theileria species in different hosts [103,107]. However, further molecular studies are needed to find out their vector competencies.

3.6. Regional Wise Distribution of Theileria Species and Its Possible Tick Vectors in Bangladesh

Different species of Theileria from large and small ruminants from various geographical regions are listed in Table 6. Among these, most of the species such as Theileria spp., T. annulata, T. mutans and T. orientalis have been identified from the large ruminants of Central and North Central regions of Bangladesh [186,187,188,189] while, from the Southwestern, Northern and Western region, only Theileria spp. and T. annulata have been reported [190,191,192,193]. Furthermore, only one species, i.e., T. annulata, was reported in goats and sheep from the central part of Bangladesh [189,194].
The possible vector tick species from the different geographical places of Bangladesh that could be involved in the transmission of various Theileria species in small and large ruminants are shown in Table 7 and Table 8. The common tick species responsible for the transmission of Theileria in cattle and buffalo are R. microplus, Hae. bispinosa, R. sanguineus, and Hy. anatolicum anatolicum [102], while, in the case of small ruminants (goats and sheep), these may be R. sanguineus and Hy. anatolicum anatolicum [102].

3.7. Phylogenetic Analysis, Genetic Divergence and Multiple Sequence Alignment

We have selected T. annulata for phylogenetic and genetic divergence analysis as this species may infect all ruminants and could be of great economic concern. The evolutionary history was inferred using an 18S rRNA taxonomic marker. Homology searches of the selected 18S rRNA isolates shared 99–100% similarities with local and global isolates deposited in the NCBI GenBank. The neighbor-joining algorithm was used to establish a phylogenetic relationship among different selected isolates. The selected 18S rRNA isolates were clustered into different clades (Figure 6). However, no single isolate was selected from Bangladesh as 18S RNA sequence was not available for T. annulata from Bangladesh. We select the 18S rRNA genetic marker as several previously published studies used this genetic marker in Pakistan, India and other parts of the world to identify and establish the phylogenetic profile of T. annulata circulating in ruminants [41,101,106,109,198]. The 18S rRNA gene play an important role in genetic variability of Theileria spp. due to the presence of conserved sequences and some hypervariable regions which are crucial in determining the evolutionary patterns and discriminating the various Theileria species [16,199]. Furthermore, targeting the amplification of the hypervariable V4 region of the 18S rRNA gene is preferably used for the accurate identification, classification and exploring the population structures of the piroplasm parasites [117,200]. Nucleotide sequence heterogeneity analysis (evolutionary/genetic divergence) showed that T. annulata isolates were different from each other by 0–4.7 bp as shown in Table 9. Maximum divergence (4.7 bp) was observed with isolates from Pakistan. Additionally, the multiple alignment analysis also showed changes in the nucleotide sequences of different isolates as can be seen in Figure 7. These genetic variations may be due to genetic variability contributed by the deletions, insertions and substitutions in the nucleotide sequences of different isolates [41,55], which may result in the various degrees of pathogenecity and treatment measures in the field. Thus, on the basis of this analysis and previous findings, we concluded that, due to the presence of a hypervariable region and genetic variability, vaccine development against Theileria species is still challenging, and we may suggest that using a single diagnostic or immunogenic molecule may not be sufficient in achieving the required goals.

3.8. Overall Comparison (Why Vector-Borne Diseases like Theileria Are Increasing Day by Day)

The global climate has been changing over the last century due to greenhouse gas emissions. It will continue to change over this century, accelerating without effective global efforts to reduce emissions. Ticks and tick-borne diseases (TTBDs) are inherently climate-sensitive due to the sensitivity of tick lifecycles to climate. Key direct climate and weather sensitivities include survival of individual ticks and the duration of development and questing (host-seeking) activity of ticks [201].
We have concluded that our data contribute to the knowledge of Theileria species diversity and distribution circulating in ruminants in different regions of India, Pakistan and Bangladesh. The diverse species and wide distribution of Theileria in the region may be linked with the presence of their possible vector tick species belonging to the main four genera including Hyalomma, Haemaphysalis, Rhipicephalus and Amblyomma as they have been identified as Theileria vectors from several parts of the world [101,102,103,107,117]. Paucity still exists; however, molecular studies have been updated and increased during the last decade regarding Theileria species identification and their possible vectors. Different ticks have been adapted to diverse climatic conditions such as aridity in the desert, and seasonal and daily fluctuations may result in widespread distribution of these ticks and subsequently lead to the diversity in Theileria species. This adaptation offers the tick a significant comparative advantage over other tick species under the predicted scenarios for climate change [103], particularly in the context of South Asian countries where these tick species might gain importance in the future. Our analysis suggests the needs of further molecular studies to discover different species and strains, and their potential vectors as microscopic studies have not been so effective in identifying different species and strains. Additionally, genetic variation among different T. annulata isolates may be due to the mutations in the hypervariable region and genetic variability, which makes the therapeutic and single molecule based vaccine development against Theilera challenging and necessitates the needs for alternative control measures. This study also helps in providing a baseline for devising integrated control measures to reduce the losses due to these pathogens being either at the pathogen or vector level.
Thus, on the basis of this analysis and previous findings, we may suggest that using a single diagnostic or immunogenic molecule may not be sufficient in achieving the required goals regarding Theileria control strategies.

