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First molecular identification of multiple tick-borne pathogens in livestock within Kassena-Nankana, Ghana


The risk of pathogen transmission continues to increase significantly in the presence of tick vectors due to the trade of livestock across countries. In Ghana, there is a lack of data on the incidence of tick-borne pathogens that are of zoonotic and veterinary importance. This study, therefore, aimed to determine the prevalence of such pathogens in livestock using molecular approaches. A total of 276 dry blood spots were collected from cattle (100), sheep (95) and goats (81) in the Kassena-Nankana Districts. The samples were analyzed using Polymerase Chain Reaction (qPCR) and conventional assays and Sanger sequencing that targeted pathogens including Rickettsia, Coxiella, Babesia, Theileria, Ehrlichia and Anaplasma. An overall prevalence of 36.96% was recorded from the livestock DBS, with mixed infections seen in 7.97% samples. Furthermore, the prevalence of infections in livestock was recorded to be 19.21% in sheep, 14.13% in cattle, and 3.62% in goats. The pathogens identified were Rickettsia spp. (3.26%), Babesia sp. Lintan (8.70%), Theileria orientalis (2.17%), Theileria parva (0.36%), Anaplasma capra (18.48%), Anaplasma phagocytophilum (1.81%), Anaplasma marginale (3.26%) and Anaplasma ovis (7.25%). This study reports the first molecular identification of the above-mentioned pathogens in livestock in Ghana and highlights the use of dry blood spots in resource-limited settings. In addition, this research provides an update on tick-borne pathogens in Ghana, suggesting risks to livestock production and human health. Further studies will be essential to establish the distribution and epidemiology of these pathogens in Ghana.


In Africa, the high demand for animal food products due to fast population development has spurred cross-regional livestock commerce leading to an increased risk of animal disease transmission (Volkova et al. 2010; Fèvre et al. 2006). Global transhumance is also associated with animal movements in Sub-Saharan Africa (Motta et al. 2018). It is common for herders to engage in cross-border migration with their livestock to efficiently use seasonal pasture resources (Lesse et al. 2016). Even though such activities could facilitate the spread of infectious pathogens, disease surveillance is poor or nonexistent near the borders of many Sub-Saharan African countries (Motta et al. 2017). The cross-border livestock trade has introduced exotic tick species and associated infections into naïve countries.

The situation in the Upper East Region of Ghana is somewhat similar, given the trade of livestock across the borders of Ghana and Burkina Faso, with no measures to prevent the spread of infectious diseases. The residents of this area are extensively involved in livestock rearing, which provides a food source and income. However, because zoonotic diseases frequently afflict people who interact with animals, these animals may act as amplifying hosts for zoonotic pathogens, placing owners at risk of becoming infected (Al-Tayib 2019). Animals are the source of various new and emerging pathogenic zoonotic diseases (Daszak et al. 2001; Taylor et al. 2001), with human activities serving as the primary drivers of their spread (Jones et al., 2013; Karesh et al., 2012). More importantly, increased livestock production, especially near wildlife habitats, has allowed disease interchange, with livestock serving as reservoirs for human zoonoses (Jones et al., 2013; Karesh et al., 2012). Furthermore, the rapid transmission of infections over long distances can be aided by animal movements inside countries and across borders (Dean et al. 2013; Fèvre et al. 2006).

In Sub-Saharan Africa, the health and productivity of livestock are greatly affected by ticks and tick-borne diseases (Jongejan and Uilenberg 2004). Babesiosis, anaplasmosis, theileriosis and ehrlichiosis are the most common tick-borne diseases in Sub-Saharan Africa, harming livestock health and incurring production losses (Morrison 2015). Climate change and the global trade of animals, according to studies, aid tick species invasion and the spread of infectious pathogens into new locations (Byamukama et al. 2021). This will most certainly increase tick-borne diseases in livestock and make pathogen transmission between wildlife and domestic animals easier (Espinaze et al. 2018; Hassell et al. 2017; Olwoch et al. 2008). It is important to note that Babesia, Theileria and Anaplasma have been identified to infect livestock in Ghana (Ayeh-Kumi et al. 2022; Beckley et al. 2016).

In resource-limited settings, the use of dry blood spots (DBS) in surveillance efforts to diagnose infectious diseases comes with some advantages, including the non-invasive collection of blood, less volume of blood required, easy transport, and the long-term storage of the blood spots (Grüner, Stambouli, and Ross 2015; Gupta and Mahajan 2018). Even though some factors such as the method of sample preparation and storage conditions could influence the results obtained using DBS (Lim 2018), studies have successfully identified tick-borne pathogens in livestock DBS (Tigani-asil et al. 2021; Roy et al. 2018). This study employed the use of DBS to determine the prevalence of tick-borne pathogens of zoonotic and veterinary importance in livestock. There is limited information on the distribution and epidemiology of these pathogens in Ghana. Findings from this study will be essential in formulating control measures, especially with the constant movement of livestock and humans.


A total of 276 DBS were collected from physically healthy livestock across the Kassena-Nankana district. The livestock sampled were Cattle (n = 100; 36.23%), Sheep (n = 95; 34.42%) and Goats (n = 81; 29.35%). These livestock were sampled from Navrongo (n = 246), Nakong (n = 10) and Pungu (n = 20). Overall, 102 (36.96%) livestocks were infected with tick-borne pathogens. Furthermore, the prevalence of tick-borne infections in livestock was recorded in sheep (19.21%), cattle (14.13%), and goats (3.62%). Also, all the sampled locations recorded at least one tick-borne pathogen, with the most diverse pathogens recorded from the Abattoir (Tables 1 and 2). No Coxiella burnetii or Ehrlichia pathogens were detected.

Table 1 Livestock characteristics and parasitic tick-borne pathogens prevalence
Table 2 Livestock characteristics and bacterial tick-borne pathogens prevalence

Prevalence of tick-borne pathogens

An overall prevalence of 3.26% was recorded for Rickettsia DNA in the livestock examined. Prevalence rates were recorded as 1.49% in cattle, 1.12% in goats, and 0.75% in sheep. However, the positive samples could not be characterized to determine the specific Rickettsia species. This could be due to insufficient DNA in the PCR products that were sequenced.

Initial screening of the samples showed that 37 (13.41%) were positive for Babesia/Theileria with an infection rate of 24% (95% CI, 15.39–34.33) in cattle and 13.68% (95% CI, 7.09–22.79) in sheep. No infections were detected in goats. Sequencing of the positive PCR products resulted in identifying Theileria orientalis (2.17%), Theileria parva (0.36%) and an unclassified Babesia designated as Babesia sp. Lintan (8.70%). BLAST analysis showed that the Babesia/Theileria positive samples in this study were 82–94% similar to Babesia and Theileria isolated in China and East and Southern Africa. From the phylogenetic analysis, the samples LK-B41, LK-B42 and LK-B44 clustered with isolates from China (accession numbers KX698109.1 and MK962313.1) with 99% bootstrap support (Fig. 1a). However, all the samples LK-B50, LK-B51 and LK-B53 clustered with a bootstrap value of 100% (Fig. 1b).

Fig. 1
figure 1

Phylogenetic analysis of Babesia and Theileria in the livestock based on the rRNA gene fragments (lsu5-lsu4) of mitochondrial genome. a Babesia. The sequences obtained in this study are indicated as LK-B41, LK-B42 and LK-B44. Theileria. The sequences obtained in this study are indicated as LK-B50, LK-B51 and LK-B53

From the 276 livestock samples examined, 85 (30.80%) were positive for Ehrlichia/Anaplasma. The highest prevalence rate was observed in sheep (18.84%), followed by cattle (9.42%) and goats (2.54%). It was observed that all positive samples were Anaplasma species after sequencing. The pathogens identified were Anaplasma capra (18.48%), Anaplasma ovis (7.25%), Anaplasma marginale (3.26%) and Anaplasma phagocytophilum (1.81%). BLAST analysis showed that the Anaplasma samples were 98–99% similar to isolates from Hungary, Panama, South Korea, and South Africa. Furthermore, from the phylogenetic analysis, all the Anaplasma samples (LK-A1, LK-A9, LK-A10 and LK-A15) clustered with isolates from France (accession number MF580636.1), Nigeria (accession numbers JF949765.1 and JF949768.1) and Burkina Faso (accession number MT259778.1) with 100% bootstrap support (Fig. 2).

