Role of Different Culicoides Vectors (Diptera: Ceratopogonidae) in Bluetongue Virus Transmission and Overwintering in Sardinia (Italy)

Overview

Journal Parasit Vectors

Publisher Biomed Central

Specialties Parasitology
Tropical Medicine

Date 2016 Aug 10

PMID 27502924

Citations 29

Authors

Cipriano Foxi

Gavino Delrio

Giovanni Falchi

Maria Giovanna Marche

Giuseppe Satta

Luca Ruiu

Affiliations

Soon will be listed here.

Abstract

Background: Bluetongue (BT) epidemics have affected the Mediterranean island of Sardinia since 2000. While Culicoides imicola represents the main bluetongue virus (BTV) vector, other European Culicoides biting midges, possibly implicated in virus transmission, have been detected here. Understanding their distribution, seasonal abundance, and infection rates is necessary to predict disease incidence and spread across coastal and inland areas, and to define their role in virus overwintering.

Methods: Biting midge abundance was determined by light traps on selected farms representing diverse climatic conditions of Sardinia. Livestock-associated Culicoides species were morphologically and molecularly identified. Infection rates in prevailing midge species captured in 2013 during a BTV-1 outbreak were determined using RT-qPCR based virus detection in insect body pools, supplemented by specific body region analyses. The seasonal infection prevalence in Culicoides samples collected in 2001 in a BTV-2 affected farm was also determined.

Results: The Newsteadi complex (C. newsteadi species A and species B) prevailed among all biting midge species (47.7 %), followed by C. imicola (27.8 %) and the Obsoletus complex (C. obsoletus and C. scoticus) (17.6 %). Whilst Culicoides imicola was more abundant along the coast, the Newsteadi complex was frequently collected at higher altitude and the Obsoletus complex was notably associated to cattle farms. Culicoides pulicaris and C. punctatus abundance was found to be marginal in all farms. BTV was detected in parous female samples of all these species, and the full dissemination of the virus within the body of C. imicola, C. obsoletus, C. scoticus, and Newsteadi complex species was confirmed by analyses of thorax and head, containing salivary glands. Higher infection rates were associated with C. scoticus, C. newsteadi species A and species B, compared to C. imicola. The virus was detected in C. newsteadi species A and C. obsoletus in winter and spring, whereas it was mainly found in summer and autumn in C. imicola.

Conclusions: In Sardinia, bluetongue virus is transmitted by multiple Culicoides vectors, including C. imicola and the Newsteadi complex being the most important. The Newsteadi complex and other midge species can play an important role in internal areas and are likely to be directly involved in virus overwintering.

Citing Articles

Culicoides and midge-associated arboviruses on cattle farms in Yunnan Province, China.

Duan Y, Li Z, Bellis G, Li L, Liu B, Wang J Parasite. 2024; 31:72.

PMID: 39565151 PMC: 11578047. DOI: 10.1051/parasite/2024072.

Diversity of biting midges, mosquitoes and sand flies at four dog shelters in rural and peri-urban areas of Central Morocco.

Zahri A, Ahlamine M, Abou-Elaaz F, Talimi H, El Berbri I, Balenghien T Parasite. 2024; 31:57.

PMID: 39331804 PMC: 11433837. DOI: 10.1051/parasite/2024057.

Updated checklist of the Culicoides Latreille biting midges (Diptera: Ceratopogonidae) of Galicia (NW Spain): Diversity, distribution and medical-veterinary relevance.

Polina A, Martinez-Barciela Y, Pereira J, Cobo F, Iniguez E, Lucientes J Vet Med Sci. 2024; 10(5):e1555.

PMID: 39180313 PMC: 11344163. DOI: 10.1002/vms3.1555.

Quantitative risk assessment for the introduction of bluetongue virus into mainland Europe by long-distance wind dispersal of Culicoides spp.: A case study from Sardinia.

Bibard A, Martinetti D, Giraud A, Picado A, Chalvet-Monfray K, Porphyre T Risk Anal. 2024; 45(1):108-127.

PMID: 38955987 PMC: 11735344. DOI: 10.1111/risa.14345.

Midge Abundance across Years: Modeling Inter-Annual Variation for an Avian Feeder and a Candidate Vector of Hemorrhagic Diseases in Farmed Wildlife.

Benn J, Orange J, Gomez J, Dinh E, McGregor B, Blosser E Viruses. 2024; 16(5).

PMID: 38793647 PMC: 11125994. DOI: 10.3390/v16050766.

References

Meiswinkel R, van Rijn P, Leijs P, Goffredo M . Potential new Culicoides vector of bluetongue virus in northern Europe. Vet Rec. 2007; 161(16):564-5. DOI: 10.1136/vr.161.16.564. View

Savini G, Goffredo M, Monaco F, Di Gennaro A, Cafiero M, Baldi L . Bluetongue virus isolations from midges belonging to the Obsoletus complex (Culicoides, Diptera: Ceratopogonidae) in Italy. Vet Rec. 2005; 157(5):133-9. DOI: 10.1136/vr.157.5.133. View

Foxi C, Delrio G . Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia, Italy. Med Vet Entomol. 2010; 24(2):199-209. DOI: 10.1111/j.1365-2915.2010.00861.x. View

