Citation of this paper

Distribution and prevalence of tick infestation in cattle in Babille district, eastern Ethiopia

Jelalu Kemal, Yimer Muktar and Sisay Alemu

College of Veterinary Medicine, Haramaya University, P.O. Box 138, Dire Dawa, Ethiopia
jelaluk@gmail.com

Abstract

Ticks are one of the most important ectoparasites of cattle which cause serious economic loss through mortality of animals, decreased production, down grading and rejection of skin and hide. A cross sectional study was conducted to determine the prevalence and distribution of tick with respect to related potential risk factors in Babille district, eastern Ethiopia. Standard physical and direct stereomicroscopy techniques were employed for identification of ticks.

Out of the total 384 cattle examined, 360 (93.8%) were found to be infested by tick parasites. A total of 1984 adult ticks were collected from the animal body parts and were identified to genera and species level. Four species of ixodidae ticks were identified from the study area. Among the ticks, Amblyomma cohaerens (41.5%) was the most prevalent, while Amblyomma variegatum was the least prevalent (6.5%) tick species recorded in the study. All species of ticks had more than one male to female ratio except Rhipicephalus (Boophilus) decoloratus (0.001:1). There was no statistically significant association between associated risk factors and tick prevalence except for body condition score. Cattle with poor body condition have significantly (p=0.02) higher tick burden than cattle with the other body condition scores. All tick species were distributed and attached with statistically significant (p=0.00) variation among different parts of the body of cattle, while all ticks inflict significantly diverse (p<0.05) types of lesion except A. variegatum. Overall, the present study revealed very high prevalence of tick infestation that could potentially hamper the productivity of cattle in the study area. Hence, a strategic control method should be put in place to combat and reduce the adverse effect of tick infestation in cattle in the area.

Key words: Amblyomma, cross-sectional, Rhipicephalus, risk factors, Tick attachment site

Introduction

Ticks are obligate blood feeding ectoparasites of vertebrates; particularly mammals, birds and reptiles throughout the world (Rajput et al 2006). They are cosmopolitan in distribution, but occur principally in tropical and subtropical regions with warm and humid climate which are suitable to undergo metamorphosis (Kilpatrick et al 2007).

Approximately 850 species have been described worldwide (William 2001). There are two well established families of ticks, the Ixodidae (hard tick) and the Argasidae (soft ticks). Both are important vectors for disease causing agents to humans and animals throughout the world. Over 79 different species of ticks are found in eastern Africa, but many of these appear to be of little or no economic importance. In Ethiopia, about 47 species of ticks are found on livestock and most of them have important as vectors and disease causing agents and also have damaging effect on skin and hide production (Anne and Conboy 2006).

Ticks transmit the wide varieties of pathogens including bacteria, rickettisia, protozoa and viruses. The major cattle tick-borne diseases in Ethiopia are anaplasmosis, babesoisis, cowdrosis and theileriosis (ILRI-FAO 2005). The highest impact on livestock health is caused by species belonging to only three genera, namely, Amblyomma, Hyalomma and Rhipicephalus (Cumming 1999).

Ethiopia has the largest livestock population in Africa that contributes to 40% of agricultural output/GDP in Ethiopia (CSA 2013). Even though the livestock sub sector contributes much to the national economy, its development is hampered by different constraints. Ectoparasites are one of the most important constraints that directly or indirectly affect the socio-economic development of poor farmers (Bekele 2002). Ectoparasites in ruminant causes serious economic loss to small holder farmers, the tanning industry and the country as a whole through mortality of animals, decreased production, down grading and rejection of skin and hide (Tikit and Addis 2011).

Ticks infestation is severe in different parts of Ethiopia and at a conservative estimate, one million USD is lost annually only through rejection of downgraded hides and skins attributed to tick damage (Gashaw 2005). Bekele (2002) estimated that an annual loss of USD 5000,000 from hide and skin downgrading from ticks, and approximately 65.5% of major defects of hide in eastern Ethiopia were from ticks. Even though losses due to tick infestation is considerable in Ethiopia, and a number of researchers reported the distribution and abundance of tick species in different parts of the country, there is no work done in estimating the prevalence and distribution of ticks in Babille district. The objectives of the present study were to estimate the prevalence, determine the distribution of tick species and assess associated risk factors in the study area.

