Skip to main content
SpringerLink
Log in

Prevalence and geographic distribution of Besnoitia besnoiti infection in cattle herds in Portugal

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Bovine besnoitiosis, caused by the apicomplexan parasite Besnoitia besnoiti is considered an emergent disease in Europe. This study aimed to determine the prevalence and geographic distribution of B. besnoiti in cattle herds in continental Portugal and to identify potential spatial clustering of infection. A stratified two-stage cross-sectional serological survey was carried out between March 2012 and May 2013 with the five administrative NUTS II regions, Norte, Centro, Lisboa, Alentejo, and Algarve, as the stratification level. Sera from 391 herds in 220 parishes and 83 municipalities were analyzed by a serial testing strategy, with the modified agglutination test (B-MAT) as the first screening assay and the immunofluorescent antibody test (IFAT) as the confirmatory test. Within-herd prevalence of positive herds varied between 0.7 and 72.4 % and was ≥10.3 % in half of the infected herds. Using a Bayesian approach, the true prevalence of B. besnoiti in cattle herds was determined to be 5.1 % (confidence interval (CI), 3.1–7.8 %) and the mean within-herd prevalence of positive herds was 33.0 % (CI, 20.3–46.0 %). The sensitivity and specificity of the B-MAT were estimated to be 96.9 % (CI, 93.7–98.8 %) and 99.7 % (CI, 99.6–99.8 %), whereas those of the IFAT were 89.6 % (CI, 86.0–92.5 %) and 99.7 % (CI, 98.5–99.9 %), respectively. Spatial scan statistics analysis identified one spatial cluster covering the majority of the Alentejo region. Seropositive herds were detected for the first time outside Alentejo, in the region Centro and in the northeast of Portugal. Further epidemiological research is needed to identify eco-biological factors, which could explain the geographic clustering of B. besnoiti in Portugal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alzieu JP, Dorchies P, Schelcher F, Gottstein B (2007) L’extension de la besnoitiose bovine en France. Le Point Vétérinaire 276:37–43

    Google Scholar 

  • Ashmawy KI, Abu-Akkada SS (2014) Evidence for bovine besnoitiosis in Egypt-first serosurvey of Besnoitia besnoiti in cattle and water buffalo (Bubalus bubalis) in Egypt. Trop Anim Health Prod 46:519–522

    Article  PubMed  Google Scholar 

  • Basso W, Schares G, Gollnick NS, Rütten M, Deplazes P (2011) Exploring the life cycle of Besnoitia besnoiti—experimental infection of putative definitive and intermediate host species. Vet Parasitol 178:223–234

    Article  PubMed  CAS  Google Scholar 

  • Bigalke RD (1968) New conception of the epidemiological features of bovine besnoitiosis as determined by laboratory investigations. Onderspoort J Vet Res 35:3–137

    CAS  Google Scholar 

  • Björkman C, Lundén A, Holmdahl J, Barber J, Trees AJ, Uggla A (1994) Neospora caninum in dogs: detection of antibodies by ELISA using an ISCOM antigen. Parasite Immunol 16:643–648

    Article  PubMed  Google Scholar 

  • Branscum AJ, Gardnerb IA, Johnson WO (2004) Bayesian modeling of animal- and herd-level prevalences. Prev Vet Med 66:101–112

    Article  PubMed  CAS  Google Scholar 

  • Cortes H, Leitão A, Vidal R, Vila-Viçosa MJ, Ferreira ML, Caeiro V, Hjerpe CA (2005) Besnoitiosis in bulls. Vet Rec 157:262–264

    PubMed  CAS  Google Scholar 

  • Cortes HC, Reis Y, Waap H, Vidal R, Soares H, Marques I, Pereira da Fonseca I, Fazendeiro I, Ferreira ML, Caeiro V, Shkap V, Hemphill A, Leitão A (2006a) Isolation of Besnoitia besnoiti from infected cattle in Portugal. Vet Parasitol 141:226–233

    Article  PubMed  CAS  Google Scholar 

  • Cortes HCE, Nunes S, Reis Y, Staubli D, Vidal R, Sager H, Leitão A, Gottstein B (2006b) Immunodiagnosis of Besnoitia besnoiti infection by ELISA and Western blot. Vet Parasitol 141:216–225

    Article  PubMed  CAS  Google Scholar 

  • Cortes H, Leitão A, Gottstein B, Hemphill A (2014) A review on bovine besnoitiosis: a disease with economic impact in herd health management, caused by Besnoitia besnoiti (Franco and Borges, 1916). Parasitology. doi:10.1017/S0031182014000262

