Prevalence and seasonal abundance of ticks on dogs and the role of Rhipicephalus sanguineus in transmitting Babesia species in Maidugiri , North-Eastern Nigeria

Aim: An investigation on ticks and haemoparasites of dogs that belonged to Maiduguri metropolis (Borno State) was conducted. Materials and Methods: Survey of ticks and haemo-parasites on 400 stray dogs was conducted in Maiduguri from December 2009 to November 2011, using a stratified random sampling technique from different locations of the town. The town was divided into 10 districts out of which a total of 40 dogs were sampled at random from each district. Results: Four genera of ticks were identified on the infested dogs 384 (96.0), all of which belonged to the family Ixodidae (hard ticks). The genus Boophilus was predominant with a prevalence of 88.0%, Rhipicephalus 10.8%, Hyalomma 0.9% and Amblyomma 0.3% at (p ? 0.05). Dogs within the age-group of 6-12 months were the most infested, while those within the agegroup of 24 –120 months were the least infested. Sex appeared to have a less significant influence (p > 0.05) on the prevalence of ticks among the dog population as females were more infested than the males. The perineum and the ear were the most commonly infested areas, with 328 (85.4%) and 252 (65.4%) respectively, while the scrotal and abdominal regions were the least infested areas 12 (3.1%) each. The month of August showed the highest mean tick burden of 462.5±3.2 ranging from 450475, while the month of February showed the least number of ticks with a mean of 244.5±3.8 ranging from 239-250. Dogs found to be infected with Babesia canis are all harboring ticks of the genus Rhipicephalus. Female dogs were more infected (66.7%) with Babesia canis than their male counterparts (33.3%) (p ? 0.05) and dogs within the age group of 1-6 months were more infected. Conclusion: Prevalence of ticks on dogs in this study area is relatively high and the occurrence of Babesia species is vector dependent, with ticks of the genus Rhipicephalus sanguineous being the most common vector in transmission of the parasite. Seasons also play a vital role in the prevalence of ticks and their associated haemoparasites.


Introduction
Ehrlichia, Anaplasma, Borrelia and Hepatozoon are of major health concern to dogs and cause severe Ticks, regarded as the largest non-microscopic economic damage to dog owners, some of which are of ectoparasites, are the most important vectors that infest zoonotic significance [1,10-12].animals, transmit a wide range of pathogens from Dog keeping habit in Borno State is mainly for infected to non-infected hosts.Ticks of the family hunting and herding, to a minimal extent, for security Ixodidae are considered as vertebrate's vectors and they purposes; in which most of them were owned but, not constitute the largest tick genera with about 235 different confined.This lack of confinement exposes them to a species described worldwide [1].Rhipicephalus variety of hazards and infections which include parasites sanguineus, also known as the brown dog tick is the and their vectors [12]; at the same time serving as most cosmopolitan specie among the families, transmireservoirs for transmission of infections to non-infected tting a wide range of pathogens to dogs and other animals, ones and the animals they herd.Maiduguri, located in including humans [2][3][4][5].Tick-borne haemoparasites the Sahel region of Nigeria, is endowed with a are one of the most important vector-borne infections favorable climate suitable for the proliferation of ticks of dogs.They are numerous and are caused by several and tick-borne parasites.Thus, this research focuses on etiological agents such as bacterial, protozoan, and the common ticks and tick-borne haemoparasites, their rickettsial organisms [6].They are cosmopolitan in distribution based on predilection sites and seasonal distribution, but are most numerous and exert their abundance among dog population in the study area.greatest impacts in the tropics and subtropics [7-9].Tick-borne haemopathogens such as Babesia, under a dissecting microscope, and identified using the the North, Chad to the North-east and Cameroon to the classification keys of [15,16]; and taxonomic characteeast.Within the country, its neighbors are Adamawa to ristics as described earlier [17].the South, Yobe to the West and Gombe to the Hematological examination: Blood samples were Southwest [13].The State has a climate which is hot collected directly from the ear veins using heparinized and dry for a greater part of the year in the northern and micro-haematocrit capillary tubes and then centrifuged central parts, while the southern part is slightly milder.
(1200 x g, 5', and room temperature).The PCV's were The period of wet season varies from place to place due determined by haematocrit reader and the color of the to the influence of the various climatic factors such as plasma was simultaneously checked and recorded.The the direction of the rain bearing winds and topography, capillary tubes were then cut using a diamond pencil 1 but generally, the rainy season is normally from July to mm below the buffy coat and the contents of the September in the north, up to early October in the south capillary tube were transferred onto clean glass slides, with a relative humidity of about 49% and evaporation mixed and covered with cover slip.Thin smears were of 203mm per year.The State has two major vegetation prepared directly from the ear vein and also from the zones viz: Sahel in the North and Sudan Savannah in buffy coat and fixed with methanol and stained with the South [13].
Giemsa.Both the wet and stained smears were examined Sampling methods: Survey of ticks and haemofor the presence of haemoparasites as described earlier parasites on 400 stray dogs was conducted in Maiduguri [15].from December 2009 to November 2011, using a Statistical analysis: Data collected were subjected to stratified random sampling technique from different student's t-test and categorical data like age group were locations of the town.The town was divided into 10 subjected to one-way analysis of variance (ANOVA) at districts out of which a total of 40 dogs were sampled at p < 0.05 regarded as statistically significant [18].random from each district.Each sub-population Microsoft excel was used for presentation of the results.(district) was divided into different strata based on age and gender.

