Prevalence of Tick Infestations and Tick-Borne Diseases in Cattle in Cameroon ()
1. Introduction
The livestock sector accounts for over 40% of global agricultural production and contributes to the livelihoods and food security of nearly one billion people worldwide [1] . Livestock farming plays an important role in rural Africa [2] [3] , and cattle are the main savings species for smallholders. Cattle are the fastest growing sector in the agricultural economy for income growth, infrastructure and technology [4] . The cattle population in Cameroon is estimated at 8,761,385 heads, and a meat beef production of 110,000 to 145,000 tons per year is equivalent to about 54% of meat products [5] .
Ticks and tick-borne diseases are major problems for human, animal and environmental health with enormous negative economic impacts and financial losses of more than $18.7 billion per year [6] [7] on beef production. Ticks are vectors of zoonoses of major public health importance [8] while tick-borne animal piroplasmosis and cowdriosis are major pathological and economic constraints on livestock development in sub-Saharan Africa [9] .
Several control methods for ticks and tick-borne diseases (TBD) have been evaluated including the use of chemical products and acaricides against the vectors which pose a huge risk of drug resistance and pollution [10] [11] [12] [13] . Though the high cost of tick and tick-borne disease prevents expansion in cattle production [14] [15] , vaccination is an alternative control tool in regions where there are no cross-border movements of cattle. Endogenous methods for tick control [8] [16] and other alternatives such as genetics geared towards using biological resistance mechanisms of certain species or breeds in livestock farming activities in tropical environments [17] [18] have been described.
The direct and indirect impacts of tick infestations of cattle are numerous including decreased milk productivity and carcass yield, low growth rate, the transmission of pathogens (eg. hemoparasites), dermatitis which may become infected by bacteria, skin coat depreciation making it less marketable and increase the cost of production due to tick control [19] [20] [21] . In the central African subregion including Cameroon, attention has focused on infectious and contagious diseases of animals while has neglected vector borne diseases especially tick-borne diseases [21] [22] [23] .
Though there are increasing urban and peri-urban livestock production systems in most of Africa, there is a dearth of information on the level of awareness of cattle breeders on the hazards caused by ticks on husbandry systems and ectoparasite status of cattle in urban areas of Cameroon. In view of the medical and veterinary importance of ticks in the livestock sector, this study was carried out to determine the prevalence of tick infestation and ticks-borne diseases in cattle in Cameroon.
2. Materials and Methods
2.1. Study Location and Management of Animals
The study was carried out to determine the prevalence and intensity of tick infestation and haemoparasites in cattle within and around the SODEPA ranches (Livestock Development Corporation) in the Administrative Divisions of Faro & Deo (Adamawa region), Lom & Djerem (East region) in the Guinean high savannah agro-ecological zone and Donga-Mantung (North West region) in the western highland agro-ecological zone of Cameroon (Figure 1). The geographical and animal husbandry situations of the study regions are presented in Table 1 and Table 2.
The selection of cattle herds in the SODEPA Faro, Dumbo and Ndokayo ranches and those of willing local farmers in the environs of these SODEPA ranches during the study period, May to October 2021, was done using a random number generation technique from the list herds in the area [26] . Briefly, in each ranch, two large herds from among herds in the female camps to enable sufficient sampling of adult and young animals, and two herds from among herds in the adult male camps were included in the study. All individual animals in the chosen herds were sampled. Overall, tick and blood samples were collected from 742 cattle (409 Goudali and 333 Simgoud breeds; 337 males and 405 females; 90 young, 264 juveniles and 388 adults) corresponding to 268 cattle in Faro & Deo, Adamawa, 186 cattle in Lom & Djerem, East and 288 cattle in Donga-Mantung, North-West.
Following rigorous visual examination of tick on the preferred sites of the skin of the animals (anogenital, udder, perineum, abdomen, armpit and neck) [27] , all the ticks encountered on the animal’s body was harvested, by gently tapping at the rostrum and traction using a pair of forceps. The harvested ticks were stored in individual 5 ml labelled (identifying the sampled animal, anatomical region, and date of harvest) tubes containing 70% ethanol and 30% glycerol for analysis within 5 - 7 days in the parasitological laboratory of the Mission Spéciale d’Eradication des Glossines (MSEG) in N’Gaoundéré. Systemic phenotypic identification of the tick species was done using a binocular microscope and guided by reference tick images as previously described [28] [29] [30] [31] [32] .
Blood samples (5 ml) from each animal were collected by jugular vein puncture into EDTA tubes for haematological analysis (Haematocrit value) and detection of haemoparasites using standard procedures. Haematocrits were determined to assess the degree of anaemia while blood smeared slides were stained with MAY-GRÜNWALD GIEMSA and observed under a light microscope at x100 magnification to detect the presence of haemoparasites.