Author Contributions

J.Z. designed the study, searched the literature, identified and screened articles, and extracted data which was reviewed by O.S., J.Z., B.S., S.H. and M.U.A. wrote the first draft of the manuscript. J.Z. performed molecular and genetic analysis. R.Z. conducted geographic and regional analysis of data. O.S. revised the manuscript critically. All the authors approved the final version of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

O.S. is a Principal Investigator of an internal research fund of the Department of Infectious Diseases and Public Health of the City University of Hong Kong (Project number 9380108).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

We are thankful to all authors whose articles are included in this study.

Conflicts of Interest

The authors declare that there is no conflict of interest.

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Diversity 14 00082 g001 550
Figure 1. Life cycle of Theileria showing different stages in ruminants and tick hosts.
Figure 1. Life cycle of Theileria showing different stages in ruminants and tick hosts.
Diversity 14 00082 g001
Diversity 14 00082 g002 550
Figure 2. Map showing the location of the study area (India, Pakistan, and Bangladesh) and a list of Theileria Species present in each country.
Figure 2. Map showing the location of the study area (India, Pakistan, and Bangladesh) and a list of Theileria Species present in each country.
Diversity 14 00082 g002
Diversity 14 00082 g003 550
Figure 3. Flow chart diagram showing the data retrieving and extraction procedure.
Figure 3. Flow chart diagram showing the data retrieving and extraction procedure.
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Diversity 14 00082 g004 550
Figure 4. Comparison of the number of epidemiological studies detecting Theileria spp. in water buffalo and cattle using molecular and microscopic diagnostic methods in India, Pakistan and Bangladesh, according to three different periods between 1975 and 2021.
Figure 4. Comparison of the number of epidemiological studies detecting Theileria spp. in water buffalo and cattle using molecular and microscopic diagnostic methods in India, Pakistan and Bangladesh, according to three different periods between 1975 and 2021.
Diversity 14 00082 g004
Diversity 14 00082 g005 550
Figure 5. Comparison of the number of epidemiological studies detecting Theileria spp. in goats and sheep using molecular and microscopic diagnostic methods in India, Pakistan and Bangladesh, according to three different periods between 1975 and 2021.
Figure 5. Comparison of the number of epidemiological studies detecting Theileria spp. in goats and sheep using molecular and microscopic diagnostic methods in India, Pakistan and Bangladesh, according to three different periods between 1975 and 2021.
Diversity 14 00082 g005
Diversity 14 00082 g006 550
Figure 6. Phylogenetic analysis of selected T. annulata isolates (18 S rRNA gene).
Figure 6. Phylogenetic analysis of selected T. annulata isolates (18 S rRNA gene).
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Diversity 14 00082 g007 550
Figure 7. CLUSTAL W multiple sequence alignment analysis for the different T. annulata isolates from India and Pakistan. The box below showing the changes in nucleotide sequences between T. annulata isolates from Pakistan and India. * means nucleotide similarities.
Figure 7. CLUSTAL W multiple sequence alignment analysis for the different T. annulata isolates from India and Pakistan. The box below showing the changes in nucleotide sequences between T. annulata isolates from Pakistan and India. * means nucleotide similarities.
