Study on the Prevalence of Ixodid Tick Infestation and its Associated Risk Factors in Cattle in and Around Lay Armachiho Districts of Amhara Region, Northwest Ethiopia

Abstract

Ticks are harmful blood sucking external parasites and cause economic loss towards livestock production and have a negative impact on food security, animal product and by products. A cross-sectional study was conducted from January 2023 to March 2024 to estimate the prevalence of Ixodid Tick and its Associated Risk Factors in cattle in Lay Armachiho District, Amhara region, Norhwest Ethiopia. Simple random sampling procedure was used for selecting study animals. Descriptive statics and mixed effect logistic regression was used to assess the associations between ticks and its potential risk factors. A total of 384 Ixodid tick samples were collected from selected study cattle to idenitfy ticks at genus and species level. The overall prevalence of tick-borne hemoparasite was 37.76% (95% CI: 0.33-0.43) in the study area. From identified ticks, the genus level prevalence was 14.32%, 11.98%, 7.55% and 3.91% for Amblyomma, Boophilus, Rhipicephalus and Hyalomma, respectively. Groin and scrotum/udder is the most favorable tick attachment sites followed by dewlap, belly, neck, under tail and legs/hoof.

Based on mixed effect logistic regression analysis, communal grazing land, agroecology, study kebeles, body condition score, season and communal watering point were identified as potential risk factors. Tick infestation plays an important role for the reduction of production and productivity in livestock industries. Therefore, strategic tick control measures should be carried out in order to minimize losses attributed to ticks in Ethiopia.

Keywords: Cattle; Lay Armachiho; Prevalence; Tick; Risk factors

Abbreviations: ASL: Above Sea Level; BCS: Body Condition Score; CSA: Central Statistical Agency; LALRDO: Lay Armachiho Livestock Resources Development Office; NMA: National Metrological Agency; OIE: World Animal Health Organization; QGIS: Quantum Geographic Information System; TBD: Tick Borne Disease; WHO: World Health Organization

Introduction

Background

Ethiopia has an extremely diverse topography, a variety climatic features and agro ecological zones that are expedient to host a very large animal population [3]. It has the largest livestock population in Africa with an estimate of 78 million cattle, 42.9 million sheep, 52.5 million goats, 2.11 million horses, 0.38 million mules, 8.98 million donkeys, 8.1 million camels and 57 million of poultry [13]. Livestock sub sector plays vital roles in national economy like in generating income to farmers, creating job opportunities, ensuring food security, providing services, contributing to asset, social, cultural and environmental values, and sustain livelihoods but its development is hampered by different constraints (Hussein et al., 2018). The most important constraints to cattle productions are widespread endemic diseases including parasitic infestation, poor veterinary service and lack of attention from government [16]. Ectoparasite is widespread and the most important prevalent constraints to the livestock sector that affect the production and productivity of cattle [33,44]. Ticks are very significant and harmful blood sucking external parasites of mammals, birds and reptiles throughout the world [43]. It has a considerable impact on animals either by inflecting direct damage or by transmission of tick-borne pathogens [40]. Tick and tick born disease affect 90% of the world’s cattle population and are widely distributed throughout the world [62]. The country's environmental condition and vegetation are highly conducive for ticks and tick-borne disease perpetuation [1]. Ticks are more prevalent in the warmer climates, especially in tropical and sub-tropical areas [30].

Tick distribution and their population in the country vary according to their adaptability to ecology, eco-climate, microhabitats, ambient temperature, rainfall and relative humidity which is critical factors affecting life cycle of ticks [40]. Ticks comprise various types of genera, including Amblyomma, Rhipicephalus, Haemaphysalis, Hyalomma and Rhipicephalus (Boophilus). The genus Amblyomma and Rhipicephalus (Boophilus) are predominating in many parts of country [20]. The life of ticks depends on the host animal which results in retardation to animal growth, loss of milk and meat production.

Generally, ticks could be affecting the market price and decreasing the annual income of humans [31]. In Ethiopia, ticks in cattle population cause serious economic loss to smallholder farmers, the tanning industry and the country as a whole through the mortality of infected animals, decreased production, down grading and rejection of hide [24]. The effects of ticks estimated annual loss of US$ 500,000 from hide and skin downgrading and approximately 65.5% of major defects of hides in Eastern Ethiopia [17].