Fig. 2
figure 2

Phylogenetic analysis of Anaplasma in the livestock based on the 16S rRNA gene. The sequences obtained in this study are indicated as LK-A1, LK-A9, LK-A10 and LK-A15

Characteristics of tick-borne pathogens in sampled livestock

A significant association was observed between the parasitic pathogen Babesia sp. Lintan and the animal host, sex and age (p < 0.001). Male cattle between the ages of 2–5 years were the most infected with Babesia sp. Lintan (Table 1). Furthermore, bacterial pathogens A. capra and A. ovis were significantly associated with animal hosts (p < 0.001), with most infections recorded in sheep at 32.63 and 15.79%, respectively (Table 2).

Single bacterial infections were recorded in 30.8% livestock DBS, with 1.81% having coinfection. Additionally, 10.87% sampled livestock had one parasite infection without coinfections. In the Livestock, DBS, single bacterial or parasite infections were reported at 30.43%, with bacterial and parasitic coinfections at 6.52%. Sheep were the most often infected livestock host, and there was a strong correlation between bacterial infections and hosts (p < 0.001).

Additionally, it was discovered that parasitic infections had a highly significant (p < 0.001) correlation with age and the hosts. The majority of parasitic infections occurred in cattle (21%) between the ages of 2–5 years (26.47%) (Table 3). However, a substantial correlation was also found between disease with bacteria or parasites and the cattle hosts (p < 0.001).

Table 3 Bacterial and parasitic pathogens in association with livestock characteristics

According to the risk analysis, no livestock attribute (age, sex or animal host) was found to significantly increase the likelihood of contracting a bacterial or parasitic tick-borne infection (Table 4).

Table 4 Multivariable multinomial logistic regression model for tick-borne bacterial and parasitic pathogens


Small-scale livestock producers in developing countries contribute significantly to agricultural production and rural development (McDermott et al. 2010). However, due to the cost of acaricides, tick infestations are not adequately controlled, especially during the rainy season (Achukwi et al. 2001), leading to an increase in tick-borne diseases infecting animals (Dantas-Torres, Chomel, and Otranto 2012).

In sub-Saharan Africa, Rickettsia infections have been identified in animals and humans, with ticks playing the role of principal vectors (Parola et al., 2013). Ticks are natural reservoir hosts of Rickettsia (Piotrowski and Rymaszewska 2020) with sparse knowledge of animals as potential reservoirs. In Spain, researchers detected Rickettsia infection in a goat blood sample, suggesting the risk of transmission to humans (Ortuño et al. 2012). Likewise, Rickettsia was found in Sika deer in Japan (Inokuma et al. 2008). In a study from China, domestic animals, including cattle and goats, were found infected with Rickettsia (Liang et al. 2012). Findings from this study indicate Rickettsia DNA in all the types of livestock sampled. Even though animals are not considered reservoir hosts of Rickettsia, they could amplify the pathogen and infect feeding ticks and humans.

An estimated 2 billion cattle are at risk of babesiosis exposure despite the efforts in research and preventive measures (Gohil et al. 2013; Bock et al. 2004). In Africa, B. bovis and B. bigemina transmitted by Rhipicephalus ticks cause bovine babesiosis (Bock et al. 2004). Although bovine infections are predominantly caused by B. bigemina, B. bovis infections are fatal due to neurological symptoms (Uilenberg 2006). In this study, cattle and sheep were infected with Babesia sp. Lintan. It causes moderate to severe infections in sheep and goats (Wang et al. 2020; A. H. Liu et al. 2007; Niu et al. 2009). This study reports the first molecular detection of Babesia sp. Lintan infections in livestock in Ghana. With no record of infections in cattle, there is a need to determine the epidemiology of Babesia sp. Lintan in cattle production. Symptoms of infections such as anemia, hemoglobinuria, fever and jaundice in sheep and goats could be similar to that in cattle since they are ruminants. The detection of B. bigemina (Bell-Sakyi et al. 2004) and B. bovis (Nagano et al. 2013), coupled with the identification of Babesia sp. Lintan suggests multiple Babesia species are in circulation within Ghana.

In animals, Theileria infections are either asymptomatic or severe, with fever, hemoglobinuria, anemia and death (Zhang et al., 2015). An animal can become infected for life, serving as a reservoir host for tick species (Glass 2001; Ahmed et al. 2008). Most cases of animal infections originate from the tropical and subtropical zones in Asia, Africa, Southern Europe and the Middle East (Sivakumar et al. 2014; Rjeibi et al. 2016; Belotindos et al. 2014; Hussain et al. 2014). In Africa, theileriosis is a significant tick-borne disease that affects domestic ruminants (Clift et al. 2020) with varying mortality and morbidity rates (Mans, Pienaar, and Latif 2015). Many African countries have reported the occurrence of Tropical theileriosis caused by T. annulata and East Coast fever (ECF) caused by T. parva (Moumouni et al., 2015). Theileria mutans, T. velifera and T. orientalis have been reported in Africa (Moumouni et al., 2015; Perveen et al., 2021) to be less pathogenic (Kalume, Losson, and Saegerman 2011). In Ghana, T. mutans and T. velifera have been identified in domestic ruminants (Bell-Sakyi et al. 2004). This study reports the first molecular identification of T. parva and T. orientalis in sheep from Ghana. Theileria parva causes significant cattle deaths (Nene et al., 2016) and further hinders livestock production in numerous African countries (Mukhebi, Perry, and Kruska 1992; Kivaria 2006; McKeever 2009). Theileria parva is thought to kill over a million cattle annually, costing at least $300,000,000 in lost revenue (Nene et al., 2016). Additionally, livestock production is hampered by sick animals’ slower growth, lower productivity, and the high costs of disease control (McKeever 2009; Kivaria 2006). It is thought that T. parva evolved from resistant African Cape buffalo to finally infect cattle with East Coast fever (Norval, Perry, and Young 1992). Africa’s cattle production has suffered greatly as a result of T. parva in nations including Zambia, Uganda, Zimbabwe, Kenya, Rwanda, Burundi, and Sudan (Mukhebi, Perry, and Kruska 1992).

Although T. orientalis infections are often mild (Aktas, Altay, and Dumanli 2006), reports link the pathogen to sporadic outbreaks that cause clinical signs and notable losses (Kamau et al. 2011; Perera et al. 2014). Mild infections produce symptoms such as anemia and hypoxia, whiles severe conditions result in weakness, pyrexia, and occasionally abortion (Lawrence et al. 2018; Swilks et al. 2017). Furthermore, hosts’ compromised immune system and stress are associated with most clinical cases of T. orientalis infection (Watts, Playford, and Hickey 2016). From interactions with livestock owners in the Kassena-Nankana Districts, it was observed that Ivermectin is typically used to treat their cattle. According to a study, Ivermectin protects against T. orientalis infection in cattle (Park et al., 2019). The use of Ivermectin may explain why the studied cattle did not have any T. orientalis infections. However, infectious diseases are likely to be exchanged because of the frequent interaction between the animals in the Kassena-Nankana Districts.

In this study, A. phagocytophilum, A. capra, A. ovis and A. marginale were identified in the sampled livestock. This finding supports studies that indicate these Anaplasma pathogens infect animals (Niaz et al. 2021; Renneker et al. 2013). However, due to A. marginale and A. ovis, the livestock industry experiences huge financial losses on a global scale (Z. Liu et al. 2012; Kocan et al. 2003). While A. ovis is only moderately detrimental to goats and sheep (Seong et al. 2015), A. marginale can result in lethal acute anaplasmosis (Abdullah et al. 2020).

According to reports from Ghana (Futse et al. 2019), South Africa (Hove et al. 2018), Madagascar, Uganda (Byaruhanga et al. 2018; Muhanguzi et al. 2010), Thailand (Jirapattharasate et al. 2017) and China (Yang et al. 2017), A. marginale has been found in cattle. Anaplasma marginale has been detected in sheep (Yousefi et al. 2017) and goats (Barbosa et al. 2021; Da Silva et al. 2018), as seen in this study, despite having a substantial impact on cattle production globally (Kocan et al. 2010). Animals with infections produce less milk, have abortions, and face death (Kumar et al., 2015). There is a higher likelihood of disease transmission among the animals in the study areas because ruminants frequently interact with one another. Additionally, animals that recover from severe A. marginale infections function as reservoir hosts and spread the disease to attached ticks (Eriks, Stiller, and Palmer 1993; Kieser, Eriks, and Palmer 1990).

