The spread of Culicoides spp. in the
Netherlands
The incidence of Insect Bite Hypersensitivity as sentinel
for African Horse Sickness
Drs. F.H.M. Schoot
Dr. M.M. Sloet van Oldruitenborgh-Oosterbaan
Index
Introduction
3
Insect Bite Hypersensitivity
3
African Horse Sickness
4
Materials and methods
Statistical Analysis
Results
5
5
6
The number of horses and pony’s in the Netherlands
6
The prevalence of IBH
7
Diagnostics, therapy and period of occurrence of IBH
9
The influence of landscape type on the prevalence of IBH
9
Discussion
11
Literature
14
2
The spread of Culicoides spp. in the Netherlands
The incidence of Insect Bite Hypersensitivity as sentinel for African Horse
Sickness
F.H.M. Schoot, M.M. Sloet van Oldruitenborgh-Oosterbaan
Introduction
Insect Bite Hypersensitivity
Insect Bite Hypersensitivity (IBH) is a seasonal, recurrent dermatitis based on type
I and type IV hypersensitivity reactions in horses. IBH is also known as ‘sweet
itch’, ‘summer eczema’, ‘Queensland itch’, ‘allergic dermatitis’, ‘kasen’ en ‘staarten maneneczeem’ and is the most common allergic skin disease in horses in the
world. The worldwide prevalence of IBH differs from 5-60% depending on
geographical regions and insect exposure (Baselgia, Doherr et al. 2006). Culicoides
spp. midges are thought to be the major cause of IBH, although other insects, such
as Similium, Stomoxys and Haematobia, may also play a role (Fadok and Greiner
1990). Worldwide, over a 1000 species of Culicoides are known, with different
species occurring in different geographical regions (Braverman 1994). In The
Netherlands there are approximately 100 species of which 5-10 biting species
(Beuk 2002). The female midges are the ones that bite and feed with blood for egg
production; the males feed with nectar (Gortel 1998). According to van der Rijt et
al 2007 C. obsoletus and C.pulicaris are mostly seen around horses in the
Netherlands and thereby most likely the major Culicoides spp. to cause IBH in
horses in the Netherlands. Beside IBH, Culicoides spp. are also the vector of the
Blue Tongue (BT) and African Horse Sickness (AHS) virus (Capela, Purse et al.
2003). The biting midges are mostly weak fliers and prefer to feed during warm,
dry weather with no considerable wind. The activity is most seen from twilight to
dusk (Gortel 1998).
Multiple factors are considered to play a role in the occurrence and the severity of
the symptoms, such as geographical location (McCaig 1973; Foster 1998; van
Grevenhof, Ducro et al. 2007), habitat (van Grevenhof, Ducro et al. 2007),
management (Pilsworth 2004), nutrition (O'Neill 2002), age of the horse (Baker
3
1978; Anderson, Belton et al. 1988; Littlewood 1998; Steinman, Peer et al. 2003),
age of first exposure to allergens (Halldordsottir 1991) and genetic predisposition
(Baker 1978; Pilsworth 2004). Although, the significance of the individually
factors is not yet fully understood, according to Steinman et al (2003) the
environmental factors are as important as the genetic basis to IBH.
IBH is characterised by intense pruritis particularly affecting the mane- and tail
basis (dorsal midline), although in some horses the ventral midline is (also)
affected (Sloet van Oldruitenborgh-Oosterbaan 2001). The pruritis is primarily
caused by erythema, oedema, vesicles and papules. Though, these symptoms are
mostly covered by self-inflicted trauma as localised alopecia, excoriations,
bleeding and crusting (Baker 1978). After repeated exposure to biting Culicoides
and therefore repeated occurrence of hypersensitivity more severe lesions can be
found, including acanthosis, hyperkeratosis, exsudation of serum and scaling
(Baker 1978; Anderson, Belton et al. 1988).
African Horse Sickness
African Horse Sickness (AHS) is a non-contagious, infectious disease caused by an
Orbivirus (African Horse Sickness virus, AHSV), of which 9 serotypes are known
(Mellor and Hamblin 2004). The virus is morphologically similar to other
orbiviruses such as the Blue Tongue virus (BTV).
The symptoms are caused by damage to the circulatory and respiratory systems.
This results in serous effusion and (severe) haemorrhage in various organs and
tissues.
Four forms of AHS are distinguished, in ascending order of severity these are horse
sickness fever, the cardio-pulmonary or mixed form, the subacute or cardiac form,
and the pulmonary form. The pulmonary form is the most common form seen in
areas with no AHS history (naïve populations). It is a peracute form and may
develop so rapidly that the infected animals can die without previous indication of
illness. Usually it is marked by depression, fever (39-41°C), respiratory distress,
severe dyspnoea and severe sweating. Mortality rates can extend up to 95%
(Coetzer 1994).
