Culicoides

International Common Names

• English: biting midges; flies, biting midges; insect hypersensitivity causing skin disease in horses, cattle and sheep; midges; seasonal pruritic, allergic, dermatitis, atopy, in horses, sheep

Parasitoses name

• Culicoides hypersensitivity
• kasen
• midge bites
• Queensland itch
• sweet itch
• sweet itch in horses

Context and history

Culicoides species (biting midges) can, depending on their geographical location, also be called ‘sandflies’ (not to be confused with the phlebotomine sandflies), ‘punkies’, ‘no-see-ums’, 'no-nos’, ‘moose-flies’ or ‘biting gnats’ (Boorman, 1993). There are more than 1400 named species of Culicoides and approximately 50 have been implicated in vectoring various pathogens and parasites to man and other animals.

Taxonomy and nomenclature

Biting midge identification and classification are based essentially on morphological characteristics. To date, only very few cytotaxonomic studies have been carried out, although some Culicoides groups have been examined by enzyme electrophoresis (Culicoides varipennis (Nunamaker and McKinnon, 1989)) and most recently, DNA analysis has been applied to some groups, including Culicoides imicola (Linton, 1998). It is generally accepted that the specialized blood-sucking habits as seen in certain ceratopogonid genera, (including Culicoides) have evolved from more primitive predaceous habits, as outlined in Wirth et al. (1974).

Diseases/parasitoses caused

• Allergic dermatitis in livestock: This is particularly a problem for horses.
  
• Virus transmission to livestock: A number of viruses can be carried by Culicoides, including bluetongue, epizootic haemorrhagic disease, Ibaraki, African horse sickness, Palyam, akabane and bovine ephemeral fever.
  
• Nematode transmission to livestock: Nematodes that can be transmitted include Oncocherca cervicalis, which is a common parasite of horses.
  
• Protozoan transmission to livestock: Protozoa transmitted include Haemoproteus spp. avian parasites and Leucocytozooncaulleryi a parasite of poultry.
  
• Pathogen transmission to man:this is minimal. It includes three species of filarial worms in tropical and sub-tropical regions. For example Mansonella ozzardie, transmitted by C. phlebotomus in coastal North Trinidad (Nathan, 1981), and a small number of viruses, including Oropouche, which are strongly pathogenic to man (but not lethal) in parts of South America and the West Indies (Linley et al., 1983).

Importance of biting midges

In certain areas midges can occur in such large numbers that they can significantly disrupt outdoor activities (for example, tourism and outdoor industry) through their biting attacks on man (Linley and Davies, 1971; Hendry and Godwin, 1988; Blackwell, 2000). Sensitivity to midge bites is also responsible for allergic dermatitis developing in some animals. Culicoides species are the most important as vectors of a number of significant livestock pathogens, affecting both dairy and beef cattle, sheep and in certain areas, equines.

Details on the pathology of bluetongue, epizootic haemorrhagic disease, African horse sickness, Akabane infection and bovine ephemeral disease can be found in the relevant disease datasheets.

Direct effects of fly infestation

Fly infestation may cause irritation and hypersensitivity which leads to an intensely pruritic skin disease. This skin disease then leads to symptoms of 'sweet itch' (see Parasitosis Course for more details).

Nematode infections: Onchocerca species

'Fistulous withers' (open, purulent lesions) may occur in equines, although there is no direct causal relationship with Onchocerca infection.

Protozoan transmission: Haemoproteus infection

The spleen, liver and kidneys may become enlarged as a result of infection. Fusiform cysts develop in the skeletal muscles, and the lungs become oedematous lungs.

Leucocytozoon caulleryi infection

This causes haemoptysis and extensive haemorrhaging in the kidneys.

Allergic dermatitis in livestock

Allergic dermatitis is particularly a problem in horses, which is caused by members of the Culicoides species. It is known as ‘sweet itch’ (UK), 'Queensland Itch' (Australia), 'kasen' (Japan) and 'dhobie itch' (the Philippines). There have been only a small number of positive identifications of the causal agents of sweet itch. These include Culicoides pulicaris in the UK (Mellor, 1974) and C. obsoletus in Canada (Anderson et al., 1991) and C. robertsi in Australia (McGarry JW, 2002, Liverpool School of Tropical Medicine, UK, personal communication). Allergic dermatitis is an acutely irritating dermatitis, which is developed in response to midge saliva. It is primarily confined to the mane and tail, although it may spread to the rest of the body. As well as in horses, the condition can also occur in ponies, donkeys, cattle and sheep. In Israel, hypersensitive lesions in the skin of sheep, cattle and donkeys have been attributed to Culicoides obsoletus, the Culicoides schultzei group, Culicoides puncticollis and Culicoides imicola (Yeruham et al., 1993).