Diversity 14 00082 g007
Table
Table 1. Common Theileria species found in India, Pakistan and Bangladesh.
Table 1. Common Theileria species found in India, Pakistan and Bangladesh.
CountryHostTheileria Species Name
IndiaCattle & BuffaloesTheileria spp. T. annulata, T. orientalis, T. mutans & T. velifera
Goats & SheepTheileria spp. T. lestoquardi T. luwenshuni & T. ovis
PakistanCattle & BuffaloesT. annulata, T. orientalis & Theileria spp.
Goats & SheepT. annulata, T. lestoquardi, T. luwenshuni T. ovis & Theileria spp. T. lestoquardi-like spp.
BangladeshCattle & BuffaloesTheileria spp. T. annulata, T. orientalis, T. Mutans,
Goats & SheepT. annulata
Table
Table 2. Regional wise distribution of Theileria Species in different regions of India.
Table 2. Regional wise distribution of Theileria Species in different regions of India.
India
Province/StateTheileria spp.Identification MethodHostYear of StudyReferences
Central India
Cattle & Buffaloes
Central IndiaT. annulataMicroscopyTicks & Cattle1975[64]
Uttar PradeshT. annulataMolecularCattle1977[65]
Uttar PradeshT. annulataMicroscopyCattle2012[66]
Uttar PradeshT. annulataMolecularCattle2015[67]
ChhattisgarhT. annulataMicroscopyCattle2016[34]
Central IndiaT. annulataMolecularCattle2017[68]
Uttar PradeshT. annulataMolecularCattle2018[69]
HisarT. annulataMicroscopyCattle1989[33]
Eastern India
West BangalT. annulataMolecularCattle2003[35]
GuineaT. mutans & T. veliferaMolecularCattle2021[36]
South India
North BangloreT. annulataMicroscopyCattle2009[37]
KeralaTheileria spp. & T. annulataMicroscopy & MolecularCattle2011[38]
South IndiaT. orientalisMolecularCattle2011[70]
South IndiaT. annulata & Theileria spp.MolecularCattle2013[40]
Tamil NaduTheileria spp.MicroscopyCattle2014[71]
Telangana and Andhra PradeshT. orientalisMolecularCattle2015[41]
KarnatakaT. annulataMicroscopyCattle2016[42]
Southwest IndiaT. annulataMicroscopyBuffalo & Cattle2016[39]
KarnatakaT. annulataMicroscopyCattle2017[72]
KeralaT. orientalisMolecularR. annulatus Ticks2019[43]
South IndiaTheileria spp.MolecularTicks & Cattle2021[73]
Goats & Sheep
West BengalT. hirci (T. lestoquardi)MicroscopyGoat1990[46]
KarnatakaTheileria spp.MicroscopySheep1985[74]
South IndiaTheileria spp.MicroscopyGoat & Ticks2017[47]
KeralaTheileria spp.Microscopy & MolecularGoats2017[75]
Karnataka T. luwenshuniMolecularGoats & Sheep2017[48]
KarnatakaT. luwenshuni & T. ovisMolecularSheep2019[76]
KarnatakaTheileria spp.MicroscopySheep2020[77]
AssamT. annulata & T. orientalisMolecularCattle2015[78]
OdishaT. annulata & T. orientalisMicroscopy & MolecularCattle2017[79]
OdishaT. annulataMicroscopy and MolecularCattle2017[80]
OdishaT. orientalisMolecularCattle2020[81]
OdishaT. annulataMolecularCattle2021[44]
OdishaT. annulataMolecularCattle2021[45]
Goats & Sheep
AssamT. luwenshuniMicroscopy & MolecularGoat2018[50]
Guwahati of AssamT. luwenshuniMicroscopy & MolecularGoat2019[49]
West India
AnandT. annulataMolecularBuffalo & Cattle2014[52]
GujratT. annulataMicroscopy and MolecularCattle2015[54]
GujratT. annulataMicroscopy & MolecularCattle & Buffalo2015[53]
MaharashtraT. annulata & T. orientalisMolecularCattle2017[58]
BiharT. annulataMicroscopyBuffalo2018[82]
AnandT. annulata & T. orientalisMolecularCattle2019[55]
Maharashtra & tamil NaduT. annulataMolecularBuffalo & Cattle2019[58]
Telangana, Gujarat, Haryana, and BiharT. annulataMolecularVaccine Isolate2019[83]
MaharashtraTheileria spp.MicroscopyBuffalo2020[51]
