Culicoides
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Top of pagePreferred Scientific Name
- 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
Overview
Top of pageContext 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.
Host Animals
Top of pageAnimal name | Context | Life stage | System |
---|---|---|---|
Bos indicus (zebu) | |||
Bos taurus (cattle) | |||
Ovis aries (sheep) |
Hosts/Species Affected
Top of pageMost Culicoides species display some degree of host preference, which have direct implications regarding their potential role as disease vectors. Some species prefer to feed on birds (for example Culicoides arakawae), whereas others prefer mammals, often feeding on large mammals such as horses, cattle and deer. This groups of species includes Culicoides imicola (Service et al., 1986) and Culicoides impunctatus (Blackwell et al., 1994, 1995). Within the mammalophilic species there can be host preferences. For example in the USA, Culicoides variipennis feeds preferentially on cattle and Culicoides crepuscularis on sheep (Raich et al., 1997). In Hanover, Germany, female midges (Culicoides heliophilus, Culicoides lupicaris and Culicoides scotius) 'prefer’ to attack large, predominantly dark cattle, feeding mainly in the evening (17.00 - 20.00 h) and feeding on the neck or abdomen (Olbrich and Liebisch, 1988).
Still, warm and humid conditions encourage blood-feeding. The majority of economically-important species are crepuscular and often have peaks of activity at dawn and dusk. The economically important species include Culicoides furens and Culicoides barbosai (Kettle, 1968), Culicoides punctatus, Culicoides pictipennis and Culicoides obsoletus (Service, 1971), Culicoides imicola (Braverman, 1992), Culicoides brevitarsis (Bishop et al., 1995), Culicoides variipennis sonorensis (Mullens, 1995) and Culicoides impunctatus (Blackwell, 1997). Other species have less obvious patterns of activity, including the Culicoides imicola and Culicoides schultzei group, whose flight activity is extended throughout the night in Kenya (Walker, 1977). Midge activity is often temperature-dependent. For example, the numbers of Culicoides trapped around dairy cows in Botswana (including Culicoides imicola) were correlated with the daily minimum and maximum temperatures (Mushi et al., 1998). Activity can also be negatively correlated with insolation (e.g. Culicoides pseudodiabolicus in Brazil (Veras and Castellón, 1998)).
Systems Affected
Top of pageskin and ocular diseases of pigs
skin and ocular diseases of small ruminants
Distribution
Top of pageCulicoides are found worldwide. The only large inhabited land-masses where they are known to be absent are New Zealand and the southern most areas of South America. The distribution and activity of the Culicoides species is related to the availability of suitable breeding grounds, bloodmeal hosts and also to climate (temperature, rainfall, humidity and insolation).
Pathology
Top of pageDetails 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.
Diagnosis
Top of pageDetails on diagnosis of bluetongue, epizootic haemorrhagic disease, African horse sickness, Akabane infection and bovine ephemeral fever are given in the relevant disease datasheets.
Allergic dermatitis
Clinical diagnosis of allergic dermatitis involves the initial lesions, which usually take the form of discrete papules on the dorsal surfaces. This is followed by the formation of hair mats and crusts, which fall off or are rubbed off, leaving hairless area. The animal may also develop intense pruritus. This usually affects the mane and tail of horses.
Nematode infection: Oncocherca species
In equines infection leads to a painless, diffuse swelling, which increases in size to a palpable soft lump and then regresses to a calcified focus. In cattle infection leads to a fibrous reaction in muscle tissue. These symptoms are the basis of a clinical diagnosis.
Laboratory diagnosis involves looking for the presence of microfilariae in skin biopsy samples, which have been warmed in saline, teased to allow microfilariae emergence and incubated for 6h. The samples are best taken from the chosen feeding sites of Culicoides (i.e. the shaded, lower parts of the trunk).
Protozoan transmission: Haemoproteus infection
Birds usually show no signs of infection following being bitten by an infected insect. Presence of infection is usually an incidental finding. However, heavy infections can occur, resulting in restlessness, lowered feed intake, lameness, diarrhoea and possibly anaemia. Birds can also develop hepatic and renal lesions.
Differential diagnosis should include avian malaria, and Leucocytozoonosis. Laboratory diagnosis is achieved by detection of gamonts in peripheral blood smears.
Protozoan transmission: Leucocytozoon caulleryi
Clinical symptoms used for diagnosis include anorexia, emaciation and lameness. Infected birds also have green excrement. High chick mortality is a further sign, and reduced egg production in adult birds. Post mortem examination may reveal renal lesions.
Differential diagnosis should include avian malaria (caused by mosquito-transmitted Plasmodium spp.) and Haemoproteus spp. Infection. Detection of gamonts in peripheral blood smears is the method used for laboratory diagnosis.