Various Tick prevalence studies have been conducted in different localities of Ethiopia. The prevalence of ticks in different studies has shown a range of 23-85%. In the study area, information is scarce as there have not been any epidemiological studies conducted on ticks in cattle. Therefore, this study was initiated to generate baseline information on the epidemiology of tick in cattle for developing disease control and prevention programs. It also expected to guide community-based awareness programs about ticks in the study area to improve effective tick prevention and control measures in cattle.

Statement of the Problem

Tick infestations in cattle are economically important ectoparasite and cause a major impediment to the health and productive performance of cattle in tropical and subtropical area [17]. This disease causes economic loss towards livestock production and has a negative impact on food security, animal product and by products [14]. In Ethiopia, ticks and tick-borne diseases in cattle population cause serious economic loss to smallholder farmers, the tanning industry and the country as a whole through the mortality of infected animals, decreased production, down grading and rejection of hide [24]. In addition, the influence of livestock farming practices on the spread and maintenance of ticks in cattle is poorly understood [6].

Despite the widespread distribution of various tick species across the study area little is known about the spread of harmful hemoparasite carried by ticks. Thus, there is paucity of information on tick in Lay Armachiho. In order to address the above problems, a study is required to fill the gaps in knowledge about the disease and its vectors in order to create baseline information that can be used to develop efficient disease control and prevention program. So, because of these problems the following research questions are formulated.

Research Questions

This research work was attempted to answer the following research questions.

¾What are the prevalence Ixodid ticks in cattle in the study district?

¾What are the associated risk factors of Ixodid tick species in cattle in the study district?

Objectives

General objective: The aim of this study was to quantify the epidemiology of Ixodid tick infestation in cattle in Lay Armachiho districts of Amhara region, Northwest Ethiopia.

Specific objectives: The specific objectives of this study are:

To determine the prevalence Ixodid ticks infestation in cattle in the study district.

To identify the associated risk factors of Ixodid tick species in cattle in the study district.

Significance of the Study

This study would be used to quantify the epidemiology of Ixodid tick infestation in cattle in the study area. To update the required bodies about the important risk factors responsible for the occurrence of ticks in cattle. The study would be promoted to future researchers to use the gap for further investigating the occurrence of this ectoparasite in cattle. It also investigating the occurrence of tick-borne diseases in cattle in the study area and bordering districts. Therefore, this study would facilitate zonal and regional animal health sectors used to designing and implementing effective control and prevention strategies of Ixodid ticks in cattle.

Literature Review

Biology and Classification of Ixodid Ticks of Cattle

Ticks are among the most significant blood-sucking arthropods and distributed worldwide. They transmit various pathogens that can cause disease and death in cattle. Ticks have several morphologic features and physiologic mechanisms that facilitate host selection, ingestion of vertebrate blood, mating, survival and reproduction [40].

Ticks are within a member called the phylum (Arthropoda), class (Arachnida), sub class (Acari) and Order (Parasitiformes) [59]. Within the Parasitiformes, ticks belong to the suborder Ixodida, which contains a single super family, the Ixodoidea, which is divided into two major families, Argasidae (soft ticks) and Ixodidae (hard ticks), and the rare family Nuttalliellidae, with a single African species [54].

The family Ixodidae, or hard ticks, contains some 683 species [32]. As adults, Ixodids exhibit prominent sexual dimorphism: the scutum covers the entire dorsum in males, but in females (and immatures) the scutum is reduced to a small podonotal shield behind the capitulum, thereby permitting great distention of the idiosomal integument during feeding [38].

Ixodidae ticks are relatively large and comprise thirteen genera. Seven of these genera contain species of veterinary and medical importance: Amblyomma, sub genus Rhipicephalus (Boophilus), Rhipicephalus, Haemaphysalis, Hyalomma, Dermacentor and Ixodes [54]. The family Argasidae, or soft ticks, consists of about 185 species worldwide and have one important genus that infests cattle, Ornithodoros [37]. Adult argasids lack a dorsal sclerotized plate or scutum, their integument is leathery and wrinkled, their mouthparts are not visible from above, and they show no obvious sexual dimorphism. Argasidae are wandering ticks, which only remain on their host while feeding [7].