BiharTheileria spp.MicroscopyCattle2021[84]
Tamil NaduT. annulataMolecularCattle2021[57]
BiharT. annulataMicroscopy & MolecularCattle2021[85]
Haryana T. annulataMicroscopyGoat, cattle, sheep Sera1998[86]
Tamil NaduTheileria Spp.MicroscopySheep2005[87]
HaryanaT. annulataMolecularTick2006[59]
Tamil NaduTheileria spp.MicroscopyGoats & Sheep2015[60]
Tamil NaduT. luwenshuniMolecularGaots & Sheep2019[61]
MaharashtraT. luwenshuniMicroscopy & MolecularSheep2021[62]
PunjabT. annulataMicroscopyTick Hy. anatolicum2010[88]
GujratTheileria spp.MicroscopyBuffalo & Cattle2021[89]
Ludhiana PunjabT. annulataMicroscopyCattle2012[90]
PunjabT. annulataMolecularCattle2015[91]
Ludhiana PunjabT. annulataMolecularTick & Cattle2015[92]
RajasthanTheileriaMicroscopyCattle2015[93]
Uttara handTheileria genusMicroscopy & MolecularCattle2014[94]
HaryanaT. annulataMicroscopyCattle2017[95]
HaryanaT. annulataMolecularCattle2020[96]
Telangana, Gujarat, Haryana, and BiharT. annulataMolecularVaccine2021[83]
GujratT. annulataMolecularCattle2021[97]
Himachal PradeshT. orientalisMolecularCattle2021[98]
Goats & Sheep
Himachal PradeshT. luwenshuniMolecularGoats & Sheep2021[63]
Table
Table 3. Distribution of the possible vector tick species of Theileria in different regions of India.
Table 3. Distribution of the possible vector tick species of Theileria in different regions of India.
Tick SpeciesHostStates/RegionReferences
R. microplus. R. haemaphysaloidesCattle & BuffaloIt is found in all places except Manipur, Kerala, Nagaland, Tripura & Maharashtra[78,102]
Hy. anatolicumRuminantsIt may be present in all parts except Andhra Pradesh, Jharkhand, Manipur, Mega laya, Stkin, Tripuri[33,46,103]
Hae. BispinosaGoats & SheepWidely distributed except Delhi, Haryana, Kerala, Nagaland, Uttar Pradesh and Chhattisgarh [47,64,70,99]
Hy. truncatumGoats & SheepIt is restricted to only Gujrat, Maharashtra & Uttar Pradesh[102]
Hy. dromedariiGoats & SheepIt can be found only in Andhra Pradesh, Delhi, Gujrat, Haryana, Himachal Pradesh, Jammu & Kashmir, Odisha, Punjab, Rajasthan, Uttar Pradesh[102]
R. SanguineusGoats & SheepIt is reported from all places except Gora, Delhi, Manipur, Megha laya, Nagaland, Tripuri and Uttar Pradesh[47,64,102]
Table
Table 4. Provincial wise distribution of the different Theileria species in Pakistan.
Table 4. Provincial wise distribution of the different Theileria species in Pakistan.
Pakistan
Province/StateTheileria SpeciesIdentification MethodHostYearReference
Punjab
Cattle & Buffaloes
PunjabTheileria spp.MicroscopyCattle1983[131]
FaisalabadTheileria spp.MicroscopyCattle1999[132]
FaisalabadT. annulataMicroscopyBuffaloes & Cattle2004[133]
KasurTheileria spp.MicroscopyCattle2005[134]
PunjabT. annulataMicroscopyBuffaloes2006[135]
KasurT. annulataMolecularCattle2008[136]
PunjabT. annulataMicroscopy & MolecularCattle2008[137]
SahiwalTheileria spp.MicroscopyCattle2010[111]
Southern PunjabT. annulataMicroscopyCattle2011[104]
SargodhaT. annulataMicroscopyCattle2012[138]
Faisalabad, Jhang, KhanewalT. annulataMolecularTicks of Cattle & Buffaloes2013[105]
FaisalabadT. annulataMolecularCattle & Buffaloes2013[106]
PunjabT. orientalisMolecularCattle2021[108]
PunjabT. annulataMolecularCattle2018[109]
PunjabT. annulata & T. orientalisMolecularCattle2018[139]
LahoreT. annulataMicroscopyCattle2018[5]
Agro-ecological Zones PunjabT. orientalis & T. annulataMolecularRuminants2019[110]
Agro-ecological Zones PunjabT. annulataMolecularCattle2020[107]
LayyahT. annulata & T. orientalisMolecularCattle2021[113]