List of Symptoms/Signs
Top of pageSign | Life Stages | Type |
---|---|---|
General Signs / Petechiae or ecchymoses, bruises, ecchymosis | Sign | |
Nervous Signs / Hyperesthesia, irritable, hyperactive | Sign | |
Pain / Discomfort Signs / Skin pain | Sign | |
Pain / Discomfort Signs / Skin pain | Sign | |
Skin / Integumentary Signs / Alopecia, thinning, shedding, easily epilated, loss of, hair | Sign | |
Skin / Integumentary Signs / Alopecia, thinning, shedding, easily epilated, loss of, hair | Sign | |
Skin / Integumentary Signs / Cracked skin, fissure | Sign | |
Skin / Integumentary Signs / Hyperkeratosis, thick skin | Sign | |
Skin / Integumentary Signs / Matted or dirty hair | Sign | |
Skin / Integumentary Signs / Moist skin, hair or feathers | Sign | |
Skin / Integumentary Signs / Parasite visible, skin, hair, feathers | Sign | |
Skin / Integumentary Signs / Parasite visible, skin, hair, feathers | Sign | |
Skin / Integumentary Signs / Pruritus, itching skin | Cattle and Buffaloes|All Stages; Other|All Stages; Sheep and Goats|All Stages | Diagnosis |
Skin / Integumentary Signs / Rough hair coat, dull, standing on end | Sign | |
Skin / Integumentary Signs / Rough hair coat, dull, standing on end | Sign | |
Skin / Integumentary Signs / Skin crusts, scabs | Cattle and Buffaloes|All Stages; Other|All Stages; Sheep and Goats|All Stages | Diagnosis |
Skin / Integumentary Signs / Skin edema | Sign | |
Skin / Integumentary Signs / Skin erythema, inflammation, redness | Sign | |
Skin / Integumentary Signs / Skin erythema, inflammation, redness | Sign | |
Skin / Integumentary Signs / Skin hypopigmentation, decreased pigment, vitiligo | Sign | |
Skin / Integumentary Signs / Skin papules | Cattle and Buffaloes|All Stages; Other|All Stages; Sheep and Goats|All Stages | Diagnosis |
Skin / Integumentary Signs / Skin plaque | Sign | |
Skin / Integumentary Signs / Skin scales, flakes, peeling | Sign | |
Skin / Integumentary Signs / Skin scales, flakes, peeling | Sign | |
Skin / Integumentary Signs / Skin ulcer, erosion, excoriation | Sign | |
Skin / Integumentary Signs / Skin ulcer, erosion, excoriation | Sign | |
Skin / Integumentary Signs / Skin vesicles, bullae, blisters | Sign | |
Skin / Integumentary Signs / Skin wheal, welt | Sign |
Disease Course
Top of pageAllergic 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.
Epidemiology
Top of pageLife 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).
Impact: Economic
Top of pageThere 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.
Disease Treatment
Top of pageInsecticides
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).
Prevention and Control
Top of pageImmunization and vaccines
Immunization and vaccination against the pathogens carried and transmitted by the biting midges are available.
- Bluetongue: A vaccination is available with modified live virus vaccine. Serotypes incorporated into the vaccine must be the same as those causing infection in the field.
- African Horse Sickness: vaccination of non-infected horses can be carried out using either a polyvalent vaccine, monovalent vaccine (works more efficiently when the virus has been typed) and monovalent inactivated vaccine (only available for sero-type 4).
- Akabane: vaccines are available in Australia and Japan, they are either formalin- and betapropiolactone-inactivated, aluminium phosphage gel-absorbed vaccines or an attenuated vaccine.
- Epizootic haemorrhagic disease virus and Ibaraki have no available vaccines.
- Bovine ephemeral Fever, there is a vaccine giving 6 months protection (Vanselow et al., 1985).
Farm-level control (movement, housing, sanitation, vaccines)
Control of the biting midges can be aided by removal of breeding sites favoured by Culicoides species. These include stagnant mud/water, which can often be contaminated with animal excreta. Another preventative measure is the use of pyrethroid-impregnated ear tags to protect cattle (Olbrich et al., 1988). Cleansing and disinfection of animal houses and insecticide applied to animals and premises also controls infections.
With bovine ephemeral fever, complete rest of cattle during acute illness and convalesence, will aid recovery, as will treatment with anti-inflammatory drugs. If infection with Onchocerca species occurs microfilariae can be killed with a single dose of ivermectin (0.2-0.5 mg/kg). Poultry can be protected from Culicoides with insecticide-painted nets (Bamba et al., 1995). Vector control is not practical in the case of Haemoproteus infections, but quinine and other members of the quinacrine group are effective against the parasite. Drug treatment in the form of pyrimethamine and sulphonamide are effective against Leucocytozoon caulleryi infections.
Local/national control (vaccination, restriction of movement, regulation)
Vector control programmes include the use of insecticides, repellents, screens and baited traps (e.g. CO2 and live baits (e.g. cattle) (Mullens and Gerry, 1998)). Affected farms should be placed under quarantine. Identification of animals by ear-tagging is important incase of infections. Carcasses should be buried. In the case of bluetongue, maintenance of sentinel cattle herds, with regular seroconversion tests is recommended (Ward et al., 1997).
References
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