    Google Scholar 

  • Costa MA, Kulldorff M (2009) Applications of spatial scan statistics: a review. In: Glaz J, Pozdnyakov V, Wallenstein S (eds) Scan statistics: methods and applications. Birkhäuser, Boston, pp 129–152

    Chapter  Google Scholar 

  • Diesing L, Heydorn AO, Matuschka FR, Bauer C, Pipano E, de Waal DT, Potgieter FT (1988) Besnoitia besnoiti: studies on the definitive host and experimental infections in cattle. Parasitol Res 75:114–117

    Article  PubMed  CAS  Google Scholar 

  • Dohoo I, Martin W, Stryhn H (2003) Veterinary epidemiological research, 1st edn. Transcontinental, Prince Edward Island

    Google Scholar 

  • Dubey JP, Yabsley MJ (2010) Besnoitia neotomofelis n. sp. (Protozoa: Apicomplexa) from the southern plains woodrat (Neotoma micropus). Parasitology 137:1731–1747

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP, Desmonts G, McDonald C, Walls KW (1985) Serologic evaluation of cattle inoculated with Toxoplasma gondii: comparison of Sabin-Feldman dye test and other agglutination tests. Am J Vet Res 46:1085–1088

    PubMed  CAS  Google Scholar 

  • Dubey JP, Thulliez P, Weigel RM, Andrews CD, Lind P, Powell EC (1995) Sensitivity and specificity of various serologic tests for detection of Toxoplasma gondii infection in naturally infected sows. Am J Vet Res 56:1030–1036

    PubMed  CAS  Google Scholar 

  • Dubey JP, Sreekumar C, Lindsay DS, Hill D, Rosenthal BM, Venturini L, Venturini MC, Greiner EC (2003) Besnoitia oryctofelisi n. sp. (Protozoa: Apicomplexa) from domestic rabbits. Parasitology 126:521–539

    PubMed  CAS  Google Scholar 

  • Dunson DB (2001) Commentary: practical advantages of Bayesian analysis of epidemiologic data. Am J Epidemiol 153:1222–1226

    Article  PubMed  CAS  Google Scholar 

  • EFSA (2010) Bovine besoitiosis: an emerging disease in Europe. European Food Safety Authority. EFSA J 8:1499–1514

    Google Scholar 

  • Fernández-García A, Risco-Castillo V, Pedraza-Díaz S, Aguado-Martínez A, Alvarez-García G, Gómez-Bautista M, Collantes-Fernández E, Ortega-Mora LM (2009) First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. J Parasitol 95:474–476

    Article  PubMed  Google Scholar 

  • Fernández-García A, Álvarez-García G, Risco-Castillo V, Aguado-Martínez A, Marcén JM, Rojo-Montejo S, Castillo JA, Ortega-Moram LM (2010) Development and use of an indirect ELISA in an outbreak of bovine besnoitiosis in Spain. Vet Rec 166:818–822

    Article  PubMed  Google Scholar 

  • Franco EE, Borges I (1916) Sur la sarcosporidiose Bovine. Arq Inst Bacteriologico Câmara Pestana 4:269–289

    Google Scholar 

  • García-Lunar P, Ortega-Mora LM, Schares G, Gollnick NS, Jacquiet P, Grisez C, Prevot F, Frey CF, Gottstein B, Alvarez-García G (2013) An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines. Transbound Emerg Dis 60:59–68

    Article  PubMed  Google Scholar 

  • Gentile A, Militerno G, Schares G, Nanni A, Testoni S, Bassi P, Gollnick NS (2012) Evidence for bovine besnoitiosis being endemic in Italy—first in vitro isolation of besnoitia besnoiti from cattle born in Italy. Vet Parasitol 184:108–115

    Article  PubMed  CAS  Google Scholar 

  • Goldman M, Pipano E (1983) Serological studies on bovine besnoitiosis in Israel. Trop Anim Health Prod 15:32–38

    Article  PubMed  CAS  Google Scholar 

  • Hornok S, Fedák A, Baska F, Hofmann-Lehmann R, Basso W (2014) Bovine besnoitiosis emerging in Central-Eastern Europe, Hungary. Parasit Vectors 7:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Jordan D, McEwen SA (1998) Herd-level test performance based on uncertain estimates of individual test performance, individual true prevalence and herd true prevalence. Prev Vet Med 3:187–209

    Article  Google Scholar 

  • Juste RA, Cuervo LA, Marco JC, Oregui LM (1990) La besnoitiosis bovina: desconocida en España? Med Vet 7:613–618

    Google Scholar 

  • Kiehl E, Heydorn AO, Schein E, Al-Rasheid KA, Selmair J, Abdel-Ghaffar F, Mehlhorn H (2010) Molecular biological comparison of different Besnoitia species and stages from different countries. Parasitol Res 106:889–894