Dera Ghazi Khan & LodhranT. annulataMolecularCattle2021[112]
AttockTheileria spp.MicroscopyGoats & Sheep2010[140]
OkaraTheileria spp.MicroscopySheep2010[141]
LahoreT. lestoquardi & T. ovisMicroscopy & MolecularSheep2011[142]
LahoreTheileria spp.MicroscopyGoats & Sheep2011[143]
OkaraT. ovisMolecularSheep2013[114]
Southern PunjabT.lestoquardiMolecularGoats & Sheep2015[144]
MultanT. ovis & T. lestoquardiMicroscopy & MolecularGoats & Sheep2017[115]
MultanT. lestoquardi & T. ovisMicroscopy & MolecularGoats & Sheep2017[145]
PunjabT. annulata T.ovis & T. lestoquardiMolecularRuminants2019[117]
MultanT. lestoquardi && T. ovisMolecular & MicroscopyGoats2019[118]
LayyahT. annulataMolecularSheep2021[119]
LahoreTheileria Spp.MicroscopyGoats & Sheep2021[116]
PeshawarT. annulataMicroscopyBuffalo & Cattle2005[146]
KPK (Southern KP)T. annulataMolecularCattle2012[147]
KPKT. annulataMolecularCattle2017[120]
Northern PakistanT. annulataMolecularCattle (Ticks)2019[101]
North-Western PakistanT. annulataMolecularCattle2021[148]
DI KhanTheileria spp.MicroscopyCattle2021[149]
Central KPKT. annulataMicroscopy & MolecularCattle2021[122]
KPKT. lestoquardi & T. ovisMolecularGoats & Sheep2013[147]
KPKT.lestoquardiMolecularGoats & Sheep2015[150]
Peshawar & PeripheryTheileria spp.MicroscopyRuminants2017[151]
Peshawar & Khyber AgencyTheileriaMicroscopyGoats & Sheep2017[152]
Southern KPKT. ovis T. lestoquardiMolecularGoats & Sheep2018[123]
Southern KPKTheileria spp.MicroscopySheep2018[153]
KPKT. annulata, T. lestoquardi, T. luwenshuni T. ovis & Theileria spp. MolecularGoats & Sheep2020[124]
Malakand DivisionTheileria spp.MicroscopyBuffalo, Cattle, Goat & Sheep2021[125]
KPKTheileria Spp. T. annulata, T. lestoquardi, T. ovisMolecularGoats & Sheep2021[126]
Sindh
HyderabadTheileria spp.MicroscopyCattle1994[154]
KarachiTheileriaMicroscopyBuffalo2012[127]
QuettaT. annulataMicroscopyCattle2021[116]
BaluchistanTheileria ovis & T. lestoquardiMolecularGoats & Sheep2017[7]
FATAT. ovisMolecularGoats & Sheep2020[107]
Punjab & KPKT. ovisMicroscopy & MolecularGoats & Sheep2012[129]
Pakistan/Punjab-KPKT. annulataMolecularRuminants2017[130]
Sindh & PunjabT. lestoquardi-like spp., T. orientalis & T. annulataMolecularCattle2021[128]
Table
Table 5. Distribution of various tick vectors for the transmission of Theileria species in Pakistan.
Table 5. Distribution of various tick vectors for the transmission of Theileria species in Pakistan.
TicksHostReferences
Punjab
R. microplus, Hy. anatolicum, Hy. aegyptium, Hy. dromedarii, R. appendiculatus, R. sanguineusCattle and buffaloes[102,105,138,147,153,157,158,159,160,161,162]
Khyber Pakhtunkhwa
R. microplus, R. appendiculatus, Hy. anatolicumCattle & buffaloes[101,163]
Sindh
Hy. hussaini, Hy. scupense, R. annulatus, R. microplus, Hy. anatolicum, Hy. scupense, Hy. excavatumBuffaloes[155,156,164]
Balochistan
R. microplus, Hy. anatolicum, Hy. scupense, Hy. aegyptium, HaemaphysalisCattle & buffaloes[107,165,166,167,168,169]
Punjab
Hy. anatolicum, Hy. excavatum R. appendiculatus, Hy. dromedarii, R. microplus, R. sanguineus, R. TuranicusGoats
& Sheep		[158,160,170,171,172,173,174]
Khyber Pakhtunkhwa
Hy. anatolicum, Hy. detritum, Hy. excavatum, Hy. scupense, Haemaphysalis longicornis, Hyalomma impeltatum, R. appendiculatus, R. microplusGoats & Sheep[107,175,176,177,178,179,180]
Sindh
Hae. bispinosa, Hy. anatolicum, Hy. detritum, Hy. dromedarii, Hy. hussaini, Hy. impeltatum, Hy. marginatum isaaci, R. microplus, R. SanguineusGoats & Sheep [181,182]
Balochistan