Bluetongue (BT)

BT is an infectious, non-contagious viral disease of domestic and wild ruminants. It is an OIE (‘Office International des Epizooties) List 'A' disease (Osburn, 1992; Erasmus, 1990). The virus can cause severe disease in some breeds of sheep. Proven vectors of the disease include Culicoides variipennis and Culicoides variipennis sonorensis in North America and southern Canada (Mellor and Boorman, 1995), Culicoides insignis and Culicoides pusillus in southern Florida, the Caribbean and Central America (Greiner et al., 1992). Culicoides imicola is a proven vector in the Old World (Mellor and Boorman, 1995) and Culicoides fulvus and Culicoides actoni in Australia and most of Asia (Ward, 1994). There are also a number of suspected vectors including: Culicoides oxystoma and Culicoides homotomus in China, Culicoides bolitinos and Culicoides cornutus in South Africa (Venter and Meiswinkel, 1994), Culicoides brevitarsis, Culicoides wadai and Culicoides brevipalpis in Australia and Asia (Ward, 1994). Also Culicoides obsoletus in Cyprus (Mellor and Pitzolis, 1979), Culicoides filarifer in the Caribbean and Central America (Greiner et al., 1992) and Culicoides boydi in southern California (Wirth and Mullens, 1992).

The virus replication period in Culicoides is 6-8 days. Infected midges remain infective for life. Once the host animal is bitten by the biting midge, virus incubation period in the host is 7-10 days. Viraemia is biphasic, occurring 3-4 days and 7 days post infection. Viraemias clear at 14-21 days.

Epizootic haemorrhagic disease

Proven vectors of epizootic haemorrhagic disease are Culicoides imicola and Culicoides varipennis (Mellor and Boorman, 1995). There are also a number of suspected vectors including Culicoides fulvus in Australia (Doyle, 1992), Culicoides oxystoma in the Sudan (Boorman, 1993), Culicoides pusillus in Puerto Rico (Mo et al., 1994) and Culicoides lahillei in the USA (Smith and Stallknecht, 1996).

Many deer are asymptomatic, but for those exhibiting signs of the disease, the first indication is depression, which is indicated by inactivity, loss of appetite, and failure to respond to threatening behaviour. Infected deer may be found near water (trying to alleviate dehydration and fever). Incidence of EHD outbreaks in deer is seasonal, usually in late summer when the numbers of biting midges are high.

There are three forms of the disease, per-acute, acute and chronic. Death can occur within 24 h of an outbreak.

African Horse Sickness

There are nine recognized serotypes of the Culicoides-transmitted orbivirus responsible for African Horse Sickness. African Horse Sickness is an OIE List 'A' disease. This is the most lethal of equine diseases, with mortality in excess of 90%. A proven vector of the disease is Culicoides imicola (Mellor and Boorman, 1995).

Palyam

Palyam is an orbivirus, with 10 serotypes which have been isolated from Culicoides in South Africa (Whistler et al., 1989). However there is no clear link with clinical disease. Chuzan virus (Kagashima virus) belongs to the Palyam subgroup and is responsible for Chuzan disease in Japan. This disease is characterised by a hydranencephaly-cerebellar hypoplasia (HCH) syndrome in calves (Miura et al., 1991).

Akabane

The akabane virus is a Culicoides-transmitted teratogenic virus, causing congenital arthrogryposis and hydranencephaly (A-H) syndrome and, less frequently, polioencephalomyelitis in the bovine, ovine and caprine foetuses after in utero infection (Walton, 1992).

Infection occurs during the first trimester of pregnancy and the virus is transmitted by mosquitoes or Culicoides to the pregnant female and is then transmitted to the foetus by transplacental passage.

Bovine ephemeral fever

Also known as 'three-day sickness'. Suspected vectors of bovine ephemeral fever are Culicoides coarctatus and Culicoides imicola in Zimbabwe (Blackburn et al., 1985), Culicoides schultzei, Culicoides homotomus and Culicoides nipponensis in China (Zhou, 1993), and Culicoides brevitarsis in Australia (Muller and Standfast, 1993).

Infection is most prevalent during the rainy seasons when Culicoides are most numerous. The virus is associated with the leucocyte fractions of blood and transmission occurs from the Culicoides to the host during blood feeding. The incubation period of the virus in the insect is unknown and mechanical transmission does not occur. Release of lymphokines mediate the host inflammatory process, resulting in the observed clinical symptoms. Once infected, animals usually develop life-long immunity upon recovery from disease.

Fibrinous exudates become apparent in the pleural, pericardial and peritoneal cavities and to varying extents in all joint capsules. Skeletal muscle lesions develop. Lungs and lymph nodes become oedematous.

Nematode transmission: Oncocherca spp.

Culicoides species (biting midges) are responsible for the transmission of a number of filarial worms to equines worldwide (Oncocherca cervicalis and possibly a second species, confined to the legs, Oncocherca reticulata) and cattle (Oncocherca gibsoni, which are confined to Africa, Asia and Australasia).

Microfilariae are ingested by midges as they feed. They develop to the third larval stage (L₃) after 20-25 days in the insect. Infection of the host animal with L₃ occurs during Culicoides feeding (often Culicoides nubeculosus). L₄, L₅ and adult worms develop in fibrous tissue (usually ligaments and intermuscular connective tissue). The primary sites in equines are ligamentum nuchae (most common) and the suspensory ligaments and flexor tendons of the lower limbs). In cattle, the primary sites are the subcutaneous and intermuscular nodules.