Cattle and sheep were discovered to be infected with A. ovis in this study. There have been reports of A. ovis infections in sheep and goats across Africa, Europe, Asia and North America (Yin and Luo 2007; Han et al. 2017). Finding A. ovis in sheep can be compared to studies in Sudan (Lee et al. 2018), Tunisia (Said et al. 2015), Senegal (Dahmani et al. 2019), West Iran (Mohammadian, Noaman, and Emami 2021), and Uganda (Kasozi et al. 2021) which recorded a higher prevalence of infections. The variations in A. ovis prevalence may be caused by stress factors such as coinfection and a dry and hot climate (Renneker et al. 2013). Given the zoonotic nature of the disease as described in Iran, the aforementioned reports indicate that A. ovis has a major impact on the production of small ruminants and poses a risk to those who handle animals (Hosseini-Vasoukolaei et al. 2014). The experimental infection of various wild ruminants with A. ovis illustrates the pathogen’s diverse host range (la Fuente et al., 2006; Zaugg, 1987, 1988; Zaugg et al., 1996). This, coupled with the continuous interactions amongst the ruminants in the Kassena-Nankana Districts, may be the cause of finding cattle with A. ovis infections.

This study reports the first detection of A. phagocytophilum in cattle from Ghana. A zoonotic pathogen with a broad host range, A. phagocytophilum can infect both domestic and wild animals and humans (Fuente et al., 2005; Dumler et al., 2001; Zhan et al., 2010). This pathogen causes infections that induce respiratory symptoms, fever, infertility, and decreased milk production in afflicted cattle (Noaman and Shayan 2009).

In addition, infections caused by A. phagocytophilum can be mild to severe, leading to multiple organ failures and death (Battilani et al., 2017; Li et al., 2015). Ticks from Kenya (Mwamuye et al. 2017), Tunisia (Sarin et al. 2005), livestock in Uganda (Muhanguzi et al. 2010), and ticks and cattle in Ethiopia (Teshale et al. 2018; Teshale et al., 2015) have all been found to carry this zoonotic pathogen. Infection with A. phagocytophilum in cattle from this investigation was lower than that reported in Iran (Mohammadian, Noaman, and Emami 2021), Uganda (Muhanguzi et al. 2010), Ethiopia (Teshale et al., 2018), and China (Zhou et al. 2019). However, it was higher than a study from Tunisia that found a prevalence rate of 0.6% in cattle for A. phagocytophilum (M’Ghirbi et al., 2016). Even though several tick-borne pathogens cause diseases in Africa (Kocan, Blouin, and Barbet 2000), there is little evidence to support the distribution of A. phagocytophilum. This is most likely because no reliable diagnostic methods are available (Stuen, Granquist, and Silaghi 2013). People who work closely with animals or reside in rural areas with tick-friendly habitats are more likely to contract the disease (Thomas, Dumler, and Carlyon 2009).

Additionally, this study also reports the first identification of A. capra in cattle, sheep and goats in the Kassena-Nankana District. This zoonotic pathogen infects humans, ruminants, and wild animals (Amer et al., 2019; Jouglin et al., 2019; Li et al., 2015; Peng et al., 2018). After A. capra was first discovered in asymptomatic goats, a case of human infection was later reported from China in 2015 (Li et al., 2015). Anaplasma capra was more prevalent in this investigation than in studies from China (Peng et al. 2018) and Turkey (Altay, Erol, and Sahin 2022).

Infections with A. capra in sheep and goats can range from mild to severe, with symptoms such as fever, weight loss, decreased milk production, miscarriage and death (Said et al., 2018; Yasini et al., 2012). Numerous hard tick species can carry and spread A. capra to zoonotic and domestic hosts (Guo et al., 2019; Segura et al., 2020; Seo et al., 2018; Yang et al., 2016). This pathogen thus poses a serious risk to public health, necessitating the development of efficient preventative and control methods. Anaplasma prevalence may be impacted by husbandry practices, according to some observations (Fuente et al., 2005). Suitable husbandry methods and tick control measures will help stop the spread of the Anaplasma pathogens and lessen the risk to animal and human health.


This study demonstrates the use of DBS in the surveillance of tick-borne pathogens in livestock. Pathogens of zoonotic and veterinary importance were identified primarily in the abattoir. Among these pathogens were Anaplasma capra and Anaplasma phagocytophilum which can cause infections in animals and humans. Poor tick prevention increases the risk of infections among the district’s Abattoir workers and animal handlers. It is evident that the trade of livestock across borders has an influence on the distribution and spread of tick-borne pathogens. As such, there is a need for effective measures to control tick populations that will prevent the spread of tick-borne pathogens to humans and animals. Furthermore, there is a need to educate the abattoir workers on hygienic practices and the use of personal protective equipment to reduce the risk of infections.


Study area and ethical approval

The study was conducted in seven locations within the Kassena-Nankana districts of Ghana. Sampling sites included the abattoir, where livestock from within the community and beyond are slaughtered daily. Other locations were based on livestock availability and the animal owners’ willingness to allow sample collections. Tick species including Amblyomma variegatum, Rhipicephalus sanguineus, Hyalomma truncatum, Hyalomma rufipes, Rhipicephalus evertsi and Rhipicephalus (Boophilus) sp. are prevalent in the Kassena-Nankana districts (Paintsil et al. 2022).

Before this study, ethical approval was obtained from the University of Ghana Institutional Animal Care and Use Committee (UG-IACUC; UG-IACUC 001/19–20). After verbal consent from the livestock owners, the animals were restrained with the help of the owners, and samples were collected under the instruction of a local veterinarian.

Sample collection

A minimum of 248 livestock was required for this study using Epi Info V. 6. The sample size was calculated based on the following assumptions; a population size of 5000 livestock (local veterinarian estimate), a prevalence rate was 21.6% (Johnson et al. 2019), and a 95% confidence level with a 5% error margin. The breed of livestock was not taken into consideration in this study. The livestock included in this study were physically examined to be healthy by the attending Veterinarian before the blood sample collection.

At the abattoir, blood samples were collected from the slaughtered livestock and spotted onto labelled FTA Gene cards (GE Whatman, Maidstone, Kent, United Kingdom), air-dried overnight, and stored in sample bags containing silica gel. Within the communities, each animal was restrained, and the blood collection area (facial vein) was disinfected. Using animal lancets (Goldenrod™ Animal Lancet, Medipoint, NY, USA) blood was drawn and spotted on FTA cards. The cards were subsequently dried overnight and stored in sample bags containing silica gel. All the samples were then transported to the laboratory and stored at -80°C pending analysis.

DNA extraction and molecular analysis

DNA was extracted from the livestock dried blood spots using Qiagen DNA Mini Kit (Qiagen Inc. Hilden, Germany) according to the manufacturer’s instructions. The extracted DNA was screened for Coxiella burnetii using an IS1111 assay that targets the 295 bp fragment of the transposase gene of C. burnetii IS1111a element (Klee et al. 2006) (see Additional file 1).

Again, Rickettsia DNA was detected in the livestock DBS using a quantitative PCR which targets the 115 bp fragment of the 17 kDa surface protein of Rickettsia species (Jiang et al., 2004). Samples that were Rickettsia positive were subsequently characterized using primers that target the rOmpA gene (ompA) of Rickettsia amplifying at 632 bp (J Jiang et al. 2005) (see Additional file 2). To identify Babesia/Theileria in the samples, a conventional PCR that amplifies the 150 bp fragment of rRNA gene fragments (lsu5-lsu4) of the Babesia mitochondrial genome (Qurollo et al. 2017) as well as other apicomplexan pathogens was performed (see Additional file 3). Furthermore, Ehrlichia and Anaplasma DNA were detected in the samples using conventional PCR that amplifies the 345 bp fragment of the Ehrlichia genus 16SrRNA gene (Nazari et al. 2013). The primers used in the PCR reaction were designed to amplify a wider spectrum of organisms in the Ehrlichia and Anaplasma genera (see Additional file 4). All positive PCR products were shipped to Macrogen Europe B.V. (Amsterdam, the Netherlands) for Sanger sequencing.

Phylogenetic analysis

The sequences obtained in this study were mapped to similar sequences in the NCBI database, including reference sequences. Sequences were further aligned using the Clustal Omega tool in MEGA X (Kumar et al. 2018). The relationships between the isolates were determined using phylogenetic trees created in MEGA X based on the Neighbour-joining method.

Statistical analysis

Chi-square analysis was used to determine the association between parasite/bacterial infection status with livestock characteristics. Logistic or multinomial regression was fitted to parasite/bacterial infection status with the animal characteristics. The statistical level was set at p < 0.05 and analysis was performed using STATA version 13.

Availability of data and materials

All the data supporting this study are included in the article.


  • Abdullah, Donea Abdulrazak, Fawwaz Fadhil Ali, Afrah Younis Jasim, Shola David Ola-Fadunsin, Fufa Ido Gimba, and Moeena Sadeq Ali. 2020. Clinical signs, prevalence, and Hematobiochemical profiles associated with Anaplasma infections in sheep of North Iraq. Veterinary World 13 (8): 1524–1527.