The cardiac form is the second common form of the disease seen in areas with no
AHS history (naïve populations). Mortality rates are approximately 70% and death
usually occurs within 3-6 days after onset of the fever (Coetzer 1994).
4
AHS is a vector-borne disease and is also transmitted by Culicoides midges, of
which C. imicola the most important. AHS is endemic in many areas in subSaharan Africa and possibly Yemen. However, AHS periodically makes excursions
beyond his endemic areas and has been reported also in India, Pakistan and in
Spain and Portugal. AHS has never been reported in central and northern Europe
(including the Netherlands). It is known that AHSV is able to overwinter in
southern Spain, Portugal and Morocco because an efficient vector species of
Culicoides is present in these regions and because the climate is sufficiently mild
for the adults of this vector to be active throughout the year (Mellor 1994;
Bouayoune, Touti et al. 1998; Capela, Purse et al. 2003). C. imicola is widespread
across southern Europe and recently found in southern Switzerland (at 46° N, the
furthest north that this species has so far been found anywhere in the world)
(Mellor and Hamblin 2004). This represents a real and general movement
northwards of this species, perhaps in response to climate change. Until recently it
was thought that C. imicola was the only Culicoides species to able to transmit
AHSV. During the 1987-1990 outbreaks of AHS in Spain and Portugal mostly
found vector of AHSV was indeed C imicola (Mellor, Boned et al. 1990).
However, isolations where also made from mixed pools of C. obsoletus and C.
pulicaris, excluding C. imicola. This suggests that either one or both of these
species might be able to transmit the AHSV in Europe (Mellor, Boned et al. 1990).
These two Culicoides species where also reported as the transmitting species in the
1998-2003 Blue Tongue outbreaks in Europe (Mellor 2002; Caracappa 2003;
Savini 2003). As BTV and AHSV utilise the same species of Culicoides as vectors
it is possible that in regions where C. obsoletus and C. pulicaris are abundant
future incursions of AHSV could also extend well beyond the distribution of C.
imicola. In this context, it should be noted that the obsoletus and pulicaris group of
midges are probably the commonest Culicoides species across the whole central
and northern of Europe, including the Netherlands (Mellor 2003). Furthermore,
AHSV infection rates of vector Culicoides and rates of virogenesis within them are
temperature dependent. Replication of AHSV does not seem to occur below 15°C
and at temperatures below this level the apparent infection rate rapidly falls to zero
(Wellby 1996). However, when midges are maintained for extended periods at
these cooler temperatures and then transferred to temperatures within the virus
permissive range, ‘latent’ virus that has presumably persisted at very low levels in
5
some individuals, commences replication and rapidly reaches sufficiently high
titres for transmission to occur (Wellby 1996).
Considering the facts described above, the aim of this study is to indicate the
spread of Culicoides biting midges throughout the Netherlands by mapping the
appearance of IBH throughout the country.
Materials and methods
A survey was designed for the members of the Netherlands Equine Veterinary
Association (NEVA) of the Royal Netherlands Veterinary Association (n=374). The
concerning veterinarians were alerted to the survey by e-mail, telephone and a
publication on the website of the Royal Netherlands Veterinary Association. The
survey was send to them by mail. The completed surveys were returned by mail
and e-mail. The participating veterinarians mostly practice equine medicine
throughout the Netherlands and therefore have a good and reliable view on the
matter of IBH. The survey contained questions relating to postal code area of the
practice, prevalence of IBH, period of occurrence, total amount of horses in the
practice, diagnostic and therapeutic matters and habitat (appendix 1). Data was
collected from October 2008 until February 2009 (response n=126). The data
contained 90 postal code areas and therefore covering 100% of The Netherlands.
Statistical analysis
Analyses of variance were performed to determine whether the factors and possible
interactions under study significantly influenced the prevalence of IBH. The
analyses of variance were performed separately for horses and pony’s. The factors
were related to IBH diagnostics and therapies, the prevalence of IBH and the
region (landscape type). Factors that were considered not significant (P>0.05) were
excluded from the model. The analyses were performed using the GLM procedure
(Statistical Analysis System, SAS Inst., Cary, NC, USA, version 9.1).
6
Results
The number of horses in the Netherlands
Although it was not the main goal of this study, the opportunity was taken to
indicate the total number and density of horses and pony’s in the Netherlands.