Materials and methods

Study area

The present study was conducted in Babille district of Oromia regional state, to assess the distribution and prevalence of tick in cattle. Babille district is situated in eastern part of Ethiopia, about 593 km east of Addis Ababa, and 37 km east of Harar town. The altitude of the district ranges from 950 to 2000 meters above sea level and found between 9°21'-9.35° North latitude and 42°48'-42.8° East longitude. The climate of the district is predominantly agro-pastoral type which is characterized by high temperature and the mean annual rainfall in the area ranges from 600 to 700 mm. A survey of the land in this district shows that 21.1% is arable or cultivable, 17.5% was under annual crops, 3.9% pasture, 3.7% forest, and the remaining 71.3% is considered built-up, degraded or otherwise unusable. Cattle, sheep, goats and camels are the main productive livestock reared in the area (CSA 2008) (Figure 1).

Figure 1: Map representing the study area (Babille district)

Study design and study population

A cross-sectional study design was implemented from September 2014 to May 2015 to determine the distribution, estimate the prevalence of tick infestation and assess associated effects in cattle in Babille district. The study population consists of cattle managed under different management system which constitute exotic, cross and local breeds and with different sex, age and body condition.

Sampling and sample size determination

Random sampling method was subjected on the study population. The total number of cattle required for the study was calculated based on the formula given by Thrusfield (2007). By rule of thumb where there is no documented information about for the prevalence of tick infestation disease in the study area, it is possible to take 50% prevalence. In this study the sample size was calculated using 50% prevalence with 5% desired level of precision and 95% of confidence interval. Sampling sites of the district were selected purposively according to accessibility and the cattle within the selected sites were selected and examined randomly from the household. The host related risk factors like age and body condition were classified into groups for the convenience of the study. Cattle were categorized into three age groups according to Gatenby (1991). These are young (1 to 2 year), adult (3 to 7 years) and old (> 8 years). Body condition score was grouped into poor, medium and good according to Nicholson and Butterworth (1986) after some modification.

Tick collection and preservation

The selected study animal was properly restrained and ticks were removed carefully and gently in a horizontal pull manually using forceps from the body surface (Wall and Shearer 2001). The skin of each selected cattle was inspected for the presence of ticks then, ticks were manually collected by using forceps from different regions of the animals’ body. The entire body surface of the animals was inspected for the presence or absence of ticks, and half body tick collections on alternative sides were made. Adult ticks were collected from different parts of body regions; dewlap, axillae, udder, groin, shoulders, hump, back, belly, flank, vulva, anus, under tail, scrotum, teat, prepuce, hind leg and sternum of animals. Date of collections, address, sites of attachment, associated lesion, breed, age, sex, body condition score and management system of animals were registered during the study period. In addition, lesion inflicted on the animals due to tick infestation was recorded during the study. The collected ticks from each body regions were preserved in separate pre-filled universal bottles with 70% ethyl alcohol, and transported to Haramaya University veterinary parasitology laboratory.

Laboratory examination for tick identification

The collected ticks were identified using stereomicroscope and classified in to different genera levels based on size, mouthparts, colour of the body, leg colour, presence and absence of the eye. Furthermore, different morphology of ticks such as shape of scutum, leg colour, body, coxae one, festoon and ventral plates were considered for species level identification according to Walker et al (2003). The additional materials used in the laboratory were props, identification key and colour print picture of different tick species.

Data analysis

The collected data from field were entered into Microsoft excel spread sheet. The data were analyzed by using Statistical Package for Social Students (SPSS) version 20. Association between explanatory variables (breed, sex, age, body condition score and management system) and outcome variable (tick infestation) was done using chi-square (χ²) test and percent values. In all analysis, all statistics were considered as significant at p<0.05, while the confidence interval was set at 95% and 5% error probability.

Results

In the study area, an overall prevalence of tick infestation was 93.8% (Table 1). Four ixodidae tick species were identified which belong to Amblyomma and Rhipicephalus genera of ticks. Ambloyomma cohaerens was the predominant tick species which was collected (1030 in number with 41.4% prevalence), while Ambloyomma variegatum was the least prevalent tick (98 in number with 6.5% prevalence) (Table 1).