    Article  Google Scholar 

  • Achukwi, M.D., V.N. Tanya, O. Messiné, and L.M. Njongmeta. 2001. Comparative study of the infestation of Namchi (Bos Taurus) and Ngaoundere Gudali (Bos Indicus) cattle by Amblyomma Variegatum adult ticks. Revue d’élevage et de Médecine Vétérinaire Des Pays Tropicaux 54 (1): 37–41.

  • Ahmed, Jabbar S., Elizabeth J. Glass, Diaeldin A. Salih, and Ulrike Seitzer. 2008. Innate immunity to tropical Theileriosis. Innate Immunity 14 (1): 5–12.

    Article  CAS  Google Scholar 

  • Aktas, Munir, Kursat Altay, and Nazir Dumanli. 2006. A molecular survey of bovine Theileria parasites among apparently healthy cattle and with a note on the distribution of ticks in eastern Turkey. Veterinary Parasitology 138 (3–4): 179–185.

  • Altay, Kursat, Ufuk Erol, and Omer Faruk Sahin. 2022. The first molecular detection of Anaplasma Capra in domestic ruminants in the central part of Turkey, with genetic diversity and genotyping of Anaplasma Capra. Tropical Animal Health and Production 54 (2).

  • Al-Tayib, Omar A. 2019. An overview of the most significant zoonotic viral pathogens transmitted from animal to human in Saudi Arabia. Pathogens 8 (1): 25.

  • Amer, Said, Sungryong Kim, Youngmin Yun, and Ki Jeong Na. 2019. Novel variants of the newly emerged Anaplasma Capra from Korean water deer (Hydropotes Inermis Argyropus) in South Korea. Parasites and Vectors 12 (1): 1–9.

  • Ayeh-Kumi, Patrick F., Irene A. Owusu, Patience B. Tetteh-Quarcoo, Nicholas T.K.D. Dayie, Kevin Kofi Adutwum-Ofosu, Seth K. Amponsah, Emilia A. Udofia, et al. 2022. Preliminary investigation into plasmodium-like Piroplasms (Babesia/Theileria) among cattle, dogs and humans in a malaria-endemic, resource-limited sub-Saharan African City. Medical Science 10 (1): 10.

  • Barbosa, Iago C., Marcos R. André, Renan Bressianini do Amaral, Jessica D.M. Valente, Priscylla C. Vasconcelos, Celso J.B. Oliveira, Marcia Mariza Gomes Jusi, et al. 2021. Anaplasma Marginale in goats from a multispecies grazing system in northeastern Brazil. Ticks and Tick-Borne Diseases 12 (1).

  • Battilani, Mara, Stefano De Arcangeli, Andrea Balboni, and Francesco Dondi. 2017. Genetic diversity and molecular epidemiology of Anaplasma. Infection, Genetics and Evolution 49: 195–211.

  • Beckley, Carl S., Salisu Shaban, Guy H. Palmer, Andrew T. Hudak, Susan M. Noh, and James E. Futse. 2016. Disaggregating tropical disease prevalence by climatic and vegetative zones within tropical West Africa. PLoS One 11 (3): 1–13.

  • Bell-Sakyi, L., E.B.M. Koney, O. Dogbey, and A.R. Walker. 2004. Incidence and prevalence of tick-borne Haemoparasites in domestic ruminants in Ghana. Veterinary Parasitology 124 (1–2): 25–42.

  • Belotindos, Lawrence P., Jonathan V. Lazaro, Marvin A. Villanueva, and Claro N. Mingala. 2014. Molecular detection and characterization of Theileria species in the Philippines. Acta Parasitologica 59 (3): 448–453.

    Article  CAS  Google Scholar 

  • Bock, R., L. Jackson, A. de Vos, and W. Jorgensen. 2004. Babesiosis of cattle. Parasitology 129: S247–S269.

    Article  Google Scholar 

  • Byamukama, Benedicto, Patrick Vudriko, Maria Agnes Tumwebaze, Dickson Stuart Tayebwa, Joseph Byaruhanga, Martin Kamilo Angwe, Jixu Li, et al. 2021. Molecular Ddetection of selected tick-borne pathogens infecting cattle at the wildlife–livestock interface of Queen Elizabeth National Park in Kasese District, Uganda. Ticks and Tick-Borne Diseases 12 (5): 101772.

    Article  Google Scholar 

  • Byaruhanga, Charles, Nicola E. Collins, Darryn L. Knobel, Zamantungwa T.H. Khumalo, Mamohale E. Chaisi, and Marinda C. Oosthuizen. 2018. Molecular detection and phylogenetic analysis of Anaplasma Marginale and Anaplasma Centrale amongst transhumant cattle in north-eastern Uganda. Ticks and Tick-Borne Diseases 9 (3): 580–588.

    Article  Google Scholar 

  • Clift, Sarah J., Nicola E. Collins, Marinda C. Oosthuizen, Johan C.A. Steyl, John A. Lawrence, and Emily P. Mitchell. 2020. The pathology of pathogenic Theileriosis in African wild artiodactyls. Veterinary Pathology 57 (1): 24–48.

    Article  CAS  Google Scholar 

  • Dahmani, Mustapha, Bernard Davoust, Masse Sambou, Hubert Bassene, Pierre Scandola, Tinhinene Ameur, Didier Raoult, Florence Fenollar, and Oleg Mediannikov. 2019. Molecular investigation and phylogeny of species of the Anaplasmataceae infecting animals and ticks in Senegal. Parasites and Vectors 12 (1): 1–15.

    Article  CAS  Google Scholar 

  • Dantas-Torres, Filipe, Bruno B. Chomel, and Domenico Otranto. 2012. Ticks and tick-borne diseases: A one health perspective. Trends in Parasitology 28 (10): 437–446.

    Article  Google Scholar 

  • Daszak, P., A.A. Cunningham, and A.D. Hyatt. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78: 103–116.

    Article  CAS  Google Scholar 

  • Dean, Anna S., Guillaume Fournié, Abalo E. Kulo, G. Aboudou Boukaya, Esther Schelling, and Bassirou Bonfoh. 2013. Potential risk of regional disease spread in West Africa through cross-border cattle trade. PLoS One 8 (10): 1–9.

    Article  CAS  Google Scholar 

  • Dumler, J.S., A.F. Barbet, C.P.J. Bekker, G.A. Dasch, G.H. Palmer, S.C. Ray, Y. Rikihisa, and F.R. Rurangirwa. 2001. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: Unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combi. International Journal of Systematic and Evolutionary Microbiology 51 (6): 2145–2165.

    Article  CAS  Google Scholar 

  • Eriks, I.S., D. Stiller, and G.H. Palmer. 1993. Impact of persistent Anaplasma Marginale Rickettsemia on tick infection and transmission. Journal of Clinical Microbiology 31 (8): 2091–2096.

    Article  CAS  Google Scholar 

  • Espinaze, Marcela P.A., Eléonore Hellard, Ivan G. Horak, and Graeme S. Cumming. 2018. Domestic mammals facilitate tick-borne pathogen transmission networks in south African wildlife. Biological Conservation 221: 228–236.

    Article  Google Scholar 

  • Fèvre, Eric M., Barend M. de C. Bronsvoort, Katie A. Hamilton, and Sarah Cleaveland. 2006. Animal movements and the spread of infectious diseases. Trends in Microbiology 14 (3): 125–131.

    Article  CAS  Google Scholar 

  • Fuente, La, José De, Robert F. Massung, Susan J. Wong, Frederick K. Chu, Hans Lutz, Marina Meli, Friederike D. Von Loewenich, et al. 2005. Sequence analysis of the Msp4 gene of Anaplasma Phagocytophilum strains. Journal of Clinical Microbiology 43 (3): 1309–1317.

    Article  CAS  Google Scholar 

  • Futse, James E., Grace Buami, Boniface B. Kayang, Roberta Koku, Guy H. Palmer, Telmo Graca, and Susan M. Noh. 2019. Sequence and immunologic conservation of Anaplasma Marginale OmpA within strains from Ghana as compared to the predominant OmpA variant. PLoS Neglected Tropical Diseases 14 (7): e0217661.

    Article  CAS  Google Scholar 

  • Glass, E.J. 2001. The balance between protective immunity and pathogenesis in tropical Theileriosis: What we need to know to design effective vaccines for the future. Research in Veterinary Science 70 (1): 71–75.

