Skip to main content

Identification of hard ticks (Acari: Ixodidae) and seroprevalence to Theileria parva in cattle raised in North Kivu Province, Democratic Republic of Congo

Parasitology Research volume 112, pages 789–797 (2013)Cite this article

Abstract

This study aimed to identify tick species and to determine their relationship with the Theileria parva seroprevalence in cattle raised under an extensive farming system in North Kivu Province, Democratic Republic of Congo in two agro-ecological zones namely medium (1,000–1,850 m) and high (>1,850 m) altitude. Among the 3,215 ticks collected on 482 animals, from February to April 2009, Rhipicephalus appendiculatus (64.26 %), the main vector of T. parva, was the most abundant species followed by Rhipicephalus decoloratus (35.49 %) and Amblyomma variegatum (0.25 %). The mean burden of R. appendiculatus tick per infested animal appeared significantly higher at medium (6.5 ± 0.22 ticks) than at high (0.07 ± 0.3 ticks) altitude (P < 0.05). However, an indirect fluorescent antibody test carried out on 450 blood samples revealed a global T. parva seroprevalence of 43 % (95 % CI: 38–47) which was not significantly (P > 0.05) different between medium (48.4 %; 95 % CI: 38–49) and high (41.9 %; 95 % CI: 35–49) altitude. These relatively low seroprevalences suggest that there is a state of endemicity to T. parva infection in the study area. The presence of the tick vector on animals was associated with an increased risk of being seropositive to T. parva infection (odds ratio = 2.04; 95 % CI: 1.8–2.3; P < 0.001). The results suggest the need for a longitudinal study to investigate the seasonal dynamics of tick species and T. parva infection. The rate of tick infection should also be evaluated in order to determine the intensity of T. parva transmission to cattle.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Ashford RW, Calisher CH, Eldridge BF, Jones TW, Wyatt G (2001) Encyclopedia of arthropod-transmitted infections of man and domesticated animals. Liverpool School of Tropical Medicine, Pembroke Place

    Google Scholar 

  • Bazarusanga T, Geysen D, Vercruysse J, Madder M (2007a) An update on the ecological distribution of Ixodid ticks infesting cattle in Rwanda: countrywide cross-sectional survey in the wet and the dry season. Expl Appl Acarol 43:279–291

    Article  Google Scholar 

  • Bazarusanga T, Vercruysse J, Marcotty T, Geysen D (2007b) Epidemiological studies on theileriosis and the dynamics of Theileria parva infections in Rwanda. Vet Parasitol 143:214–221

    PubMed  Article  CAS  Google Scholar 

  • Burkot TR, Graves PM (2000) Malaria, babesiosis, theileriosis and related diseases. In: Bruce FE, Edman JD (eds) Medical entomology. Kluwer, Netherlands, pp 187–230

    Chapter  Google Scholar 

  • Burridge MJ, Kimber CD (1972) The indirect fluorescent antibody test for experimental east coast fever (Theileria parva infection of cattle). Evaluation of a cell culture schizont antigen. Res Vet Sci 13:451–455

    PubMed  CAS  Google Scholar 

  • Byavu N, Henrard C, Dubois M, Malaisse F (2000) Phytothérapie traditionnelle des bovins dans les élevages de la plaine de la Ruzizi. Biot Agron Soc Envir 4:135–156

    Google Scholar 

  • Cummings GS (2002) Comparing climate and vegetation as limiting factors for species ranges of African ticks. Ecology 83:255–268

    Article  Google Scholar 

  • Dagnelie P (1998) Statistique théorique et appliquée. Inférence statistique à une et à deux dimensions. (Tome 2), De Boek Université (ed), Bruxelles, Belgique

  • Deem SL, Perry BD, Katende JM, McDermott JJ, Mathan SM, Maloo SH, Morzaria SP, Musoke AJ, Rowland GJ (1993) Variations in prevalence of tick borne diseases in zebu cattle by agroecological zone: Implications for East Coast fever immunisation. Prev Vet Med 16:171–187

    Article  Google Scholar 

  • Dohoo I, Martin W, Stryhn H (2003) Veterinary epidemiologic research. In: Mcpike SM (ed) A comprehensive text for the discipline. AVC, Charlottetown

    Google Scholar 

  • Dolan TT (1986) Chemotherapy of East Coast fever, the long term weight changes, carrier state and disease manifestations of parvaquone treated cattle. J Comp Pathol 96:137–146

    PubMed  Article  CAS  Google Scholar 

  • Estrada-Peña A (2003) Climate change decreases habitat suitability for some tick species (Acari: Ixodidea) in South Africa. Ond J Vet Res 70:79–93