Table 1: Prevalence of ticks and percentage of tick species from the total tick count.
Tick species	No. of cattle Infested	Prevalence (%)	Number of ticks Collected	Total ticks (%)

	No. of cattle Infested	Prevalence (%)	Number of ticks Collected	Total ticks (%)
A. cohaerens	159	41.4	1030	51.91
B. decoloratus	124	32.3	620	31.25
R. evertsievertsi	52	13.5	236	11.98
A. variegatum	25	6.5	98	4.9

Total	360	93.8	1984	100

In the present study, male to female sex ratio for tick species indicated higher number of males than females for all species of ticks except Rhipicephalus (Boophilus) decoloratus which had (0.001:1) ratio of male to female tick (Table 2).

Table 2: Identified tick species count with sex ratio in the study area
Tick species	Sex		Male to female ratio
Tick species	No. of male tick count	No. of female tick count


A. cohaerens	634	396	1.6:1
Rh. (B.) decoloratus	6	614	0.001:1
Rh. evertsi evertsi	142	94	1.5:1
A. variegatum	62	36	1.7:1

Total	844	1140	-

Regarding related potential risk factors in the study, there was no variation in the prevalence of ticks between breed, management system of cattle production (Table 3), sex and age groups (Table 4). On the other hand, poor conditioned animals were significantly (p=0.02) infested than the other groups in each species of identified ticks except for A. variegatum (p=0.09) (Table 4).

Concerning tick inflicted lesions on the cattle, A. cohaerens (35.0%) was the dominant tick species which inflict bite mark followed by Rh. e. evertsi (14.1%), while Rh. (B.) decoloratus (6.3%) was the leading tick species in inflicting dermatitis followed by A. cohaerens (3.9%). Abscessation, inflammation, skin keratinization and focal haemorrhage were dominantly inflicted by Amblyomma. There were differences in association between the lesion inflicted and tick species infestation except for A. variegatum (p=0.19) (Table 5).

In the current study, A. cohaerens was predominantly tend to attach to genital area (scrotum/prepuce/vulva) (14.9%), A. variegatum to groin/hind leg (7.9%), Rh. (B.) decoloratus to dewlap (14.7%) and Rh. e. evertsi to anal region (anus/under tail) (14.9%). There was a difference between all tick species and attachment site of ticks to the host (p= 0.00) (Table 6).

Table 3: Number of infested animal and prevalence of tick species with respect to breed and management system of cattle
Tick species	Breed						χ²	p-value	Management						χ²	p-value
	Local		Cross		Exotic				Extensive		Semi intensive		Intensive
	No.	%	No.	%	No.	%			No.	%	No.	%	No.	%

A. cohaerens	152	39.6	6	1.6	1	0.3	1.83	0.4	154	40.2	4	1.0	1	0.3	22	0.33
Rh (B) decoloratus	113	29.4	7	1.8	4	1.0	5.52	0.06	113	30.7	5	1.3	6	1.6	11.7	0.3
Rh. e. evertsi	51	13.3	1	0.3	-	-	2.01	0.36	52	13.5	-	-	-	-	2.61	0.27
A. variegatum	24	6.2	1	0.3	-	-	0.41	0.81	24	6.2	1	0.3	-	-	0.8	0.67

Total	340	88.6	15	4	5	1.3	-	-	343	90.6	10	2.6	7	1.9	-	-

Table 4: Number of infested animal and prevalence of tick species in relation to sex, age and body condition score of cattle
Tick species	Sex				χ²	p-value	Age						χ²	p-value	BCS						χ²	p-value
	Female		Male				Young		Adult		Old				Poor		Medium		Good
	No	%	No	%			No	%	No	%	No	%			No	%	No	%	No	%

A. cohaerens	91	23.7	68	17.8	0.11	0.74	51	13.3	82	21.4	26	6.8	0.27	0.89	81	21.1	63	16.4	15	3.9	7.37	0.02
Rh (B) decoloratus	70	18.2	54	14.1	0.19	0.65	40	10.4	67	34.5	17	4.4	5.52	0.06	50	13	48	12.5	26	6.8	7.9	0.02
Rh. e. evertsi	30	7.8	22	5.7	0.004	0.96	14	3.6	27	7.0	11	2.9	1.69	0.42	27	7.0	21	5.5	4	1.0	3.05	0.02
A. variegatum	12	3.1	13	3.4	1.11	0.29	10	2.6	13	3.4	2	0.5	1.46	0.48	10	2.6	13	3.4	2	0.5	4.71	0.09