    Article  CAS  Google Scholar 

  • Gohil, Sejal, Susann Herrmann, Svenja Günther, and Brian M. Cooke. 2013. Bovine Babesiosis in the 21st century: Advances in biology and functional genomics. International Journal for Parasitology 43 (2): 125–132.

    Article  CAS  Google Scholar 

  • Grüner, Nico, Oumaima Stambouli, and R. Stefan Ross. 2015. Dried blood spots - preparing and processing for use in immunoassays and in molecular techniques. Journal of Visualized Experiments 97: e52619.

    Article  CAS  Google Scholar 

  • Guo, Wen Ping, Bing Zhang, Yi Han Wang, Xu Gang, Xiaoquan Wang, Xuebing Ni, and En Min Zhou. 2019. Molecular identification and characterization of Anaplasma Capra and Anaplasma platys-like in Rhipicephalus microplus in Ankang, Northwest China. BMC Infectious Diseases 19 (1): 1–9.

    Article  CAS  Google Scholar 

  • Gupta, Kapil, and Rajiv Mahajan. 2018. Prucalopride: A recently approved drug by the Food and Drug Administration for chronic idiopathic constipation. International Journal of Applied and Basic Medical Research 8 (1): 1–2.

    Article  Google Scholar 

  • Han, Rong, Jifei Yang, Zhijie Liu, Shaodian Gao, Qingli Niu, Muhammad Adeel Hassan, Jianxun Luo, and Hong Yin. 2017. Characterization of Anaplasma Ovis strains using the major surface protein 1a repeat sequences. Parasites and Vectors 10 (1): 6–11.

    Article  CAS  Google Scholar 

  • Hassell, James M., Michael Begon, Melissa J. Ward, and Eric M. Fèvre. 2017. Urbanization and disease emergence: Dynamics at the wildlife–livestock–human Interface. Trends in Ecology and Evolution 32 (1): 55–67.

    Article  Google Scholar 

  • Hosseini-Vasoukolaei, Nasibeh, Mohammad Ali Oshaghi, Parviz Shayan, Hassan Vatandoost, Farhang Babamahmoudi, Mohammad Reza Yaghoobi-Ershadi, Zakkyeh Telmadarraiy, and Fatemeh Mohtarami. 2014. Anaplasma infection in ticks, livestock and human in Ghaemshahr, Mazandaran Province, Iran. Journal of Arthropod-Borne Diseases 8 (2): 204–211.

    Google Scholar 

  • Hove, Paidashe, Mamohale E. Chaisi, Kelly A. Brayton, Hamilton Ganesan, Helen N. Catanese, Moses S. Mtshali, Awelani M. Mutshembele, Marinda C. Oosthuizen, and Nicola E. Collins. 2018. Co-infections with multiple genotypes of Anaplasma Marginale in cattle indicate pathogen diversity. Parasites and Vectors 11 (1): 1–13.

    Article  CAS  Google Scholar 

  • Hussain, Muhammad Hammad, Muhammad Saqib, Fahad Raza, Ghulam Muhammad, Muhammad Nadeem Asi, Muhammad Khalid Mansoor, Muhammad Saleem, and Abdul Jabbar. 2014. Seroprevalence of Babesia Caballi and Theileria Equi in five draught equine populated metropolises of Punjab, Pakistan. Veterinary Parasitology 202 (3–4): 248–256.

    Article  Google Scholar 

  • Inokuma, Hisashi, Nobutaka Seino, Masatsugu Suzuki, Koichi Kaji, Hiroshi Takahashi, Hiromasa Igota, and Satoshi Inoue. 2008. Detection of Rickettsia Helvetica DNA from peripheral blood of Sika deer (Cervus Nippon Yesoensis) in Japan. Journal of Wildlife Diseases 44 (1): 164–167.

    Article  CAS  Google Scholar 

  • Jiang, J., P.J. Blair, J.G. Olson, E. Stromdahl, and A.L. Richards. 2005. Development of a duplex quantitative real-time PCR assay for the detection of tick-borne spotted fever group Rickettsiae and Rickehsia Rickettsil. Revue Internationale Des Services de Santé Des Forces Armées 78 (3): 174–179.

    Google Scholar 

  • Jiang, Ju, Teik-Chye Chan, Joseph J. Temenak, Gregory A. Dasch, Wei-Mei Ching, and Allen L. Richards. 2004. Development of a quantitative real-time polymerase chain reaction assay specific for Orientia Tsutsugamushi. The American Journal of Tropical Medicine and Hygiene 70 (4): 351–356

    Article  CAS  Google Scholar 

  • Jirapattharasate, Charoonluk, Paul Franck Adjou Moumouni, Shinuo Cao, Aiko Iguchi, Mingming Liu, Guanbo Wang, Mo Zhou, et al. 2017. Molecular detection and genetic diversity of bovine Babesia Spp., Theileria Orientalis, and Anaplasma Marginale in beef cattle in Thailand. Parasitology Research 116 (2): 751–762.

    Article  Google Scholar 

  • Johnson, Sherry A.M., John B. Kaneene, Kweku Asare-Dompreh, William Tasiame, Ivy G. Mensah, Kofi Afakye, Shirley V. Simpson, and Kwasi Addo. 2019. Seroprevalence of Q fever in cattle, sheep and goats in the Volta region of Ghana. Veterinary Medicine and Science 5 (3): 402–411.

    Article  CAS  Google Scholar 

  • Jones, B.A., Delia Grace, Richard Kock, Silvia Alonso, Jonathan Rushton, M.Y. Mohammed Y. Said, Declan McKeever, et al. 2013. Zoonosis emergence linked to agricultural intensification and environmental change. Proceedings of the National Academy of Sciences of the United States of America 110 (21): 8399–8404.

    Article  Google Scholar 

  • Jongejan, F., and G. Uilenberg. 2004. The global importance of ticks. Parasitology 129 (Suppl): S3–S14.

    Article  Google Scholar 

  • Jouglin, Maggy, Barbara Blanc, Nathalie de la Cotte, Suzanne Bastian, Katia Ortiz, and Laurence Malandrin. 2019. First detection and molecular identification of the zoonotic Anaplasma Capra in deer in France. PLoS One 14 (7): 1–10.

    Article  CAS  Google Scholar 

  • Kalume, M.K., B. Losson, and C. Saegerman. 2011. Epidemiologie et Controle de La Theileriose Bovine a T. Parva En Afrique : Une Revue de La Littérature. Annales de Médicine Vétérinaire 155: 88–104.

    Google Scholar 

  • Kamau, Joseph, Albertus J. De Vos, Matthew Playford, Bashir Salim, Peter Kinyanjui, and Chihiro Sugimoto. 2011. Emergence of new types of Theileria Orientalis in Australian cattle and possible cause of Theileriosis outbreaks. Parasites and Vectors 4 (1): 1–10.

    Article  CAS  Google Scholar 

  • Karesh, W.B., A. Dobson, J.O. Lloyd-Smith, J. Lubroth, M.A. Dixon, M. Bennett, S. Aldrich, et al. 2012. Ecology of Zoonoses: Natural and unnatural histories. The Lancet 380 (9857): 1936–1945.

    Article  Google Scholar 

  • Kasozi, Keneth Iceland, Susan Christina Welburn, Gaber El Saber, Najat Marraiki Batiha, David Paul Nalumenya, Monica Namayanja, Kevin Matama, et al. 2021. Molecular epidemiology of Anaplasmosis in small ruminants along a human-livestock-wildlife Interface in Uganda. Heliyon 7 (1): e05688.

    Article  CAS  Google Scholar 

  • Kieser, S.T., I.S. Eriks, and G.H. Palmer. 1990. Cyclic Rickettsemia during persistent Anaplasma Marginale infection of cattle. Infection and Immunity 58 (4): 1117–1119.

    Article  CAS  Google Scholar 

  • Kivaria, F.M. 2006. Estimated direct economic costs associated with tick-borne diseases on cattle in Tanzania. Tropical Animal Health and Production 38 (4): 291–299.

    Article  CAS  Google Scholar 

  • Klee, Silke R., Judith Tyczka, Heinz Ellerbrok, Tatjana Franz, Sonja Linke, Georg Baljer, and Bernd Appel. 2006. Highly sensitive real-time PCR for specific detection and quantification of Coxiella Burnetii. BMC Microbiology 6 (1): 1–8.

    Article  CAS  Google Scholar 

  • Kocan, Katherine M., Edmour F. Blouin, and Anthony F. Barbet. 2000. Anaplasmosis control: Past, present, and future. Annals of the New York Academy of Sciences 916: 501–509.

    Article  CAS  Google Scholar 

  • Kocan, Katherine M., José de la Fuente, Edmour F. Blouin, Johann F. Coetzee, and S.A. Ewing. 2010. The natural history of Anaplasma Marginale. Veterinary Parasitology 167 (2–4): 95–107.