Therefore the respondents were asked to check the number of horses and pony’s
listed in their practice administration. The county was divided into ten regions to
ease the further assimilation of the data (table 1). According to the data the total
number of horses is 271,580 and 126,610 for pony’s. The regions ‘Zuid-Holland’
and ‘Achterhoek en Twente’ contain the highest number of horses, which is 40.7 %
of the total number of horses in the Netherlands. For pony’s the same regions
contained also the highest number, which is 44% of the total.
Number of
Number of
Number of
Regions
horses
pony's
respondents
Noord-Holland
29.600
10.400
11
Zuid-Holland
54.350
35.000
21
Veluwe en Polders
35.130
16.030
11
Zeeland en Zuid-Hollandse eilanden
15.000
4.200
6
Noord-Brabant
29.800
16.150
17
Limburg
14.200
6.150
11
Achterhoek en Twente
56.200
20.680
24
Drente, Zuid-Friesland, Zuid-Groningen
14.500
5.150
7
Noord-Friesland, Noord-Groningen, Wadden 17.700
8.250
11
Rivierenland
5.100
4.600
7
Total
271.580
126.610
126
Table 1: Number of horses and pony’s in different regions in The Netherlands and the amount of
survey respondents in the regions
The prevalence of IBH
For the analysis there was set a minimum of 50 horses and 50 pony’s per
respondent and therefore three records were deleted for horses and five records
were deleted for pony’s.
The observed mean prevalence is 6.79% in horses with a range of 0-40% (n=123).
The observed mean prevalence in pony’s is 8.39% with a range of 0-80% (n=121).
7
The mean prevalence’s are a weighted average in which the practices with higher
amounts of horses and pony’s had a bigger influence.
Prevalence (mean ± sd) of IBH in Horses and Pony's in The
Netherlands
25
Mean Prevalence of IBH in horses
Mean Prevalence of IBH in pony's
Prevalence (%)
20
15
10
5
an
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Regions in The Netherlands
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Figure 1: The prevalence of IBH in horses and pony’s in the Netherlands
In most regions the prevalence in pony’s was higher than the prevalence in horses,
apart from the regions ‘Noord-Holland’ and ‘Noord-Friesland, Noord-Groningen,
Wadden’. The regions ‘Noord-Brabant’ and ‘Limburg’ are high-risk areas for both
horses and pony’s. Striking is that the ‘Achterhoek, Twente’ region is a high-risk
area only for pony’s and not for horses. The areas with the low-risk for horses are
localized along the coastline and a small area in the centre of the country. The lowrisk areas for pony’s are localized along the northern coastline and in the north of
the Netherlands (figure 1 and 2).
8
< 4%
4 - 7%
7 - 10%
10 - 12%
> 12%
Figure 2: Map of the Netherlands showing IBH prevalence in horses (left) and pony’s (right) in
different regions in the Netherlands
Diagnostics, therapy and period of occurrence of IBH
All (100%) of the respondents (n=126) based the diagnosis IBH on clinical
symptoms (most of them in combination with other characteristics as described
below) and is therefore the most used characteristic to base an IBH diagnosis on in
the Netherlands. Ninety four point four percent also used seasonal predisposition,
67.2% also used race predisposition, 20% also used vector free housing of the
patient as a diagnostic therapy and 15% also used additional diagnostics (such as
blood tests, allergy tests and skin biopsy’s).
Several therapy methods were used, of which fly sheets (insect blankets) were the
most used therapy (90%). Other therapy methods were symptomatic treatment with
corticosteroids (82.5%), stabling (vector free environment, 81.7%), insect
repellents (72.2%) and other therapy’s such as food supply’s, fungal vaccines,
desensitizing, homoeopathy, herbs and sales/slaughter advice (31.7%).
The clinical symptoms start to appear in the second half of April (range MarchAugust) and disappear late October (range August-December).
The influence of landscape type on the prevalence of IBH
There were six landscape types of which the respondents could choose and they
were asked to choose the most common landscape type in their practice area. The
landscape types were pasture, dunes, heath land, mixed grove-pasture, forest and
9
city. 70.6% of the respondents mostly saw pasture, 54% mostly saw forest, 25.4%
mostly saw heath land, 21.4% mostly saw city landscape, 16.7% mostly saw mixed
grove-pasture and 5.6% mostly saw landscape of dunes.
It was found that the pasture, dune, heath land and mixed grove-pasture did not
have any significant influence on the prevalence of IHB in horses and pony’s. On
the contrary, the combination of forest and city landscapes did have a significant
influence on the prevalence of IBH (p<0.05). In the presence of forest and city the
prevalence in pony’s was 21.82%. In the presence of forest and the absence of city
the prevalence in pony’s was 9.10% and city without forest the prevalence in
pony’s was 7.49%. The same was found for the prevalence in horses: forest and
city 19.54%, forest without city 6.63% and city without forest 5.70% (figure 3).