Life Cycle of Ticks

There are four major stages in the life cycle of ticks: egg, larva, nymph, and adult. Following their engorgement on the host, female ticks drop off the host and seek protected places, such as in cracks and crevices or under leaves and branches, to lay their eggs [29]. During the passage through these stages, Ixodidae ticks take a number of large blood meals, interspersed by lengthy free-living periods. The time spent on the host may occupy as little as 10% of the ticks. They are relatively long-lived and each female may produce several thousand eggs [48].

The lifecycle of ticks (both Ixodids and Argasids) undergo four stages in their development (Figure 1); eggs, 6-legged larva, 8-legged nymph and adult [63]. According to the numbers of hosts, Ixodids ticks are classified as one host ticks, two-host ticks, three-host ticks and Argasids classified as multi-host ticks.

In one-host ticks, all the parasitic stages (larva, nymph and adult) are on the same hosts; in two- host ticks, larva attach to one host, feed and molt to nymph stage and engorged, after which they detach and molt on the ground to adult; and in three-host ticks, the larva, nymph and adult attach to different hosts and all detach from the host after engorging, and molt on the ground. In multi-host ticks (Argasids), a large number of hosts are involved and it is common to have five molts, each completed after engorging and detaching from the hosts [40].

Epidemiology of ticks

Geographical Distribution of Ixodid ticks in Ethiopia: Ticks are more prevalent in the warmer climates, especially in tropical and sub-tropical areas [30]. Ticks are considered to be most important to the health of domestic animal in Ethiopia. The distribution and abundance of tick species infesting domestic ruminants in Ethiopia vary greatly from one area to another area [17]. In Ethiopia, study on ticks begun early in the 19th century. Different researchers from Ethiopia and other worlds determine the pattern of ticks and ticks are common in all agro-ecological zones [47,52].

The main tick genera found in domestic animals of Ethiopia are Amblyomma, Hyalomma, Rhipicephalus, Haemaphysalis and Rhipicephalus [17]. Among the genera Rhipicephalus, Rhipicephalus lunulatus species were observed in Central Ethiopia [41], and Rhipicephalus muhasmae in Borena [53], in wetter western areas of the country [15,52]. Among the genera Rhipicephalus, Rhipicephalus lunulatus species were observed in Central Ethiopia in wetter western areas of the country [8]. Rhipicephalus evertsi evertsi is the most widespread species of Rhipicephalus [23,56]. Rhipicephalus pulchellus is distributed widely in the north eastern and southern parts of the country [23,55]. Of the genus Amblyomma four species that commonly infest cattle includes Amblyomma variegatum, A. gemma, A. lepidum and A. cohaerens and are known to exist in Ethiopia [42]. The study conducted by Mekonnen et al. (2001) in Borena zone showed that A. variegatum, A. gemma and A. lepidum distributed in wider area of southern Ethiopia. Amblyomma variegatum and A. coherence are the two most prevalent Amblyomma species in Awassa areas in decreasing order [11]. It is clearly associated with dry types of vegetation or semi-arid rangelands [52].

Two species of Rhipicephalus (Boophilus) sub genus are known to exist in Ethiopia, which include Rhipicephalus (Boophilus) decoloratus and Rhipicephalus (Boophilus) annulatus [41,55]. Rhipicephalus (Boophilus) annulatus is known to present in Gambella region and recorded by [52].

In Ethiopia, about eight species of Hyalomma that affect cattle are identified, which includes Hyalomma marginatum rufipes, Hyalomma Dromedarii, Hyalomma Tuncatum, Hyalomma Marginatum, Hyalomma Impelatum, Hyalomma Anatolicum excavatum, Hyalomma Anatolicum anatolicum and Hyalomma Albiparmatum [8].

Risk Factors

Host factors: Heavy infestations can kill calves and even adult cattle. Previously unexposed cattle become heavily infested until they build up a degree of resistance. Bos Indicus (tropical breeds of cattle) and their crosses, develop a greater degree of resistance than Bos Taurus (British and European breeds of cattle [1]. Cattle ticks transmit the organisms that cause tick fever, which is a serious blood parasite disease of cattle [37].