    Article  CAS  Google Scholar 

  • Kocan, Katherine M., José De la Fuente, Alberto A. Guglielmone, and Roy D. Meléndez. 2003. Antigens and alternatives for control of Anaplasma Marginale infection in cattle. Clinical Microbiology Reviews 16 (4): 698–712.

    Article  Google Scholar 

  • Kumar, Sudhir, Glen Stecher, Michael Li, Christina Knyaz, and Koichiro Tamura. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547–1549.

    Article  CAS  Google Scholar 

  • Kumar, Tarun, Neelesh Sindhu, Gaurav Charaya, Ankit Kumar, Parmod Kumar, Gauri Chandratere, Divya Agnihotri, and Rajesh Khurana. 2015. “Emerging Status of Anaplasmosis in Cattle in Hisar.” Veterinary World 8 (6): 768.

  • la Fuente, José, Mark W. De, John T. Atkinson, David S. Hogg, Victoria Naranjo Miller, Consuelo Almazán, Neil Anderson, and Katherine M. Kocan. 2006. Genetic characterization of Anaplasma Ovis strains from Bighorn sheep in Montana. Journal of Wildlife Diseases 42 (2): 381–385.

    Article  Google Scholar 

  • Lawrence, K.E., S.F. Forsyth, B.L. Vaatstra, A.M.J. McFadden, D.J. Pulford, K. Govindaraju, and W.E. Pomroy. 2018. Clinical Haematology and biochemistry profiles of cattle naturally infected with Theileria Orientalis Ikeda type in New Zealand. New Zealand Veterinary Journal 66 (1): 21–29.

    Article  CAS  Google Scholar 

  • Lee, Seung Hun, Ehab Mossaad, Abdalla Mohamed Ibrahim, Ahmed Ali Ismail, Paul Franck Adjou Moumouni, Mingming Liu, Aaron Edmond Ringo, et al. 2018. Detection and molecular characterization of tick-borne pathogens infecting sheep and goats in Blue Nile and West Kordofan states in Sudan. Ticks and Tick-Borne Diseases 9 (3): 598–604.

    Article  Google Scholar 

  • Lesse, Paolo, Marcel R.B. Houinato, Jonas Djenontin, Hippolyte Dossa, Bouraima Yabi, Ismael Toko, Brice Tente, and Brice Sinsin. 2016. Transhumance En République Du Bénin : États Des Lieux et Contraintes. International Journal of Biological and Chemical Sciences 9 (5): 2668.

    Article  Google Scholar 

  • Li, Hao, Yuan Chun Zheng, Lan Ma, Na Jia, Bao Gui Jiang, Rui Ruo Jiang, Qiu Bo Huo, et al. 2015. Human infection with a novel tick-borne Anaplasma species in China: A surveillance study. The Lancet Infectious Diseases 15 (6): 663–670.

    Article  Google Scholar 

  • Liang, Chang Wei, Jing Bo Zhao, Juan Li, Li Tao Chang, Yu Hui Lan, Li Xia Zhang, Li Juan Zhang, and Yu. Xue Jie. 2012. Spotted fever group Rickettsia in Yunnan Province, China. Vector-Borne and Zoonotic Diseases 12 (4): 281–286.

    Article  Google Scholar 

  • Lim, Mark D. 2018. Dried blood spots for Global Health diagnostics and surveillance: Opportunities and challenges. American Journal of Tropical Medicine and Hygiene 99 (2): 256–265.

    Article  Google Scholar 

  • Liu, A.H., H. Yin, G.Q. Guan, L. Schnittger, Z.J. Liu, M.L. Ma, Z.S. Dang, et al. 2007. At least two genetically distinct large Babesia species infective to sheep and goats in China. Veterinary Parasitology 147 (3–4): 246–251.

    Article  CAS  Google Scholar 

  • Liu, Zhijie, Miling Ma, Zhaowen Wang, Jing Wang, Yulv Peng, Youquan Li, Guiquan Guan, Jianxun Luo, and Hong Yin. 2012. Molecular survey and genetic identification of Anaplasma species in goats from central and southern China. Applied and Environmental Microbiology 78 (2): 464–470.

    Article  CAS  Google Scholar 

  • M’Ghirbi, Youmna, Marwa Bèji, Beatriz Oporto, Fatma Khrouf, Ana Hurtado, and Ali Bouattour. 2016. Anaplasma Marginale and A. Phagocytophilum in cattle in Tunisia. Parasites and Vectors 9 (1): 1–8.

    Article  CAS  Google Scholar 

  • Mans, Ben J., Ronel Pienaar, and Abdalla A. Latif. 2015. A review of Theileria diagnostics and epidemiology. International Journal for Parasitology: Parasites and Wildlife 4 (1): 104–118.

    Article  Google Scholar 

  • McDermott, J.J., S.J. Staal, H.A. Freeman, M. Herrero, and J.A. Van de Steeg. 2010. Sustaining intensification of smallholder livestock Systems in the Tropics. Livestock Science 130 (1–3): 95–109.

    Article  Google Scholar 

  • McKeever, Declan J. 2009. Bovine immunity - a driver for diversity in Theileria parasites? Trends in Parasitology 25 (6): 269–276.

    Article  CAS  Google Scholar 

  • Mohammadian, Baharak, Vahid Noaman, and Seyyed Jamal Emami. 2021. Molecular survey on prevalence and risk factors of Anaplasma Spp. infection in cattle and sheep in west of Iran. Tropical Animal Health and Production 53 (2): 1–7.

    Article  Google Scholar 

  • Morrison, W.I. 2015. The Aetiology, pathogenesis and control of Theileriosis in domestic animals. Revue Scientifique et Technique (International Office of Epizootics) 34 (2): 599–611.

    Article  CAS  Google Scholar 

  • Motta, Paolo, Thibaud Porphyre, Saidou M. Hamman, Kenton L. Morgan, Victor Ngu Ngwa, Vincent N. Tanya, Eran Raizman, Ian G. Handel, and Barend Mark Bronsvoort. 2018. Cattle transhumance and Agropastoral nomadic herding practices in Central Cameroon. BMC Veterinary Research 14 (1): 1–12.

    Article  Google Scholar 

  • Motta, Paolo, Thibaud Porphyre, Ian Handel, Saidou M. Hamman, Victor Ngu Ngwa, Vincent Tanya, Kenton Morgan, Rob Christley, and Barend M. Dec Bronsvoort. 2017. Implications of the cattle trade network in Cameroon for regional disease prevention and control. Scientific Reports 7: 1–13.

    Article  CAS  Google Scholar 

  • Moumouni, Adjou, Paul Franck, Gabriel Oluga Aboge, Mohamad Alaa Terkawi, Tatsunori Masatani, Shinuo Cao, Ketsarin Kamyingkird, Charoonluk Jirapattharasate, et al. 2015. Molecular detection and characterization of Babesia Bovis, Babesia Bigemina, Theileria species and Anaplasma Marginale isolated from cattle in Kenya. Parasites and Vectors 8 (1): 1–14.

    Article  CAS  Google Scholar 

  • Muhanguzi, D., K. Ikwap, K. Picozzi, and C. Waiswa. 2010. Molecular characterization of Anaplasma and Ehrlichia species in different cattle breeds and age groups in Mbarara District (Western Uganda). International Journal of Animal and Veterinary Advances 2 (3): 76–88

    CAS  Google Scholar 

  • Mukhebi, A.W., B.D. Perry, and R. Kruska. 1992. Estimated economics of Theileriosis control in Africa. Preventive Veterinary Medicine 12 (1–2): 73–85.

    Article  Google Scholar 

  • Mwamuye, Micky M., Edward Kariuki, David Omondi, James Kabii, David Odongo, Daniel Masiga, and Jandouwe Villinger. 2017. Novel Rickettsia and emergent tick-borne pathogens: A molecular survey of ticks and tick-borne pathogens in Shimba Hills National Reserve, Kenya. Ticks and Tick-Borne Diseases 8 (2): 208–218.

    Article  Google Scholar 

  • Nagano, Daisuke, Thillaiampalam Sivakumar, Alane Caine Costa De De Macedo, Tawin Inpankaew, Andy Alhassan, Ikuo Igarashi, and Naoaki Yokoyama. 2013. The genetic diversity of Merozoite surface antigen 1 (MSA-1) among Babesia Bovis detected from cattle populations in Thailand, Brazil and Ghana. Journal of Veterinary Medical Science 75 (11): 1463–1470.