Protozoan transmission: Haemoproteus spp. avian parasites

More than 120 species of Haemoproteus protozoa infecting birds are transmitted by either the Culicoides species or hippoboscids (louse flies). Species found in domestic poultry and pet birds include Haemoproteus meleagridis in domestic and wild turkeys (Atkinson, 1991), Haemoproteus columbae and Haemoproteus saccharovi in pigeons and doves, and Haemoproteus nettionis in waterfowl (Mushi et al., 1999).

The birds become infected when bitten by Hippoboscid or Culicoides. Sporozoites enter the blood of the bird and invade the endothelial cells of the blood vessels, lungs, liver and spleen, forming schizonts. Schizonts develop to merozoites which enter the erythrocytes and become macrogametes and microgamonts after 28-30 days. Culicoides or Hippoboscid insects ingest the macrogametes and microgamonts with a bloodmeal.

In the insect, the sporozoites are formed and pass to the salivary gland to be injected into a new host.

Protozoan transmission: Leucocytozoon caulleryi avian parasite

Leucocytozoon caulleryi is an important poultry pathogen in Japan and south-east Asia, causing chick mortality and reduced egg production in adult hens. It causes leucocytozoonosis in birds. Domestic chickens are the only reported host of the parasite.

Known vectors for the parasite include Culicoides arakawa, C. circumscriptus and C. odibilis (Wei and Hu, 1988). Suspected vectors include C. effusus, C. peregrinus and C. palpifer in the Philippines (Abella et al., 1994). Sporozoites introduced during Culicoides bloodmeal follow the same path as the Haemoproteus spp.

Life cycles

Culicoides species have four larval instars, which are found in a variety of habitats from damp leaf litter to rotting fruit, where they live as omnivores/detritivores. Larvae of the species that are of veterinary importance are found frequently in mud contaminated with animal excreta. In temperate regions, species are usually univoltine (meaning only one generation annually), although a small number of species are bivoltine such as Culicoides impunctatus in Scotland (Blackwell et al., 1992). Where numerous generations can occur, development occurs rapidly. For example, up to seven generations have been recorded for Culicoides variipennis in Colorado, each with a development time of 14 days (Boorman, 1993). Either the larvae or the eggs act as the dormant stage in the life cycle.

Biting behaviour and disease transmission

The blood-feeding habit of female midges predisposes them to vectoring disease pathogens. Approximately 30 Culicoides species are autogenous, laying their first (and often largest) egg batch without requiring a bloodmeal (anautogeny; Linley, 1983). This is perhaps a mechanism that has evolved to promote survival in areas where bloodmeal hosts are scarce, as hypothesized for Culicoides impunctatus in Scotland (Blackwell et al., 1992). Subsequent egg batches of autogenous species (and all of those of anautogenous species) require a bloodmeal for egg maturation. Individual midges, which have laid their first egg batch (i.e. parous) may be determined by a red pigment in the abdominal epidermis, as occurs in Culicoides victoriae and Culicoides furens (Dyce, 1969).

Dispersal and distribution

The distances over which midges disperse are matters of contention. As well as playing an important role in midge population dynamics (Murray, 1987), dispersal distances can play an integral role in disease transmission. This is particularly the case with wind-borne dispersal. This was responsible for a bluetongue (BT) infection outbreak in New South Wales, Australia, 150-200 km from a major source of infection (Murray and Kirkland, 1995) and also for the introduction of epizootic haemorrhagic disease virus and BT virus into British Columbia in 1987 (Sellers and Maarouf, 1991).

There are very few quantifications of the economic importance of biting midge activity. The few that exist include an assessment of the impact of midge-transmitted Bluetongue virus in the USA. This virus causes annual losses estimated at US $125 million, due to restrictions on the movement of livestock and germplasm to bluetongue-free countries. In Australia: the cost of a major bovine-ephemeral-fever epidemic (Culicoides transmitted) is in excess of US $100 million and results from reduced milk yield in dairy herds, weight loss in beef animals and overall mortality (StGeorge, 1988).

Nematode infections, obtained through Culicoides bites, in cattle are responsible for economic losses due to carcass trimming.

Insecticides

Culicoides treatment is difficult due to the often widespread nature of their breeding sites, the high mobility of the adults and the wind-borne migration of adults into treated areas. Some reduction in Culicoides feeding on livestock is brought about by the application of permethrin (65% a.i.) to animals (Mullens, 1993) and ivermection has been reported to have a systemic effect on Culicoides brevitarsis for up to 15 days at antihelmintic dose rates (Standfast and Muller, 1989).

Parasitoids

There are no effective biological treatments for Culicoides species, although a number of parasites and pathogens are associated with them (Wirth, 1977). They can be parasitized by a mermethid nematode, Heleidormis magnapapula, and there is some indication that this parasitism alters the sex ratio of offspring (Paine and Mullens, 1994). This affects the number of females, which is the sex responsible for the blood feeding behaviour.

Medicinal plants and herbal preparations

In addition to traditional chemical repellents, there are a number of reports of herbal preparations; for example, eucalyptus-based repellent (Trigg and Hill, 1996).