An updated review on bluetongue virus: epidemiology, pathobiology, and advances in diagnosis and control with special reference to India

Abstract

Bluetongue (BT) is an economically important, non-contagious viral disease of domestic and wild ruminants. BT is caused by BT virus (BTV) and it belongs to the genus Orbivirus and family Reoviridae. BTV is transmitted by Culicoides midges and causes clinical disease in sheep, white-tailed deer, pronghorn antelope, bighorn sheep, and subclinical manifestation in cattle, goats and camelids. BT is a World Organization for Animal Health (OIE) listed multispecies disease and causes great socio-economic losses. To date, 28 serotypes of BTV have been reported worldwide and 23 serotypes have been reported from India. Transplacental transmission (TPT) and fetal abnormalities in ruminants had been reported with cell culture adopted live-attenuated vaccine strains of BTV. However, emergence of BTV-8 in Europe during 2006, confirmed TPT of wild-type/field strains of BTV. Diagnosis of BT is more important for control of disease and to ensure BTV-free trade of animals and their products. Reverse transcription polymerase chain reaction, agar gel immunodiffusion assay and competitive enzyme-linked immunosorbent assay are found to be sensitive and OIE recommended tests for diagnosis of BTV for international trade. Control measures include mass vaccination (most effective method), serological and entomological surveillance, forming restriction zones and sentinel programs. Major hindrances with control of BT in India are the presence of multiple BTV serotypes, high density of ruminant and vector populations. A pentavalent inactivated, adjuvanted vaccine is administered currently in India to control BT. Recombinant vaccines with DIVA strategies are urgently needed to combat this disease. This review is the first to summarise the seroprevalence of BTV in India for 40 years, economic impact and pathobiology.

Keywords: Cattle; Indian scenario; bluetongue virus; control; diagnosis; epidemiology; goat; immune responses; mice model; pathogenesis; pathology; sheep; vaccination.

Figure 1.

Seroprevalence of bluetongue virus in different States of India among various species of animals. The seroprevalence data was expressed as percentage. Seroprevalence data for Telangana and Andhra Pradesh States were mentioned together. The references for mentioned data were available in Table 3.

Figure 2.

Various routes of transmission of bluetongue virus. Adult Culicoides spp. bites the infected ruminants, suck blood, virus replicate in vectors, and transmit to other susceptible animals by bite. The virus also transmitted to other susceptible animals by various routes like contact, oral, transplacental, venereal, mechanical, and iatrogenic transmission.

Figure 3.

Pathogenesis of bluetongue virus in ruminants. After bite of an infected Culicoides spp. in ruminants, virus is transported by dendritic cells of skin to regional lymph nodes where primary replication occurs. Then virus reaches blood circulation, then disseminated to secondary organs where virus replicates in endothelium, and mononuclear phagocytes (dendritic cells, macrophages, etc). As a result of endothelial damage, excessive levels of various cytokines and vasoactive mediators are released (cytokine storm), which are responsible for pathogenesis of BT like increased vascular permeability, severe haemorrhages, oedema and effusions, thrombosis, infarction and disseminated intravascular coagulation. BTV infection in pregnant ruminants results in cerebral malformations in offspring.

Figure 4.

Clinical signs and gross lesions in bluetongue virus infected sheep. a. Hyperaemia and oedema of lips and nostrils with serous to mucoid nasal discharge. Lips are swollen with greyish brown necrotic deposition. b. Nasal area showed rhinitis and occluded by mucopurulent nasal discharge and excoriations. c. Oral mucosa showed congestion and oedema. d. BTV affected sheep showing weight loss, severe lethargy, dermatitis and break in the wool. Weakness, torticollis and reluctancy to move (knee-walking) as a result of necrosis of skeletal muscles and coronitis. e. Hyperaemia of coronary band (coronitis) in the feet. f. Lungs were heavy, oedematous, congested, haemorrhagic, and not collapsed. Areas of consolidation and emphysematous changes were noticed in apical and diaphragmatic lobes.

Figure 5.

Histopathological lesions and immunohistochemical localization of bluetongue virus antigen in sheep and IFNAR1-blocked mice. a. Pulmonary artery of sheep showing severe hemorrhage, degeneration and hyalinization of tunica media. H&E, scale bar 200 µm. b. Lymph node of sheep showing severe hemorrhages and oedema in the medulla. H&E, scale bar 200 µm. c. Brain of sheep showd endothelial cell damage, severe hemorrhages and oedema in cerebrum. H&E, scale bar 200 µm. d. Lungs of IFNAR1-blocked mice showing severe hemorrhages and oedema due to endothelial damage. H&E, scale bar 200 µm. e. Lymph node of IFNAR1-blocked mice showing lymphoid depletion and starry-sky pattern due to apoptosis of lymphocytes. H&E, scale bar 200 µm. f. Positive immunolabelling of BTV antigen in the cytoplasm of mononuclear cells of skin of sheep. IP-DAB-MH, scale bar 200 µm.