The genus Rhipicephalus, Haemaphysalis and Ixodes larvae, nymphs and adults will quest on vegetation [40]. The tick grabs onto the host using their front legs and crawl over the skin to find a suitable place to attach and feed. Adult tick of genera Amblyomma and Hyalomma are active hunters, they run across the ground after nearby hosts [1].

Pathogen factors: They are considered second only to mosquitoes as the most medically important group of arthropods [60]. The pathogenic effect of ticks on host species can be divided into cutaneous and systemic effects [42]. In cutaneous infection the sites of tick bite local dermal necrosis and hemorrhage occur, followed by an inflammatory response, dermal necrosis is sufficient to damage the hide. Tick bites wounds can become infected with staphylococcus bacteria causing local cutaneous abscess or pyaemia.

Heavy tick infestation can result in significant blood loss, reduced productivity, reduced weight gain, and can cause restlessness (NMA, 2008). In the systemic effect blood-feeding habit of ticks are important as vectors of animal disease-transmitting a wide range of pathogenic viruses, Rickettsial, bacteria, and protozoa (Urquhart et al., 1996).

Environmental factors: Ticks are more prevalent in the warmer climates, especially in tropical and sub-tropical areas [30]. The country's environmental condition and vegetation are highly conducive for ticks and tick-borne disease perpetuation [1]. The disease occurs when there is much tick activity, mainly during summer but a single tick can cause fatal infection (Pieszko, 2015). The heaviest losses occur in marginal areas where the tick population is highly variable depending on the environmental conditions [29].

There is a seasonal variation in the prevalence of clinical babesiosis, the greatest incidence occurring soon after the peak of the tick population, climatic factors and air temperature is the most important because of their effect on tick activity, higher temperatures increase its occurrence [3]. In temperate regions seasonal occurrence of the disease is associated with the occurrence of the vectors and the prevalence of Anaplasmosis is found higher in hot and humid weather associated with the abundance of ticks (Sajid et al., 2017).

The presence of ticks on animals are an important risk factors for the spread of Theileriosis reported as there is higher prevalence of T. annulata in hot dry summer (Niaz et al., 2021). The pattern of seasonal occurrence of R. appendiculatus (Vector of T. parva) is determined by climate. Rhipicephalus appendiculatus is most active following onset of rain, outbreak of ECF may be seasonal or, where rainfall is relatively constant, may occur at any time [46].

Clinical Findings of Ticks

Tick infestations in cattle are economically important ectoparasite and cause a major impediment to the health and productive performance of cattle in tropical and subtropical area (Desalegn et al., 2024). They can cause fever, anemia, jaundice, anorexia, weight loss, swelling of lymph nodes, dyspnoea, diarrhea, nervous disorders, and even death by affecting the blood and/ or lymphatic system of the animals [6].

It also causes economic loss towards livestock production and has a negative impact on food security, animal product and by products [14]. In Ethiopia, ticks and tick-borne diseases in cattle population cause serious economic loss to smallholder farmers, the tanning industry and the country as a whole through the mortality of infected animals, decreased production, down grading and rejection of hide [24].

Prevention and Control Methods

Vector Control: It is done by repeated treatment of cattle with acaricides in areas of high challenge, such treatment may require to be carried out twice weekly in order to kill the tick before the infective sporozoite develops in the salivary gland [29]. Significant factors currently affecting the control of babesiosis include increased resistance to acaricides by ticks and the numerous draw backs of the current live vaccines (Suarez et al., 2019). Tick-borne pathogen controls include tick control, vaccines against ticks, and parasites and drugs against ticks and parasites [29].

Biological tick control methods: Ticks have numerous natural enemies, but only a few species have been evaluated as tick biocontrol agents. Some laboratory results suggest that several bacteria are pathogenic to ticks, but their mode of action and their potential value as bio-control agents remain to be determined (Uilenberg, G.1994).