Total	203	52.9	157	41.0	-		115	29.9	189	66.3	56	14.6		-	168	43.7	145	37.8	47	12.2		-

Table 5: Number of affected animals and tick prevalence in relation to lesions inflicted by ticks
Tick species	Bite mark		Dermatitis		Abscessation		Inflammation		Skin keratinization		Focal hemorrhage		χ²	p-value
Tick species	No	%	No	%	No	%	No	%	No	%	No	%	χ²	p-value

A. cohaerens	72	35.0	8	3.9	11	5.3	-	-	10	4.9	37	18.0	13.1	0.02
Rh (B) decoloratus	-	-	13	6.3	-	-	3	1.5	3	1.5	-	-	137.7	0.00
R. e. evertsi	29	14.1	-	-	4	1.9	12	5.8	-	-	2	1.0	19.7	0.00
A. variegatum	10	4.9	-	-	-	-	4	1.9	2	1.0	9	4.4	7.3	0.19
Total	111	54.0	21	10.2	15	7.2	36	18.4	15	7.4	48	23.4	-	-

Table 6: Number of affected animal and tick prevalence in relation to attachment site on the animal
Tick species (cattle infested)	Attachment sites																		χ²	p-value
	Face		Dewlap		Neck/shoulder/ hump		Belly/flank/ back		Scrotum/prepuce/ vulva		Anus/ under tail		Axillae/ sternum		Groin/ hind leg		Udder/ teat
	No	%	No	%	No	%	No	%	No	%	No	%	No	%	No	%	No	%

A. cohaerens (159)	-	-	16	4.4	1	0.3	-	-	47	13.1	17	4.7	11	3.1	21	5.8	46	12.8	181.1	0.00
Rh (B) decoloratus (124)	10	2.8	47	13.1	28	7.8	28	7.8	5	1.60	3	0.8	-	-	-	-	3	0.8	238.1	0.00
Rh. e. evertsi (52)	-	-	-	-	-	-	-	-	5	1.4	47	13.1	-	-	-	-	-	-	226.3	0.00
A. variegatum (24)	-	-	2	0.6	-	-	-	-	7	1.9	1	0.3	6	1.7	1	0.3	8	2.2	43.5	0.00

Discussion

In the current study, there was high prevalence (93.8%) of tick infestation in cattle in the district. This result is in line with Abera et al (2010) who reported 95% cattle tick infestation prevalence in south western Ethiopia. Our finding is also comparable with the reports of Alemu et al (2014) with an overall prevalence of 81.5%. However, the prevalence of ticks in the current study is higher than the reports of Gedilu et al (2014), Tadesse and Sultan (2014) and Abdisa (2012) who reported prevalence of tick infestation with overall prevalence of 74.0, 59.4 and 53.2%, respectively. In addition, various researchers work has proven to find less prevalence of tick infestation than the present study including the reports of Tikit and Addis (2011) and Onu and Shiferaw (2013) who indicated tick prevalence of 25.64 and 14.5%, respectively. This difference could be due to the difference in the agro-climatic condition of the study areas, since tick activity was influenced by rainfall, altitude and atmospheric relative humidity (Pegram et al 1981).

A. cohaerens was found to be the most abundant tick species with prevalence of 41.4 and 51.91% (1030 in number) of total tick collected in the current study (Table 1). Likewise, Belay (2004) had reported high prevalence of A. cohaerens (50.5%). On the contrary, Gedilu et al (2014), Huruma et al (2015), Alemu et al (2014) and Abdisa (2012) had reported A. cohaerens as the least prevalent tick species with a prevalence of 0.20, 2.4, 5.21 and 7.73% in their respective study. This can be attributed to the great susceptibility of A. cohaerens for losses of total body water which ultimately make it to perish rapidly when the humid protection is disrupted according to Gashaw (2005).