Discussion
adolescent ones; even though, the difference as seen in this study is not significant.The insignificance difference The ticks collected in this study were Boophilus in the rate of infestation amongst sexes and age-group spp., Rhipicephalus sanguineus, Hyalomma spp.and may be due to congregation of males and females during Amblyomma variegatum, all belonging to the family mating and close proximity of the young animal's body Ixodidae are the common ticks found in Nigeria.[19][20][21][22][23][24][25][26][27].
to the ground than the adult ones.Furthermore, intimacy With respect to sex and age, female dogs were between the older ones and their offspring helps in the more infested than their male counterparts.This might spread of transmission.be due to the fact that female dogs usually form a The perineum was the most infested predilection sedentary habit while nursing their offspring; as a site on the dogs examined.This shows that preference result, they easily get infested by ticks.This finding of ticks to the various predilection sites could be due to also conforms to the reports of Tanwia [21,24,25,28].
accessibility of blood vessels, difference in the thick-The infestation rate was insignificantly (p>0.05)ness of the skin in the different parts of the body, tempehigher in the age-group of 6-12 month old dogs.This rature or variation in microhabitat [30].The perineum finding contrast to the report by Shitta et al [25] and and ears happen to be the most prevalent areas infested Jame-Rugu [29] who reported that adult and young on the dogs examined.(puppies) dogs were more infested by ticks than the    Cumulative monthly distribution of ticks in this more accurate and comparative result between the two study area revealed that infestation was higher during techniques.the rainy season than during the dry season.This might sites like Ehrlichia canis and Anaplasma platys may be which are highly effective against most of these bacteria.
Study area: Borno State with Maiduguri as its capitalCollection of ticks: A total of 400 dogs were physically N examined for ticks; ticks present were detached using city lies approximately between latitude 10.20 and N E E forceps or hand picking.The collection procedure was 13.40 , and longitude 9.80 and 14.40 .Maiduguri town N N carefully performed to avoid destroying the mouthlies around latitude 11.300 and 11.450 and longitude E parts and the ticks were preserved in 2% formalin for 13.50 .Borno State has an area of 69,436sqkm and it is further identification [14].the largest State in the Federation in terms of geographical area.Located in the north-eastern corner of Identification of ticks: Ticks collected from individual Nigeria, the State occupies the greatest part of the Chad dogs were transferred into petri dishes and examined basin and shares border with the Republic of Niger to

Figure- 2 .
Figure-2.Photomicrograph of a Giemsa's stain thin blood smear showing a red blood cell infected with B. canis (arrow) appearing as a pair of pyriform shaped bodies with basophilic cytoplasm and a reddish chromatin (x100).
borne diseases of companion animals in Europe.Vet. a result of common usage of antibiotics like Doxycy-Parasitol.163: 298-305.cline in most of the veterinary clinics in the study area 4. Dantas-Torres, F. (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus.Parasites and Vectors.3:26.
months are more prone to infection than other age 10.Robertson, I.D., Irwin, P.J., Lymbery, A.J. and Thompson, groups and the month of August has the highest tick R.C.A. (2000) The role of companion animals in the burden while the month of February showed the lowest emergence of parasitic disease.Int.J. Parasitol.30: 1369-1377.tick burden among dogs in the study area and the 11.Patz, J.A., Gractzyk, T.K., Gella, N. and Vittor, A.Y.(2002) haemoparasites of the genus Babesia canis is the most Effects of environmental changes on emerging parasitic common tick-borne haemopathogens found in the diseases.Int.J. Parasitol.30:1395-1405.study area.12. Okubanjo, O.O., Adeshina, O.A., Jatau, I.D. and Natala, A.J. (2013) Prevalence of Babesia canis and Hepatozoon canis Recommendation in Zaria.Nigeria.Sokoto J. Vet.Sci.11(2): 15-20.13.Borno State Diary (2005) Geographical history of Borno It is highly recommended that a modern molecular State; By: The Ministry for Local Government and diagnostic technique like PCR be employed to detect Chieftaincy Affairs.ALGON DIARY Preliminary pages.tick-borne haemoprotozoans in the area so as to give a 14.Uade, S.U., Liana, A., Jorg, H. and Anton, B. (2008) Parasitology Laboratory, Department of Veterinary Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Maiduguri for their assistance during the course of the research and partial funding.

Table - 1
. Prevalence of tick species infesting dogs in Maiduguri.

Table - 2
. Prevalence of ticks infesting dogs based on age and sex of dogs.
Values with similar superscripts are not statistically significant (p>0.05).

Table - 3
. Distribution of ticks based on predilection sites examined.

Table - 4
. Cumulative monthly distribution of tick infestation on dogs in Maiduguri.

Table - 5
. Prevalence of Babesia canis based on the sex and age of the dogs examined.