Natural enemies of ticks include insectivorous birds, parasitoid wasps, nematodes, Bacillus thuringiensis bacteria, and deuteromycete fungi (largely Metarhizium anisopliae and Beauvaria bassiana). The potential of each of these taxa as bio-control agents will be discussed in turn. Mammals and birds typically consume ticks during self-grooming [40].

Tick vaccine: Tick infestations affect animal health and production worldwide, with an impact of ecto-parasites. Acaricides are a major component of integrated tick control strategies, but their application had limited efficacy in reducing tick infestations and often accompanied by serious drawbacks, it includes the selection of acaricide-resistant ticks, environmental contamination and contamination of milk and meat products with drug residues (Uilenberg, G.1994). All of these issues re-inforce the need for alternative approaches to control tick infestations and pathogen transmission that is the use of vaccines (a vaccine which is prepared from infected ticks) with tick antigens (Suarez et al., 2019).

Breed selection for tick resistance: Indigenous Sanga and Zebu cattle which are predominantly reared by communal farmers have a high degree of tick and tick-borne disease resistance and require minimal tick control methods. This tick control method is suitable and cost effective (minimize) for usages, even farmers (Kaur et al., 2015). Tick resistance has been shown to be heritable reported a heritability estimate of 34% for tick resistance, indicating that genetic improvement through selection should be effective. Resistance of cattle to tick infestation was reported to consist of innate and acquired components [1].

Application of chemicals methods: The use of acaricides in the control of ticks has improved the viability of cattle farming in the tick infested areas. Ticks can be killed by dipping or spraying cattle with an appropriate chemical (acaricides). Ticks can develop resistance to acaricides [29]. Dipping animals are immersed in a dipping tub containing solution of chemicals. Infested cattle should be dipped in the organophosphate acaricide coumaphos (0.3% active ingredient. In general dipping vats provide a highly effective method of treating animals with acaricides for tick control [40].

Spray the application of fluid acaricides to an animal by means of a spray has many advantages and has been successfully practiced for controlling ticks on most of the animals (Solomon and Molla, 2020). Spraying equipment is highly portable, and only small amounts of acaricides need to be mixed for a single application. However, spraying is generally less efficient in controlling ticks than immersion in a dipping vat because of problems associated with applying the acaricides thoroughly on all parts of the animal body (Oundo et al., 2022).

The application of insecticides with aerosols and in oils, smears, and dusts by hand to limited body areas is time-consuming and laborious, but in certain instances it may be more effective and economical (in terms of cost) of acaricides than treating the entire animal [29].

Economic Importance of Tick infestations

In Ethiopia, ticks occupy the first place among the external parasites through mortality of animals, decreased production, downgrading and general rejection of skins and hides [14]. The impacts of ticks on animals were either by inflecting direct damage or by transmission of tick-borne pathogens. They are responsible for severe economic losses both through the direct effects associated with their blood sucking behavior [36] and also indirectly act as reservoirs and vectors for a wide range of human and animal pathogens [32].

Ticks and tick-borne diseases affect 90% of the world’s cattle population and are widely distributed throughout the world [19]. In Ethiopia, ticks and tick-borne diseases in cattle population cause serious economic loss to smallholder farmers, the tanning industry and the country as a whole through the mortality of infected animals, decreased production, down grading and rejection of hide [24]. Generally, ticks could be affecting the market price and decreasing the annual income of humans [31]. The effects of ticks estimated annual loss of US$ 500,000 from hide and skin downgrading and approximately 65.5% of major defects of hides in Eastern Ethiopia [17].

Materials and Methods

Study Area

The study was conducted in Lay Armachiho district in Amhara region, Northwest Ethiopia from February 2023 to April 2024. The administrative zone was selected purposively based on their livestock population agro ecology representation and accessibility.

Lay Armachiho district is found in Central Gondar zone with an area of 1,059.33 square kilometers. It is located in Central Gondar zone, Amhara regional state, Northwest Ethiopia, located at latitude of 13° north and longitude of 37.2° east at an altitude range from 1,500-2,700 meters above sea level. The administrative center of the district is Tikel Dingay, with 29 rural and two town administrative units/kebeles. The agro climatic zone of the area is characterized as highland (7%), midland, (61%) and lowland (32%) with the temperature and rainfall ranges between 18-30°C and 800-1,500 mm, respectively.