    Google Scholar 

  • Gachohi JM, Kitala PM, Ngumi PN, Skilton RA (2011) Envrionment and farm factors associated with exposure to Theileria parva infection in cattle under traditionnel mixed farming system in Mbeere District, Kenya. Trop Anim Health Prod 43:271–277

    PubMed  Article  Google Scholar 

  • Gilioli G, Groppi M, Vesperoni MP, Baumagärtner J, Gutierrez AP (2009) An epidemiological model of East Coast fever in African livestock. Ecol Mod 220:1652–1662

    Article  Google Scholar 

  • Gitau G, Perry BD, McDermont JJ (1999) The incidence, morbidity and mortality due to Theileria parva infections in smallhorder dairy farms in Murang’a District, Kenya. Prev Vet Med 39:65–79

    PubMed  Article  CAS  Google Scholar 

  • Goddeeris BM, Morrison WI (1988) Techniques for the generation, cloning and characterization of bovine cytotoxic T cells specific for the protozoan Theileria parva. J Tissue Cult Meth 11:101–110

    Article  Google Scholar 

  • Kabamba B, Malumalu AM (2010) Cadastre des infrastructures des Provinces du Nord et Sud-Kivu République Démocratique du Congo: Problèmes et recommandations. Cellule d’Appui Politologique en Afrique Centrale (CAPAC)

  • Kalume MK, Losson B, Vyambwera CG, Mbegumbaya L, Makumyaviri AM, Saegerman C (2009) Enquête épidémiologique auprès des vétérinaires concernant trois maladies vectorielles des bovins élevés dans la Province du Nord-Kivu, République Démocratique du Congo. Epidémiol Santé Anim 56:197–216

    Google Scholar 

  • Kasonia K, Yamalo KM (1994) Ethnologie des traitements vétérinaires dans la région du Nord-Kivu (Zaïre). In: Métissages en santé animale de Madagascar à Haïti. Presses Universitaires de Namur (ed), Namur, Belgique pp 275–286

  • Kivaria FM, Ruheta MR, Mkonyi PA, Malamsha PC (2007) Epidemiological aspects and economic impact of bovine theileriosis (East Coast fever) and its control: a preliminary assessment with special reference to kibaha district, Tanzania. Vet J 173:384–390

    PubMed  Article  CAS  Google Scholar 

  • Lessard P, L’Eplattenier R, Norval RAI, Kundert K, Dolan TT, Croze H, Walker JB, Irvin JB, Perry BD (1990) Geographical information systems for studying the epidemiology of cattle diseases caused by Theileria parva. Vet Rec 126:255–262

    PubMed  CAS  Google Scholar 

  • Madder M, Speybroeck N, Brandt J, Berkvens D (1999) Diapause induction in adults of three Rhipicephalus appendiculatus stocks. Exp Appl Acarol 23:968–999

    Article  Google Scholar 

  • Madder M, Speybroeck N, Brandt J, Tirry L, Hodek I, Berkvens D (2002) Geographic variation in diapause response of adult Rhipicephalus appendiculatus ticks. Exp Appl Acarol 27:209–221

    PubMed  Article  Google Scholar 

  • Madder M, Thys E, Geysen D, Baudoux C, Horak I (2007) Boophilus microplus ticks found in West Africa. Exp Appl Acarol 43:233–234

    PubMed  Article  Google Scholar 

  • Madder M, Thys E, Achi L, Toure A, De Deken R (2011) Rhipicephalus (Boophilus) microplus: a most successful invasive tick species in West Africa. Exp Appl Acarol 53:139–145

    PubMed  Article  CAS  Google Scholar 

  • Makumyaviri AM, Habimana M (1993) Prévalence de la theilériose bovine à Theileria parva surles plateaux d’Itombwe, Centre Est Zaïre. Rev Méd Vét 144:415–418

    Google Scholar 

  • Makumyaviri AM, Mwilambwe KP (1998) Dépistage et diagnostic de la theilériose et del’anaplasmose chez les bovins élevés au ranch des Marungu, République Démocratique du Congo. Cah Vét Congo 01:22–23

    Google Scholar 

  • Maloo SH, Rowlands GJ, Thorpe W, Gettinby G, Perry BD (2001) A longitudinal study of disease incidence and case-fatality on small-holder dairy farms in coastal Kenya. Prev Vet Med 52:17–29

    PubMed  Article  CAS  Google Scholar 

  • Mararo SB (2001) Pouvoirs, élevage bovin et la question foncière au Nord-Kivu. L’Afrique des Grands Lacs, Annuaire