Hy. anatolicum, Hy. dromedarii, Hy. excavatum, Hy. scupense, R. microplusGoats & Sheep [168,183,184,185]
Table
Table 6. Regional wise distribution and diversity of Theileria species in various regions of Bangladesh.
Table 6. Regional wise distribution and diversity of Theileria species in various regions of Bangladesh.
Bangladesh
CityTheileria spp.Identification MethodHostYear of StudyReferences
Central Region
Dhaka TargilT. annulataMicroscopyCattle1983[195]
DhakaT. annulata and T. mutansMicroscopyCattle1989[196]
Dhaka, Sirajganj and NikhangsoriT. annulataMicroscopy & MolecularCattle goats & Sheep2019[194]
Goats & Sheep
DhakaTheileria spp.Microscopy & MolecularGoats2021[189]
South Eastern Region
ChittagongTheileria spp.MicroscopyCattle2010[190]
North Central Region
SirajganjTheileria spp.MicroscopyCattle2015[187]
SirajganjT. annulata & T. mutansMicroscopyCattle1976[186]
SirajganjT. annulataMolecularCattle1977[197]
MymensinghT. orientalisMolecularCattle2018[188]
Northern Region
Dinajpur Theileria spp.MicroscopyCattle2016[191]
Western region
RajshahiT. annulataMolecularCattle2016[192]
NatoresT. annulataMolecularCattle2019[193]
Table
Table 7. Distribution of possible tick vectors for Theileria species in various regions of Bangladesh.
Table 7. Distribution of possible tick vectors for Theileria species in various regions of Bangladesh.
DivisionsPossible Tick VectorReference
Braisel, Dhaka, Savar, Narayanganj, TangaliR. microplus[102]
Dhaka, Rajshahi, SavarHae. bispinosa[102]
North western dry Region (Rajshahi, Rangpur, and Dinajpur districts)Hy. anatolicum anatolicum[102]
SavarHy. Truncatum[102]
Braisal, Chitagang, Dhaka, Narayanganj, Tangail, Rangpur, SylhetR. sanguineus[102]
Table
Table 8. Common tick species in different hosts in Bangladesh.
Table 8. Common tick species in different hosts in Bangladesh.
Possible Tick Vectors for TTHostReferences
R. microplus, Hae. bispinosa, R. sanguineus, Hy. anatolicum anatolicumCattle & Buffaloes[102]
R. sanguineus, Hy. anatolicum anatolicumGoats & Sheep[102]
Table
Table 9. Evolutionary divergence analysis of T. annulata 18S rRNA gene isolates.
Table 9. Evolutionary divergence analysis of T. annulata 18S rRNA gene isolates.
123456789
MF287947.1 T annulata Central India
MF287920.1 T annulata West India0.58
MF287949.1 T annulata Eastern India0.620.22
MF287937.1 T annulata South India0.630.250.19
MF287934.1 T annulata North India0.580.160.190.28
JQ743631.1 T annulata Pakistan0.40.550.590.60.56
JQ743636.1 T annulata Pakistan0.70.60.630.0650.60.5
MW046053.1 T annulata Pakistan2.141.654.74.70.650.120.15
MW046054.1 T annulata Pakistan0.90.572.633.620.573.80.110.0_
123456789
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Zeb, J.; Song, B.; Aziz, M.U.; Hussain, S.; Zarin, R.; Sparagano, O. Diversity and Distribution of Theileria Species and Their Vectors in Ruminants from India, Pakistan and Bangladesh. Diversity 2022, 14, 82. https://doi.org/10.3390/d14020082

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Zeb J, Song B, Aziz MU, Hussain S, Zarin R, Sparagano O. Diversity and Distribution of Theileria Species and Their Vectors in Ruminants from India, Pakistan and Bangladesh. Diversity. 2022; 14(2):82. https://doi.org/10.3390/d14020082

Chicago/Turabian Style

Zeb, Jehan, Baolin Song, Muhammad Umair Aziz, Sabir Hussain, Riaz Zarin, and Olivier Sparagano. 2022. "Diversity and Distribution of Theileria Species and Their Vectors in Ruminants from India, Pakistan and Bangladesh" Diversity 14, no. 2: 82. https://doi.org/10.3390/d14020082

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