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Table 1. Geographical characteristics of the study regions.
Source: Djoufack, 2011 [24] .
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Table 2. Animal husbandry features of the study regions.
source: MINEPIA/DEPCS, 2020 [25] .
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Figure 1. Map of Cameroon showing study regions and administrative divisions within the regions.
Information related to the breed, sex, age and body condition score of the sampled animals were noted. Estimation of ages was done by dental inspection and examination of the horn rings for animals without teeth (especially old/adult females) while the breed of the animals was obtained as previously described [33] [34] [35] . The body condition score was done by assessing the general appearance and palpation of the lumbar region of the animal on a scale of 1 to 5 and further classed into 3 categories: 1 - 2 (poor), 3 (good) and 4 - 5 (very good) as previously described [36] .
2.2. Ethical Consideration
Risk assessments of the project were performed by the researchers to avoid hazards to all persons involved in the project. Permission for the study was obtained from the required authorities in Cameroon including the MINEPIA delegations in Adamawa, East and Northwest and North Regions, SODEPA Cameroon (SODEPA Faro, Dumbo and Ndokayo ranches) and the Faculty of Agronomy and Agricultural Sciences of the University of Dschang, Cameroon. The purpose of the study was explained (with the assistance of local community leaders and trusted intermediaries) to cattle professionals with herds in the environs of the SODEPA ranches used in this study. Animals and farms were used in the study after informed consent was given by the owners.
2.3. Data Analysis
The data were analysed using SPSS 21.1 statistical software. Simple percentages were generated and Chi-square test was used to assess the association between factors and the odds-ratios determined for associated risk factors along 95% confidence intervals [26] [37] . The statistical significance was set at P < 0.05.
3. Results
3.1. Prevalence of Tick Infestation in Cattle in Cameroon
In this study, of the 742 cattle sampled 566 (76.28%, 95% CI: 73.00 - 79.56) animals were infested with ticks. Locality, age, breed and sex had significant effects (P < 0.05) on the prevalence of tick infestation in cattle in the study. Tick infestation was significantly higher in the Adamawa region (99.25%) than in the other 2 regions, in adult animals over 24 months of age (86.34%), in the Simgoud breed (79.87%) and in males (82.49%) (Table 3).
Microscopic examination of ticks taken from the cattle sampled revealed the presence of three genera (4 species) of ticks, including Amblyomma variegatum (75.09%), Rhipicephalus microplus (19.43%), Rhipicephalus decoloratus (0.88%) and Hyalomma marginatum (0.18%). There are also associations of ticks on the same animal. This was the case for A. variegatum/R. microplus (4.06%) and A. variegatum/H. marginatum (0.36%) (Table 4).
3.2. Prevalence of Tick-Borne Blood Diseases in Cattle in Cameroon
In this study, of the 742 cattle sampled 682 (91.91%, 95% CI) animals were infected with tick-borne blood diseases. Locality, age, and breed had significant effects (P < 0.05) on the prevalence of tick-borne disease infection in cattle in the study while sex did not a significant effect (P > 0.05). Tick-borne disease infections were significantly higher in the East region (97.31%) than in the other 2 regions, in juvenile animals between 7 to 24 months of age (93.94%) and in the Simgoud breed (93.69%) (Table 5).
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Table 3. Prevalence and risk factor for tick infestation of cattle in Cameroon.
CT: Contingency test, ns: non-significant, *: significant.
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Table 4. Distribution of tick infested cattle according to locality, breed, age and sex in Cameroon.
#: number cattle infested by tick, *: proportion (%) of infested cattle.
Microscopic examination of blood smears taken from the cattle sampled revealed the presence of three genera (5 species) of tick-borne blood diseases, including Babesia bovis (1.32%), Babesia major (0.44%), Anaplasma marginale (11.29%), Anaplasma phagocytophylum (0.29%) and Ehrlichia ruminantium (3.52%). There are also many associations of tick-borne diseases on the same animal. This represents the vast majority of tick-borne blood diseases (79.77%). We also identified Dermatophilus congolensis (3.37%), which is not a tick-borne blood disease but is strongly associated with the presence of Amblyomma variegatum (Table 6).
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Table 5. Prevalence and risk factor for tick-borne blood diseases infection of cattle in Cameroon.
CT: Contingency test, ns: non-significant, *: significant.
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Table 6. Distribution of tick-borne blood diseases in cattle according to locality, breed, age and sex in Cameroon.
#: number of cattle infected by haemoparasites, *: proportion (%) of infected cattle.