  • Marcotty T, Billiouw M, Chaka G, Berkvens D, Losson B, Brandt J (2001) Immunisation against East Coast fever by the infection and treatment method: evaluation of the use of ice baths for the field delivery and apparaisal of an acid formulation of long-acting tetracycline. Vet Parasitol 99:175–187

    PubMed  Article  CAS  Google Scholar 

  • Martin SW, Meek AH, Willeberg P (1987) Veterinary epidemiology: principles and methods. Iowa State University Press, Ames

    Google Scholar 

  • Matthysse JG, Colbo MH (eds) (1987) The Ixodid ticks of Uganda. Entomological Society of America. College Park, Maryland

    Google Scholar 

  • Mbwambo HA, Sudi FF, Mkonyi PA, Mfinanga JM, Mella ES, Ngovi CJ (2002) Comparative studies of the efficacy of parvaquone and parvaquone-plus-frusemide in the treatment of Theileria parva infection (East Coast fever) in cattle. Vet Parasitol 108:195–205

    PubMed  Article  CAS  Google Scholar 

  • Mbwambo HA, Magwisha HB, Mfinganga JM (2006) Evaluation of parvaquone (BUTA-Kel™ KELA, Belgium) as a treatment of East Coast fever in cattle, in the peri-urban of Dar Es Salaam City, Tanzania. Vet Parasitol 139:67–73

    PubMed  Article  CAS  Google Scholar 

  • Moorling MS, Mazhowu W, Scott CA (2004) The effect of rainfall on tick challenge at Kyle Recreational Park, Zimbabwe. Exp Appl Acarol 18:507–520

    Article  Google Scholar 

  • Morel PC (2000) Maladies à tiques du bétail en Afrique. In : Chartier C, Itard J, Morel PC, Troncy PM (eds), Précis de parasitologie vétérinaire tropicale. Editions Médicales internationales, Cachan, Editions TEC et DOC III, pp. 452–761

  • Mugabi KN, Mugisha A, Ocaido M (2010) Socio-economic factors influencing the use of acaricides on livestock: a case study of the pastoralist communities of Nakasongola District, Central Uganda. Trop Anim Hlth Prod 42:131–136

    Article  Google Scholar 

  • Mwangi EN, Newson RM, Kaaya GP (1991) Drop-off patterns for engorged adult females, nymphs and larvae of Rhipicephalus appendiculatus. Ins Sci Appl 12:629–633

    Google Scholar 

  • Norval RAI, Perry BD, Young AS (1992) The epidemiology of theileriosis in Africa. Academic, London

    Google Scholar 

  • Nshimiyimana J, Mutandwa E (2010) Seasonal dynamics and distribution of ticks in Rwanda: implications for tick control strategy in Rwanda. Int J Anim Vet Adv 2:21–25

    Google Scholar 

  • Ochanda H, Young AS, Medley GF, Perry BD (1998) Vector competence of 7 rhipicephalid tick stocks in transmitting 2 Theileria parva parasite stocks from Kenya and Zimbabwe. Parasitol 116:539–545

    Article  Google Scholar 

  • Odongo DO, Ueti MW, Mwaura SN, Knowles DP, Bishop RP, Scoles GA (2009) Quantification of Theileria parva in Rhipicephalus appendiculatus (Acari: Ixodidae) confirms differences in infection between selected tick strains. J Med Entomol 46:888–894

    PubMed  Article  Google Scholar 

  • Olwoch JM, Rautenbach CJW, Erasmus BFN, Engelbrecht BFA, Jaarsveld AS (2003) Simulating tick distributions over sub-Saharan Africa: the use of observed and simulates climate surfaces. J Biogeogr 30:1221–1232

    Article  Google Scholar 

  • Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12:361–371

    Article  Google Scholar 

  • Perry BD (1996) Epidemiology indicators and their application to the control of tick-borne diseases. In: Tatchell RJ (ed). Manual on tick and tick-borne disease control. Food and Agriculture Organisation of the United Nations (FAO): Rome, Italy

  • Phiri BJ, Benschop J, French NP (2010) Systematic review of causes and factors associated with morbidity and mortality on smallholder dairy farms in Eastern and Southern Africa. Prev Vet Med 94:1–8

    PubMed  Article  CAS  Google Scholar 

  • Rubaire-Akiiki C, Okello-Onen J, Nasinyama GW, Vaarst M, Kabagambe EK, Mwayi W, Musunga D, Wandukwa W (2004) The prevalence of serum antibodies to tick-borne infections in Mbale District, Uganda: the effect of agro-ecological zone, grazing management and age of cattle. J Insect Sci 4:8–16