It is located 749 kilo-meters away from Addis Ababa, the capital city of the country, and 207 kilo-meters away from Bahir Dar, the capital city of the region (Demeke et al., 2020). The livestock populations of the district were 456,522 (cattle 145,733, sheep 40,917, goats 72,247, horses 330, mules 295, donkeys 20,219 and poultry 197,000) (LALRDO, 2023). A total human population of a district estimated to be 157,836, of whom 79,538 were males and 78,298 females.

Study Population

The study was conducted on local and cross breed of cattle with different age, sex and Body Condition Scores (BCS). Cattle are kept under extensive and semi-intensive management system in which it depends on grazing for their feed sources.

Study Design

A cross-sectional study was conducted from February 2023 to April 2024. to estimate the prevalence of ixodid ticks and identify its associated risk factors in cattle in Lay Armachiho district. Body condition scores of each cattle was evaluated during sample collection and the cattle was classified as emaciated (poor), moderate (medium) and good based on anatomical parts and the flesh and fat cover at different body parts (Nicholson and Butterworth, 1986) (Annex 1). Animals were conveniently classified as young (<3 years) and Adult (>3 years) age categories as described by De-lahunta and Habel (1986).

Sampling Method and Sample Size Determination

The study districts were selected purposively based on their livestock population, agro ecology representation and accessibility. Simple random sampling techniques were used to select study kebeles, villages and animals. Sample size was calculated according to the formula given by Thrusfield (2007) with 95% confidence level and 5% absolute precision.

Where, n = required sample size

Pexp = expected prevalence

d = desired absolute precision

Thus, a total of 384 both local and cross breed cattle were used for this study.

Data Collection

Tick sample collection and preservation: The entire body surface of the animal was examined thoroughly for the presence or absence of ticks from each body part of animals. Ticks were collected after cattle restrained properly. Then, ticks were collected carefully and gently in a horizontal pull to the body surface of cattle by using forceps and care was taken to avoid decapitulation [62]. The collected ticks were preserved in clean universal bottle containing 70% ethyl alcohol and labeled it. During examination the selected animal’s age, sex, breed, body condition score, tick infestation, date of collection, kebeles and its tick predication sites were recorded on a data recording format designed for this purpose.

Tick identifications: Ticks were identified to the genus and species level according to their morphological key structures such as shape of scutum, leg colour, scutum ornamentation, body grooves, punctuations, basis capitulum, coaxes and ventral plates. During tick identification in the laboratory, the sample was put on Petri dish and adult ticks were identified under a stereomicroscope using the standard identification keys [28,62].

Data Analysis

The collected data was entered into Microsoft Excel, coded and summarized using descriptive statistics. The prevalence was calculated for all data by dividing positive samples over the total number of examined samples and multiplying by hundred. All statistical analyses were done using Stata 17 statistical software. A mixed effect logistic regression model (household was taken as random effect) was used to assess the association of risk factors with the occurrence of hemioparaite infections in cattle. Districts, breed, sex, age category, health status, season, body condition score, tick infestation, communal grazing land and watering points were the predictor variables in which associations examined. Factors with p-value less than 0.25 in the univariable analysis were incorporated into the multivariable mixed effect logistic regression model. In the multivariable mixed effect logistic regression, P-value < 0.05 was considered as statistically significant and Odds Ratio (OR) and 95% CI were also calculated. Correlation, confounding and interaction tests were checked.

Results

Prevalence of Bovine Ixodid tick infestation at Kebele Level

A total of 384 cattle were examined for tick infestation. Of which, 145 cattle were found positive for tick infestation with overall prevalence of 37.76 % was recorded at 95% confidence interval in the study areas. Examined animals were considered to be positive for a given tick infestation when at least one tick was collected from them. Out of the total animals exposed to Ixodid tick infestation 32 (42.1%), 30 (40.5%), 27 (39.7%), 23 (36.5%), 18 (32.14%) and 15 (31.91%) were from Atsemider, Janikaw, Jiha, Shumara lomeye, Kerker and Chira kebeles respectively (Figure 1).