Gomulski L, Meiswinkel R, Delecolle J, Goffredo M, Gasperi G . Phylogeny of the subgenus Culicoides and related species in Italy, inferred from internal transcribed spacer 2 ribosomal DNA sequences. Med Vet Entomol. 2006; 20(2):229-38. DOI: 10.1111/j.1365-2915.2006.00620.x. View

Lorusso A, Sghaier S, Carvelli A, Di Gennaro A, Leone A, Marini V . Bluetongue virus serotypes 1 and 4 in Sardinia during autumn 2012: new incursions or re-infection with old strains?. Infect Genet Evol. 2013; 19:81-7. DOI: 10.1016/j.meegid.2013.06.028. View

Romon P, Higuera M, Delecolle J, Baldet T, Aduriz G, Goldarazena A . Phenology and attraction of potential Culicoides vectors of bluetongue virus in Basque Country (northern Spain). Vet Parasitol. 2011; 186(3-4):415-24. DOI: 10.1016/j.vetpar.2011.11.023. View

Pili E, Carcangiu L, Oppo M, Marchi A . Genetic structure and population dynamics of the biting midges Culicoides obsoletus and Culicoides scoticus: implications for the transmission and maintenance of bluetongue. Med Vet Entomol. 2010; 24(4):441-8. DOI: 10.1111/j.1365-2915.2010.00887.x. View

Shaw A, Monaghan P, Alpar H, Anthony S, Darpel K, Batten C . Development and initial evaluation of a real-time RT-PCR assay to detect bluetongue virus genome segment 1. J Virol Methods. 2007; 145(2):115-26. DOI: 10.1016/j.jviromet.2007.05.014. View

Mullens B, Gerry A, Lysyk T, Schmidtmann E . Environmental effects on vector competence and virogenesis of bluetongue virus in Culicoides: interpreting laboratory data in a field context. Vet Ital. 2010; 40(3):160-6. View

10.

Meiswinkel R, Gomulski L, Delecolle J, Goffredo M, Gasperi G . The taxonomy of Culicoides vector complexes - unfinished business. Vet Ital. 2010; 40(3):151-9. View

11.

Pages N, Munoz-Munoz F, Talavera S, Sarto V, Lorca C, Nunez J . Identification of cryptic species of Culicoides (Diptera: Ceratopogonidae) in the subgenus Culicoides and development of species-specific PCR assays based on barcode regions. Vet Parasitol. 2009; 165(3-4):298-310. DOI: 10.1016/j.vetpar.2009.07.020. View

12.

Maan N, Maan S, Belaganahalli M, Ostlund E, Johnson D, Nomikou K . Identification and differentiation of the twenty six bluetongue virus serotypes by RT-PCR amplification of the serotype-specific genome segment 2. PLoS One. 2012; 7(2):e32601. PMC: 3289656. DOI: 10.1371/journal.pone.0032601. View

13.

De Liberato C, Scavia G, Lorenzetti R, Scaramozzino P, Amaddeo D, Cardeti G . Identification of Culicoides obsoletus (Diptera: Ceratopogonidae) as a vector of bluetongue virus in central Italy. Vet Rec. 2005; 156(10):301-4. DOI: 10.1136/vr.156.10.301. View

14.

Del Rio Lopez R, Miranda M, Paredes-Esquivel C, Lucientes J, Calvete C, Estrada R . Recovery rates of bluetongue virus serotypes 1, 2, 4 and 8 Spanish strains from orally infected Culicoides imicola in South Africa. Med Vet Entomol. 2011; 26(2):162-7. DOI: 10.1111/j.1365-2915.2011.00990.x. View

15.

Kluiters G, Pages N, Carpenter S, Gardes L, Guis H, Baylis M . Morphometric discrimination of two sympatric sibling species in the Palaearctic region, Culicoides obsoletus Meigen and C. scoticus Downes & Kettle (Diptera: Ceratopogonidae), vectors of bluetongue and Schmallenberg viruses. Parasit Vectors. 2016; 9:262. PMC: 4857416. DOI: 10.1186/s13071-016-1520-7. View

16.

Carpenter S, Wilson A, Barber J, Veronesi E, Mellor P, Venter G . Temperature dependence of the extrinsic incubation period of orbiviruses in Culicoides biting midges. PLoS One. 2011; 6(11):e27987. PMC: 3220716. DOI: 10.1371/journal.pone.0027987. View

17.

Dye C . The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol. 1992; 37:1-19. DOI: 10.1146/annurev.en.37.010192.000245. View

18.

Wilson A, Mellor P . Bluetongue in Europe: past, present and future. Philos Trans R Soc Lond B Biol Sci. 2009; 364(1530):2669-81. PMC: 2865089. DOI: 10.1098/rstb.2009.0091. View

19.

McDermott E, Mayo C, Gerry A, Laudier D, Maclachlan N, Mullens B . Bluetongue virus infection creates light averse Culicoides vectors and serious errors in transmission risk estimates. Parasit Vectors. 2015; 8:460. PMC: 4573699. DOI: 10.1186/s13071-015-1062-4. View

20.

Wilson A, Darpel K, Mellor P . Where does bluetongue virus sleep in the winter?. PLoS Biol. 2008; 6(8):e210. PMC: 2525685. DOI: 10.1371/journal.pbio.0060210. View