4. Discussion
The prevalence of ticks and TBD has been widely documented in tropical environments. This aspect is addressed in several ways by various methods, namely blood sampling and germ detection or molecular analysis of the ticks themselves. The results obtained on prevalence as a function of locality significantly corroborate those of [38] , who argue that the prevalence of each tick species in its geographical distribution is conditioned by biomes and specific environmental conditions such as temperature. It is normal that, depending on the environmental conditions, there should be various adaptations of species.
4.1. Amblyomma variegatum
The results obtained from the frequency of this tick in the different regions of 75.09% show the abundance of this tick and are similar to those obtained from 46.3% to 73.8% [39] - [45] . These same authors found that it is practically the most widespread in several African countries. However, [46] found that the genus Rhipicephalus (80.60%) was more important than Amblyomma (19.31%). This tick thrives in the warmer regions of Africa. We note that it is less significant in the north-west, which is a mountainous area with low average annual temperatures compared with the other two regions.
4.2. Rhipicephalus microplus
The results obtained for this tick are 19.43% overall. However, it is very prevalent in the North West region, where 57.07% of animals are infested with this species, in contrast to the other two regions, where it was only mentioned very rarely. This prevalence is not far from the results obtained by numerous authors in several countries, including Cameroon [41] [43] , which vary from 15.6% to 24.11%. This confirms the presence of this highly invasive species in Cameroon [47] .
4.3. Hyalomma marginatum
The results obtained from the presence of this tick, concentrated in the north-west with a very low prevalence of around 0.18%, are similar to those obtained from several studies which only mention its presence without mentioning a precise prevalence. These include [39] [48] [49] . However, other authors have given prevalence ranging from 1.8% to 13.8% [45] [50] [51] .
4.4. Rhipicephalus decoloratus
The results we obtained (0.88%) were founded only in the north-west among adults. However, several studies have mentioned its presence (20.1% to 50.6%) in various regions of Africa [38] [44] [52] [53] . Our results are higher than obtained in north-west Cameroon (0.4%) by [39] .
The results obtained in the different regions mentioning the presence of babesiosis, anaplasmosis, richetsiosis and dermatophilosis are caused by several germs sometimes associated with each other on the same animal.
4.5. Babesiosis
We encountered two germs, Babesia bovis (1.3%) and Babesia major (0.44%), especially in the East region. The results are not very far from those obtained in small ruminants (2.9%) in the Adamawa region [41] . This disease is usually mentioned in the records of the veterinary services in all regions where cattle are reared.
4.6. Anaplasmosis
We encountered two germs, Anaplasma marginale (11.29%) and Anaplasma phagocytophilum (0.29%), respectively in the three regions for the former and only in Adamawa for the latter. The prevalence of Anaplasma marginale is similar to the results obtained for small ruminants (9.1%) in Adamawa [41] . This species is the most pathogenic of its genus [54] .
4.7. Ehrlichia ruminantium
The results obtained for the prevalence of around 3.52% are different from those obtained in a study carried out in Benin using molecular analysis of ticks, which revealed the germ with an overall prevalence in ticks of 10.8% [49] and 28.4% [55] . This may be due to the different techniques used, as we worked on the animals and not on the ticks. In addition, there is a correlation between the presence of this germ and the environment.
5. Conclusion
This study was carried out to determine the prevalence and intensity of tick infestation and haemoparasites in cattle within and around the SODEPA ranches in the Guinean high savannah agro-ecological zone and in the western highland agro-ecological zone of Cameroon reveals the presence of three ticks genus (4 species): Amlyomma variegatum, Rhipicephalus microplus, Hyalomma marginatum and Rhipicephalus decoloratus. The following tick-borne diseases were also identified: Babesia bovis, Babesia major, Anaplasma marginale, Anaplasma phagocytophylum and Ehrlichia ruminantium. We also identified Dermatophilus congolensis which is not a tick-borne disease but associated with Amblyomma presence. There is a significant dependence between the prevalence of ticks and locality, sex, breed and age. Similarly, there was a dependence on the prevalence of tick-borne diseases and locality, breed and age. On the other hand, there was no dependence between tick-borne diseases and the sex of the animal. The perspective of this study is to examine the implementation of a tick and haemoparasite control mechanism that is both animal welfare-friendly and environmentally friendly.
Authors’ Contributions
HH conceptualised the study under the direction of FM, and he collected data and wrote the first draft of the manuscript. AFE contributed to the final manuscript. FM, RA, NAJ and BM supervised HH.
Acknowledgements
The authors are grateful to the Agronomic and Veterinary Institute Hassan II and the University of Dschang for their institutional support. We also thank the staff of the Ministry of Livestock, Fisheries and Animal Industries for their administrative and technical support.