    Article  PubMed  Google Scholar 

  • Konstantinov SA, Ul’ianov KN (1988) Effect of cattle color, age, size and behavior on the intensity of the attack and sucking attachment by gadflies. Parazitologiia 22:488–495

    PubMed  CAS  Google Scholar 

  • Kulldorff M (1997) A spatial scan statistic. Communications in Statistics. Theory Methods 26:1481–1496

    Article  Google Scholar 

  • Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V (2010) Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. Int J Health Geogr 9:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Lesser M, Braun U, Deplazes P, Gottstein B, Hilbe M, Basso W (2012) First cases of besnoitiosis in cattle in Switzerland. Schweiz Arch Tierheilkd 154:469–474

    Article  PubMed  CAS  Google Scholar 

  • Manuali E, Lepri E, Salamida S, D’Avino N, Mangili P, Vitellozzi G, Grelloni V, Filippini G (2011) An outbreak of bovine besnoitiosis in beef cattle born in central Italy. Transbound Emerg Dis 58:464–467

    Article  PubMed  CAS  Google Scholar 

  • Marotel M (1912) Discussion of paper by Besnoit and Robin. Bull et Mem de la Soc des Sciences Vet de Lyon et de la Soc de Med Vet de Lyon e du Sud-Est 15:196–217

    Google Scholar 

  • Mehlhorn H, Klimpel S, Schein E, Heydorn AO, Al-Quraishy S, Selmair J (2009) Another African disease in Central Europa: besnoitiosis of cattle. I. Light and electron microscopical study. Parasitol Res 104:861–868

    Article  PubMed  Google Scholar 

  • Nasir A, Lanyona SR, Schares G, Malcolm Anderson ML, Reichel MP (2012) Sero-prevalence of Neospora caninum and Besnoitia besnoiti in South Australian beef and dairy cattle. Vet Parasitol 186:480–485

    Article  PubMed  Google Scholar 

  • Neuman M (1972) Serological survey of Besnoitia besnoiti (Marotel 1912) infection in Israel by immunofluorescence. Zentralbl Veterinarmed B 19:391–396

    Article  PubMed  CAS  Google Scholar 

  • Olias P, Schade B, Mehlhorn H (2011) Molecular pathology, taxonomy and epidemiology of Besnoitia species (Protozoa: Sarcocystidae). Infect Genet Evol 11:1564–1576

    Article  PubMed  CAS  Google Scholar 

  • Packham AE, Sverlow KW, Conrad PA, Loomis EF, Rowe JD, Anderson ML, Marsh AE, Cray C, Barr BC (1998) A modified agglutination test for Neospora caninum: development, optimization, and comparison to the indirect fluorescent-antibody test and enzyme-linked immunosorbent assay. Clin Diagn Lab Immunol 5:467–473

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pols JW (1960) Studies on bovine besnoitiosis with special reference to the aetiology. Onderspoort J Vet Res 28:265–356

    Google Scholar 

  • Reis Y, Cortes HC, Viseu Melo L, Fazendeiro I, Leitão A, Soares H (2006) Microtubule cytoskeleton behaviour in the initial steps of host cell invasion by Besnoitia besnoiti. FEBS Lett 580:4673–4682

    Article  PubMed  CAS  Google Scholar 

  • Reisen WK (2010) Landscape epidemiology of vector-borne diseases. Annu Rev Entomol 55:461–483

    Article  PubMed  CAS  Google Scholar 

  • Rinaldi L, Maurelli MP, Musella V, Bosco A, Cortes H, Cringoli G (2013) First cross-sectional serological survey on Besnoitia besnoiti in cattle in Italy. Parasitol Res 112:1805–1807

    Article  PubMed  Google Scholar 

  • Sergeant ESG (2014) Epitools epidemiological calculators. AusVet Animal Health Services and Australian Biosecurity Cooperative Research Centre for Emerging Infectious Disease. Available at: http://epitools.ausvet.com.au

  • Schares G, Basso W, Majzoubd M, Rostaher A, Scharr JC, Langenmayer MC, Selmair J, Dubey JP, Cortes HC, Conraths FJ, Gollnick NS (2010) Comparative evaluation of immunofluorescent antibody and new immunoblot tests for the specific detection of antibodies against Besnoitia besnoiti tachyzoites and bradyzoites in bovine sera. Vet Parasitol 171:32–40