    Article  CAS  Google Scholar 

  • Nazari, Mojgan, Sue Yee Lim, Malaika Mahira Watanabe, Reuben S.K.K. Sharma, Nadzariah A.B.Y.B.Y. Cheng, and Malaika Mahira Watanabe. 2013. Molecular Detection of Ehrlichia Canis in Dogs in Malaysia. PLoS Neglected Tropical Diseases 7 (1): 7–10. Edited by David H. Walker.

    Article  Google Scholar 

  • Nene, Vishvanath, Henry Kiara, Anna Lacasta, Roger Pelle, Nicholas Svitek, and Lucilla Steinaa. 2016. The biology of Theileria Parva and control of East Coast fever - current status and future trends. Ticks and Tick-Borne Diseases 7 (4): 549–564.

    Article  Google Scholar 

  • Niaz, Sadaf, Zia Ur Rahman, Ijaz Ali, Raquel Cossío-Bayúgar, Itzel Amaro-Estrada, Abdullah D. Alanazi, Irfan Khattak, Jehan Zeb, Nasreen Nasreen, and Adil Khan. 2021. Molecular prevalence, characterization and associated risk Factors of Anaplasma Spp. and Theileria Spp. and Small Ruminants in Northern Pakistan. Parasite 28 (3).

  • Niu, Qingli, Jianxun Luo, Guiquan Guan, Zhijie Liu, Miling Ma, Aihong Liu, Jinliang Gao, et al. 2009. Differentiation of two ovine Babesia based on the ribosomal DNA internal transcribed spacer (ITS) sequences. Experimental Parasitology 121 (1): 64–68.

    Article  CAS  Google Scholar 

  • Noaman, V., and P. Shayan. 2009. Molecular Detection of Anaplasma Phagocytophilum in Carrier Cattle of Iran - First Documented Report. Iranian Journal of Microbiology 1 (2 SE-Articles): 37–42

    Google Scholar 

  • Norval, R.A.I., B.D. Perry, and A.S. Young. 1992. The epidemiology of Theileriosis in Africa. Illustrated. San Diego: ILRI (aka ILCA and ILRAD).

    Google Scholar 

  • Olwoch, J.M., B. Reyers, F.A. Engelbrecht, and B.F.N. Erasmus. 2008. Climate change and the tick-borne disease, Theileriosis (East Coast fever) in sub-Saharan Africa. Journal of Arid Environments 72 (2): 108–120.

    Article  Google Scholar 

  • Ortuño, Anna, Imma Pons, Mariela Quesada, Sergio Lario, Esperança Anton, Andreu Gil, Joaquim Castellà, and Ferran Segura. 2012. Evaluation of the presence of Rickettsia Slovaca infection in domestic ruminants in Catalonia, northeastern Spain. Vector Borne and Zoonotic Diseases 12 (12): 1019–1022.

    Article  Google Scholar 

  • Paintsil, Shirley C., Mba Mosore Nimo, Seth Offei Addo, Taylor Lura, Janice Tagoe, Danielle Ladzekpo, Charlotte Addae, et al. 2022. Ticks and prevalence of tick - borne pathogens from domestic animals in Ghana. Parasites & Vectors: 1–11.

  • Park, Jinho, Jeong Byoung Chae, Suhee Kim, Yu Do Hyeon, Hyeon Cheol Kim, Bae Keun Park, Joon Seok Chae, and Kyoung Seong Choi. 2019. Evaluation of the efficacy of Ivermectin against Theileria Orientalis infection in grazing cattle. BMC Veterinary Research 15 (1): 1–7.

    Article  CAS  Google Scholar 

  • Parola, Philippe, Christopher D. Paddock, Cristina Socolovschi, Marcelo B. Labruna, Oleg Mediannikov, Tahar Kernif, Mohammad Yazid Abdad, et al. 2013. Update on tick-borne Rickettsioses around the world: A geographic approach. Clinical Microbiology Reviews 26 (4): 657–702.

    Article  Google Scholar 

  • Peng, Yongshuai, Kunlun Wang, Shanshan Zhao, Yaqun Yan, Haiyan Wang, Jichun Jing, Fuchun Jian, Rongjun Wang, Longxian Zhang, and Changshen Ning. 2018. Detection and phylogenetic characterization of Anaplasma Capra: an emerging pathogen in sheep and goats in China. Frontiers in Cellular and Infection Microbiology 8: 1–7.

    Article  CAS  Google Scholar 

  • Perera, Piyumali K., Robin B. Gasser, Simon M. Firestone, Garry A. Anderson, Jakob Malmo, Gerry Davis, David S. Beggs, and Abdul Jabbar. 2014. Oriental Theileriosis in dairy cows causes a significant milk production loss. Parasites and Vectors 7 (1): 1–8.

    Article  Google Scholar 

  • Perveen, Nighat, Sabir Bin Muzaffar, and Mohammad Ali Al-Deeb. 2021. Ticks and tick-borne diseases of livestock in the Middle East and North Africa: A review. Insects 12 (1): 1–35.

    Article  Google Scholar 

  • Piotrowski, Mariusz, and Anna Rymaszewska. 2020. Expansion of tick-borne Rickettsioses in the world. Microorganisms 8 (12): 1–28.

    Article  CAS  Google Scholar 

  • Qurollo, Barbara A., Nikole R. Archer, Megan E. Schreeg, Henry S. Marr, Adam J. Birkenheuer, Kaitlin N. Haney, Brittany S. Thomas, and Edward B. Breitschwerdt. 2017. Improved molecular detection of Babesia infections in animals using a novel quantitative real-time PCR diagnostic assay targeting mitochondrial DNA. Parasites and Vectors 10 (1): 1–13.

    Article  CAS  Google Scholar 

  • Renneker, S., J. Abdo, D.E.A. Salih, T. Karagenç, H. Bilgiç, A. Torina, A.G. Oliva, et al. 2013. Can Anaplasma Ovis in small ruminants be neglected any longer? Transboundary and Emerging Diseases 60 (SUPPL.2): 105–112.

    Article  Google Scholar 

  • Rjeibi, M.R., M.A. Darghouth, M. Rekik, B. Amor, L. Sassi, and M. Gharbi. 2016. First molecular identification and genetic characterization of Theileria Lestoquardi in sheep of the Maghreb region. Transboundary and Emerging Diseases 63 (3): 278–284.

    Article  CAS  Google Scholar 

  • Roy, B.C., J. Krücken, J.S. Ahmed, S. Majumder, M.P. Baumann, P.H. Clausen, and A.M. Nijhof. 2018. Molecular identification of tick-borne pathogens infecting cattle in Mymensingh District of Bangladesh reveals emerging species of Anaplasma and Babesia. Transboundary and Emerging Diseases 65 (2): e231–e242.

    Article  CAS  Google Scholar 

  • Said, Mourad Ben, Hanène Belkahia, Alberto Alberti, Rosanna Zobba, Maha Bousrih, Mouna Yahiaoui, Monia Daaloul-Jedidi, Aymen Mamlouk, Mohamed Gharbi, and Lilia Messadi. 2015. Molecular survey of Anaplasma species in small ruminants reveals the presence of novel strains closely related to a. Phagocytophilum in Tunisia. Vector-Borne and Zoonotic Diseases 15 (10): 580–590.

    Article  Google Scholar 

  • Said, Mourad Ben, Hanène Belkahia, and Lilia Messadi. 2018. Anaplasma Spp. in North Africa: A review on molecular epidemiology, associated risk factors and genetic characteristics. Ticks and Tick-Borne Diseases 9 (3): 543–555.

    Article  Google Scholar 

  • Sarin, M’Hammed, Youmna M’Ghirbi, Ali Bouattour, Lise Gern, Guy Baranton, and Danièle Postic. 2005. Detection and identification of Ehrlichia Spp. in ticks collected in Tunisia and Morocco. Journal of Clinical Microbiology 43 (3): 1127–1132.

    Article  Google Scholar 

  • Segura, Juan A., Juan P. Isaza, Luz E. Botero, Juan F. Alzate, and Lina A. Gutiérrez. 2020. Assessment of bacterial diversity of Rhipicephalus Microplus ticks from two livestock agroecosystems in Antioquia, Colombia. PLoS One 15: 1–18.

  • Seo, Min Goo, In Ohk Ouh, Haeseung Lee, Paul John L. Geraldino, Man Hee Rhee, Oh. Deog Kwon, and Dongmi Kwak. 2018. Differential identification of Anaplasma in cattle and potential of cattle to serve as reservoirs of Anaplasma Capra, an emerging tick-borne zoonotic pathogen. Veterinary Microbiology 226: 15–22.