On the other hand, Rh. (B.) decoloratus was the second most abundant tick species in the present study with prevalence of 32.3% (Table 1), which is in line with the findings of Alemu et al (2014), Gedilu et al (2014) and Bedaso et al (2014) who reported B. decoloratus as the most abundant tick with respective prevalence of 40.86, 47.93 and 26.3%, respectively. This might be due to B. decoloratus has been abundant in wetter highlands and sub-highlands receiving more than 800 mm rainfall annually according to Pegram et al (1981). Rh. e. evertsi was the third most abundant tick species in the present study area with prevalence of 13.5% (Table 1), which agrees with the report of Alemu et al (2014) with prevalence of 11.51%.

In another research, Rh. e. evertsi was the second most abundant tick species with prevalence of 50.9% according to Abdisa (2012) and it was the most abundant tick species with prevalence of 53.4% according to Huruma et al (2015) finding. On the other hand, A. variegatum was the least abundant tick species in the present study area with prevalence of 6.5% (Table 1), which agrees with reports of Onu and Shiferaw (2013) with prevalence of 4.7% and Abebe et al (2010) with prevalence of 4.2%. However, the findings of Tadesse and Sultan (2014), Bedaso et al (2014) and Tikit and Addis (2011) were greater than the current finding with prevalence of 32.2, 41 and 45.49%, respectively.

The current study indicates that the number of male ticks were higher than the number of females except in Rh. (B.) decolaratus in which the number of females are higher than male ticks (Table 2). This finding was in agreement with the report of Abdisa (2012) and Bedaso et al (2014) who reported similar trend. This might be attributed to the fact that male ticks take less food than females but remain longer on the host and can mate with several females. Furthermore, the observed female outnumbering of male ticks in B. decolaratus in the current study might be due to the small size of male tick which may not be seen during collection according to Huruma et al (2015) who reported the same result.

In the current study, animals with poor body condition were highly infested (p=0 .02) than the other body condition groups by each species of the ticks with the exception of A. variegatum (p=0.09) (Table 4). This finding is in line with the work of Bilkis et al (2011) and Wolde and Mohamed (2014) who reported cattle with poor body condition were significantly infested more than that of cattle with normal body condition. This might be due to the fact that poorly conditioned animals were least resistant to tick infestation and lack enough body potential to build resistance whereas over-conditioned animals showed reasonable combat to the infestation according to Manan et al (2007). Alternatively, tick infestation might be a cause for poor body condition; hence high prevalence was computed in this group of animals.

In the present study, there were differences in association between the lesion inflicted and specific tick species infestation except for A. variegatum (p=0.19) (Table 5). Rh. (B.) decoloratus (6.3%) was the leading tick species in inflicting dermatitis while A. cohaerens and A. variegatum was the most important tick species to inflict the bite mark (wound) and focal haemorrhage in the present study (Table 5). This was probably due to their long mouth part that results in severe bite according to Gebre et al (2001) and Gashaw (2005).

Regarding the attachment site of the ticks, there were differences (p=0.00) in attachment site on host in present study (Table 6). The predilection sites found in this study agree with with those reported by Wolde and Mohamed (2014) at southern part of Ethiopia. Specifically, Kabir et al (2011) at Bangladesh also reported that hard tick infestation on groin and mammary glands was most prevalent in cattle (48.75%), whereas lowest in face and neck region (30.0%) which is almost in line with present finding. In fact, Stachurski (2000) states that short hypostome ticks like Rhipicephalus usually prefer upper body parts including nape of neck and margin of anus and under tail while long hypostome ticks like Ambloyomma attaches to lower parts of the animal body, which is also the case in the present study.

Conclusions

The present study revealed high prevalence of ixodid tick infestation in cattle with overall prevalence of 93.8% having A. cohaerens as the most abundant tick species with prevalence of 41.4% in the study area. These pose huge economical and health constraint to the farmers and the animals in the area. The direct pathological lesion encountered during the study support the effect of tick infestation on the skin condition of the animals which can be reflected on the tannery industry as a whole. Therefore, systematic intervention and control of tick infestation should be put in place to tackle the diseases.

Acknowledgements

The authors would like to thankful to Haramaya University College of Veterinary Medicine laboratory assistants particularly Mr. Dereje Regassa for his support in tick species identification and overall technical support. We also grateful to the Bibille district veterinary clinic staff members for their all-round helps during the work. Cattle owners would also be greatly acknowledged for their cooperation during sample collection.

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Received 6 November 2016; Accepted 10 November 2016; Published 1 December 2016

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