    PubMed  CAS  Google Scholar 

  • Rubaire-Akiiki CM, Okello-Onen J, Musunga D, Kabagambe EK, Vaarst M, Okello D, Opolot C, Bisagaya A, Okori C, Bisagati C, Ongyera S, Mwayi MT (2006) Effet of agro-ecological zone and grazing system on incidence of East Coast Fever in calves in Mbale and Sironko Districts of Eastern Uganda. Prev Vet Med 75:251–266

    PubMed  Article  Google Scholar 

  • Short NJ, Norval RAI (1981a) Regulation of seasonal occurrence in the tick Rhipicephalus appendiculatus Neumann, 1901. Trop Anim Hth Prod 13:19–26

    Article  CAS  Google Scholar 

  • Short NJ, Norval RAI (1981b) Seasonal activity of Rhipicephalus appendiculatus Neumann, 1901 (Acari:Ixodidae) in the highveld of Zimbabwe Rhodesia. J Parasitol 67:77–84

    PubMed  Article  CAS  Google Scholar 

  • Speybroeck N, Madder M, Brandt J, Chungu H, Van Den Bossche P, Mbao V, Berkvens D (2003) Questing activity of Rhipicephalus appendiculatus (Acari: Ixodidae) nymphs: a random process? Physiol Entomol 28:256–361

    Article  Google Scholar 

  • Swai ES, Karimuribo ED, Rugaimukamu EA, Kambarage DM (2006) Factors influencing the distribution of questing ticks and the prevalence estimation of T. parva infection in brown ear ticks in the Tanga region, Tanzania. J Vector Ecol 31:224–248

    PubMed  Article  CAS  Google Scholar 

  • Swai ES, Karimuribo ED, Kambarage DM, Moshy WE (2009) A longidinal study on morbidity and mortality in youngstock smallholder dairy cattle with special reference to tick borne infections in Tanga region, Tanzania. Vet Parasitol 160:34–42

    PubMed  Article  Google Scholar 

  • Taylor MA, Coop RL, Wall RL (2008) Veterinary parasitology, 3rd edn. Blackwell, London

    Google Scholar 

  • Walker AR, Bouatour A, Camicas JL, Estrada-Peña A, Horak IG, Latif AA, Pegram RG, Preston PM (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, Scotland

    Google Scholar 

  • Yeoman GH, Walker JB (1967) The Ixodid ticks of Tanzania. Commonwealth Institute of Entomology, London

    Google Scholar 

Download references

Acknowledgments

The authors thank the Belgian Technical Cooperation (BTC) for logistical support and all cattle breeders from the territories of Lubero and Beni who participated to this study.

Author information

Affiliations

  1. Faculty of Veterinary Medicine, Catholic University of Graben, B. P. 29, Butembo, North Kivu Province, Democratic Republic of Congo

    Moïse Kasereka Kalume, Daniel Kambale Mbahikyavolo & Alexis M’Pondi Makumyaviri

  2. Research Unit in Epidemiology and Risk Analysis Applied to the Veterinary Sciences (UREAR), Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liège, Boulevard de Colonster, 20, B42 Sart-Tilman, 4000, Liège, Belgium

    Claude Saegerman

  3. Animal Health, Institute of Tropical Medicine, Nationalestraat 155, 2000, Antwerp, Belgium

    Tanguy Marcotty & Maxime Madder

  4. Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort, 0110, Pretoria, South Africa

    Tanguy Marcotty & Maxime Madder

  5. Laboratory of Parasitology and Parasitic Diseases, Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liège, Boulevard de Colonster, 20, B43 Sart-Tilman, 4000, Liège, Belgium

    Yannick Caron, Laetitia Lempereur & Bertrand Losson

Authors
  1. Moïse Kasereka Kalume
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claude Saegerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Kambale Mbahikyavolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexis M’Pondi Makumyaviri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tanguy Marcotty
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maxime Madder
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yannick Caron
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Laetitia Lempereur
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bertrand Losson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bertrand Losson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kalume, M.K., Saegerman, C., Mbahikyavolo, D.K. et al. Identification of hard ticks (Acari: Ixodidae) and seroprevalence to Theileria parva in cattle raised in North Kivu Province, Democratic Republic of Congo. Parasitol Res 112, 789–797 (2013). https://doi.org/10.1007/s00436-012-3200-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3200-7

Keywords

  • High Altitude
  • Tick Species
  • Indirect Fluorescence Antibody Test
  • Medium Altitude
  • Tick Burden