    Article  Google Scholar 

  • Seong, Giyong, Yu Jung Han, Jeong Byoung Chae, Joon Seok Chae, Yu Do Hyeon, Young Sung Lee, Jinho Park, Bae Keun Park, Jae Gyu Yoo, and Kyoung Seong Choi. 2015. Detection of Anaplasma Sp. in Korean native goats (Capra Aegagrus Hircus) on Jeju Island, Korea. Korean Journal of Parasitology 53 (6): 765–769.

    Article  CAS  Google Scholar 

  • Silva, Nayara B., Naomi S. Da, Wendell C. Taus, Anabela Mira Johnson, Leonhard Schnittger, Jessica D.M. Valente, Odilon Vidotto, et al. 2018. First report of Anaplasma Marginale infection in goats, Brazil. PLoS One 13 (8): 1–6.

    Article  CAS  Google Scholar 

  • Sivakumar, Thillaiampalam, Kyoko Hayashida, Chihiro Sugimoto, and Naoaki Yokoyama. 2014. Evolution and genetic diversity of Theileria. Infection, Genetics and Evolution 27: 250–263.

  • Stuen, S., E.G. Granquist, and C. Silaghi. 2013. Anaplasma Phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies.

  • Swilks, Emma, Shayne A. Fell, Jade F. Hammer, Narelle Sales, Gaye L. Krebs, and Cheryl Jenkins. 2017. Transplacental transmission of Theileria Orientalis occurs at a low rate in field-affected cattle: Infection in utero does not appear to be a major cause of abortion. Parasites and Vectors 10 (1): 1–9.

  • Taylor, L.H., S.M. Latham, and M.E.J. Woolhouse. 2001. Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B: Biological Sciences 356 (1411): 983–989.

    Article  CAS  Google Scholar 

  • Teshale, S., D. Geysen, G. Ameni, Y. Asfaw, and D. Berkvens. 2015. Improved molecular detection of Ehrlichia and Anaplasma species applied to Amblyomma ticks collected from cattle and sheep in Ethiopia. Ticks and Tick-Borne Diseases 6 (1): 1–7.

  • Teshale, Sori, Dirk Geysen, Gobena Ameni, Pierre Dorny, and Dirk Berkvens. 2018. Survey of Anaplasma Phagocytophilum and Anaplasma Sp. ‘Omatjenne’ infection in cattle in Africa with special reference to Ethiopia. Parasites and Vectors 11 (1): 1–10.

  • Thomas, Rachael J., J. Stephen Dumler, and Jason A. Carlyon. 2009. Current management of human Granulocytic Anaplasmosis, human Monocytic Ehrlichiosis and Ehrlichia Ewingii Ehrlichiosis. Expert Review of Anti-Infective Therapy 7 (6): 709–722.

    Article  Google Scholar 

  • Tigani-asil, El Tigani, Ahmed El, Valeria Blanda, Ghada Elderdiri Abdelwahab, Zulaikha Mohamed Al Hammadi, Shameem Habeeba, Abdelmalik Ibrahim Khalafalla, Mohamed Ali Alhosani, et al. 2021. Molecular investigation on tick-borne Hemoparasites and Coxiella Burnetii in dromedary camels (Camelus Dromedarius) in Al Dhafra region of Abu Dhabi, UAE. Animals 11 (3): 1–12.

  • Uilenberg, Gerrit. 2006. Babesia — A historical overview. Veterinary Parasitology 138: 3–10.

  • Volkova, Victoriya V., Richard Howey, Nicholas J. Savill, and Mark E.J. Woolhouse. 2010. Sheep movement networks and the transmission of infectious diseases. PLoS One 5 (6).

  • Wang, Xiaoxing, Jinming Wang, Junlong Liu, Aihong Liu, Xin He, Quanjia Xiang, Youquan Li, Hong Yin, Jianxun Luo, and Guiquan Guan. 2020. Insights into the phylogenetic relationships and drug targets of Babesia isolates infective to small ruminants from the mitochondrial genomes. Parasites and Vectors 13 (1): 1–11.

  • Watts, J.G., M.C. Playford, and K.L. Hickey. 2016. Theileria Orientalis: A review. New Zealand Veterinary Journal 64 (1): 3–9.

  • Yang, Jifei, Rong Han, Zhijie Liu, Qingli Niu, Guiquan Guan, Guangyuan Liu, Jianxun Luo, and Hong Yin. 2017. Insight into the genetic diversity of Anaplasma Marginale in cattle from ten provinces of China. Parasites and Vectors 10 (1): 1–7.

  • Yang, Jifei, Zhijie Liu, Qingli Niu, Junlong Liu, Rong Han, Guangyuan Liu, Yaoxu Shi, Jianxun Luo, and Hong Yin. 2016. Molecular survey and characterization of a novel Anaplasma species closely related to Anaplasma Capra in ticks, northwestern China. Parasites and Vectors 9 (1): 9–13.

  • Yasini, S.P., Z. Khaki, S. Rahbari, B. Kazemi, J. Salar Amoli, A. Gharabaghi, and S.M. Jalali. 2012. Hematologic and clinical aspects of experimental ovine Anaplasmosis caused by Anaplasma Ovis in Iran. Iranian Journal of Parasitology 7 (4): 91–98.

  • Yin, Hong, and Jianxun Luo. 2007. Ticks of small ruminants in China. Parasitology Research 101 (Suppl 2): S187–S189.

  • Yousefi, Ali, Sadegh Rahbari, Parviz Shayan, Zainab Sadeghi-dehkordi, and Alireza Bahonar. 2017. Molecular detection of Anaplasma Marginale and Anaplasma Ovis in sheep and goat in West Highland pasture of Iran. Asian Pacific Journal of Tropical Biomedicine 7 (5): 455–459.

  • Zaugg, J.L. 1987. Experimental infections of Anaplasma Ovis in pronghorn Antelope. Journal of Wildlife Diseases 23 (2): 205–210.

  • Zaugg, J.L. 1988. Experimental Anaplasmosis in mule deer: Persistence of infection of Anaplasma Marginale and susceptibility to a. Ovis. Journal of Wildlife Diseases 24 (1): 120–126.

  • Zaugg, Jerry L., Will L. Goff, William Foreyt, and David L. Hunter. 1996. Susceptibility of elk (Cervus Elaphus) to experimental infection with Anaplasma Marginale and A. Ovis. Journal of Wildlife Diseases 32 (1): 62–66.

  • Zhan, Lin, Wu Chun Cao, Jia Fu Jiang, Xiao Ai Zhang, Wu Xiao Ming, Wen Yi Zhang, Wei Liu, et al. 2010. Anaplasma Phagocytophilum in livestock and small rodents. Veterinary Microbiology 144 (3–4): 405–408.

  • Zhang, Jilei, Patrick Kelly, Jing Li, Xu Chuanling, and Chengming Wang. 2015. Molecular detection of Theileria Spp. in livestock on five Caribbean Islands. BioMed Research International 2015.

  • Zhou, Z., K. Li, Y. Sun, J. Shi, H. Li, and Y. Chen. 2019. Molecular epidemiology and risk factors of Anaplasma Spp., Babesia Spp. and Theileria Spp. infection in cattle in Chongqing, China. PLoS One 14 (8): 1–11.

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The authors are grateful to the Navrongo Health Research Centre and the Parasitology Department of Noguchi Memorial Institute for Medical Research for their support and contribution.

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The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the US Government. Opinions, interpretations, conclusions, and recommendations are those of the authors and are not necessarily endorsed by the US Army.

The authors Joseph W. Diclaro II and Suzanne Mate are military service members or employees of the US Government. This work was prepared as part of their official duties. Title 17 USC §105 provides that “Copyright protection under this title is not available for any work of the United States Government”. Title 17 USC §101 defines US Government work as work prepared by a military service member or employee of the US Government as part of that person’s official duties.


This study was funded by the Uniformed Services University Center for Global Health Engagement (CGHE) through the Global Health Engagement Research Initiative (Grant number: GRANT12767296).

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SOA and REB wrote the main manuscript. SOA, REB, KNY, JA, EB, PO, and SB conducted the laboratory analysis. EB analysed the data. SOA, VA, SM, JAL, PKB, MDW, JWD and SKD designed the study. JAL, PKB, MDW and SKD supervised this study. All authors reviewed and approved the final manuscript.

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Correspondence to Seth Offei Addo or Samuel K. Dadzie.

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Addo, S.O., Bentil, R.E., Yartey, K.N. et al. First molecular identification of multiple tick-borne pathogens in livestock within Kassena-Nankana, Ghana. Animal Diseases 3, 1 (2023).

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