    Article  PubMed  CAS  Google Scholar 

  • Schares G, Langenmayer MC, Scarr JC, Minke L, Maksimov P, Maksimov A, Schares S, Barwald A, Basso W,Dubey JP, Conraths FJ, Gollnik NS (2013) Novel tools for the diagnosis and differentiation of acute and chronic bovine besnoitiosis. Int J Parasitol 43:143–154

  • Schofield S, Torr SJ (2002) A comparison of the feeding behaviour of tsetse and stable flies. Med Vet Entomol 16:177–185

    Article  PubMed  CAS  Google Scholar 

  • Shaapan RM, El-Nawawi FA, Tawfik MA (2008) Sensitivity and specificity of various serological tests for the detection of Toxoplasma gondii infection in naturally infected sheep. Vet Parasitol 153:359–362

    Article  PubMed  CAS  Google Scholar 

  • Shkap V, Ungar-Waron H, Pipano E, Greenblatt C (1984) Enzyme linked immunosorbent assay for detection of antibodies against Besnoitia besnoiti in cattle. Trop Anim Health Prod 16:233–238

    Article  PubMed  CAS  Google Scholar 

  • Shkap V, Reske A, Pipano E, Fish L, Baszler T (2002) Immunological relationship between Neospora caninum and Besnoitia besnoiti. Vet Parasitol 106:35–43

    Article  PubMed  CAS  Google Scholar 

  • Smith RD (2006) Veterinary clinical epidemiology, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Smith DD, Frenkel JK (1984) Besnoitia darlingi (Apicomplexa, Sarcocystidae, Toxoplasmatinae): transmission between opossums and cats. J Protozool 31:584–587

    Article  PubMed  CAS  Google Scholar 

  • Torr S, Mangwiro TN (2000) Interactions between cattle and biting flies: effects on the feeding rate of tsetse. Med Vet Entomol 14:400–409

    Article  PubMed  CAS  Google Scholar 

  • Torr SJ, Mangwiro TNC, Hall DR (2006) The effects of host physiology on the attraction of tsetse (Diptera: Glossinidae) and Stomoxys (Diptera: Muscidae) to cattle. Bull Entomol Res 96:71–84

    Article  PubMed  CAS  Google Scholar 

  • Waap H, Cardoso R, Marcelino E, Malta J, Cortes H, Leitão A (2011) A modified agglutination test for the diagnosis of Besnoitia besnoiti infection. Vet Parasitol 178:217–222

    Article  PubMed  Google Scholar 

  • Wallace GD, Frenkel JK (1975) Besnoitia species (Protozoa, Sporozoa, Toxoplasmatidae): recognition of cyclic transmission by cats. Science 188:369–371

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The present work was performed at the Parasitology Laboratory, Instituto Nacional de Investigação Agrária e Veterinária (INIAV), which provided the necessary research resources. This work further received partial support from the Fundação para a Ciência e a Tecnologia, Portugal, project grant PTDC/CVT/65674/2006. The authors thank the National Veterinary Authority (DGAV) and the official laboratories DRAPN, Segalab, Viseu, Guarda, Alcains, Proleite, LMV, COPRAPEC, Évora, ACOS, Assisvet, and DRAALG, for the invaluable collaboration in this study. The authors also wish to acknowledge gratefully Prof. Adam Branscum for the helpful comments on the Bayesian model application, Lucinda Marques and Maria do Carmo Ramos (INIAV) for assistance in sample processing, and Margarida Arede (CIISA-FMV) for the kind help in the spatial analysis of data.

Author information

Authors and Affiliations

  1. Laboratório de Parasitologia, Instituto Nacional de Investigação Agrária e Veterinária, Rua General Morais Sarmento, 1500-311, Lisbon, Portugal

    Helga Waap

  2. CIISA, Faculdade de Medicina Veterinária, Universidade de Lisboa, Av. da Universidade Técnica, 1300-447, Lisbon, Portugal

    Telmo Nunes & Yolanda Vaz

  3. Laboratório de Parasitologia, Núcleo da Mitra, ICAAM, Universidade de Évora, Apartado 94, 7000-554, Évora, Portugal

    Helder Cortes

  4. Instituto de Investigação Científica Tropical, CVZ, CIISA, Faculdade de Medicina Veterinária, Av. da Universidade Técnica, 1300-447, Lisbon, Portugal

    Alexandre Leitão

Authors
  1. Helga Waap
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Telmo Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helder Cortes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandre Leitão
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yolanda Vaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Alexandre Leitão or Yolanda Vaz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Waap, H., Nunes, T., Cortes, H. et al. Prevalence and geographic distribution of Besnoitia besnoiti infection in cattle herds in Portugal. Parasitol Res 113, 3703–3711 (2014). https://doi.org/10.1007/s00436-014-4035-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4035-1

Keywords

Search

Navigation