Influence of forest and city landscapes on the prevalence
(mean ± sd) of IBH
30
Prevalence (%)
25
20
Mean Prevalence of IBH in pony's
15
Mean Prevalence of IBH in horses
10
5
0
Forest
City
Forest and
City
Neither Forest
nor City
Landscape type
Figure 3: The influence of forest and city landscapes on the prevalence of IBH in pony’s and
horses
Apart from the landscape types there was also asked about the share of non flowing
water in the practice area. The mean percentage of non flowing water was 9% with
a range of 0.1-75%. To ease the assimilation, the share of non flowing water is
given in three percentage groups: 1 0-5% (63% of the respondents), 2 6-15% (21%
of the respondents) and 3 >16% (11.5% of the respondents). It was found that the
higher the percentage of non flowing water, the higher the prevalence of IBH in
pony’s and horses kept in this areas (figure 4). The prevalence in the first group
10
was: 7.73% for pony’s and 5.36% for horses, in the second group 10.42% for
pony’s and 11.12 for horses and in the third group 15.99% for pony’s and 12.45%
for horses.
The influence of non flowing water on the prevalence
(mean ± sd) of IBH
20,00
18,00
Prevalence ((%)
16,00
14,00
Mean Prevalence of IBH in
pony's
12,00
10,00
Mean Prevalence of IBH in
horses
8,00
6,00
4,00
2,00
0,00
0 tot 5
6 tot 15
>16
Percentage of non flowing water (%)
Figure 4: The influence of non flowing water on the prevalence of IBH in pony’s and horses
Discussion
Although the returned and completed surveys contained 33.6% (n=126) of the total
sent (n=374), the authors think this is a reliable amount to base their conclusions
on. Dear the fact that many of the respondents participate in the same equine
practice and completed only one survey per practice, thereby representing a lot
more equine practitioners than the returned number of surveys.
Apart from the primary aim of the study the opportunity was taken to indicate the
total number of horses and pony’s within the Netherlands. The numbers are based
on the numbers listed in the databases of the responded equine practitioners. It
must be said that not all equine practitioners responded and not all horse owners in
the Netherlands did visit a veterinarian once. Therefore, care must be taken
interpreting these numbers.
The prevalence’s found are not in line with van Grevenhof (2007), who reported
prevalence’s of 18% in Friesian mares and 8% in Shetland mares in the
Netherlands. This discrepancy could be explained by the fact that van Grevenhof
only inspected Friesian and Shetland mares and in the present study all horse and
11
pony breeds were included. This could also be the reason of the discrepancy
between the prevalence maps of the Netherlands presented in this study and the
map presented by van Grevenhof. However, a resemblance can be in seen in the
prevalence maps presented by van den Boom (2008). The high and low risk areas
according to van den Boom are almost similar to the ones found in the present
study, apart from the most southern part of the ‘Limburg’ region. In the present
study it is a high risk area. Van den Boom did not make an estimate of the
prevalence in this area because not enough respondents from ´Limburg` retuned a
completed survey.
The explanation for the high risk areas found in the present study could be the
climate. According to van Grevenhof these areas have a higher amount of warm
days (with a maximum temperature higher than 20˚C) than the rest of the
Netherlands. Considering the fact that Culicoides spp. need a warm climate to
survive and replicate, this could be a good explanation for these areas to be high
risk areas for IBH.
The fact that the ‘Achterhoek en Twente’ region is a high risk area only for pony’s
and not for horses could be explained by the fact that this region contains the
second highest amount of pony’s in the Netherlands, however this region also
contains the highest amount of horses and it is not a high risk area for horses. A
possible explanation could be that the ‘Achterhoek en Twente’ region contains
more pony breeds with race predisposition compared with the rest of the
Netherlands. According to van Grevenhof’s prevalence map of the Netherlands, the
area corresponding with the ‘Achterhoek en Twente’ region is an area with high
IBH prevalence. Considering that van Grevenhof only inspected Friesian and
Shetland mares (it is thought that both of them have a distinct genetic
predisposition for IBH), it could be possible that the population of Shetland pony’s
in the ‘Achterhoek en Twente’ region is considerably higher than in the rest of the
Netherlands.
In most regions the prevalence in pony’s was higher than the prevalence in horses,
apart from the regions ‘Noord-Holland’ and ‘Noord-Friesland, Noord-Groningen,
Wadden’. The explanation for this could be that in these two regions, compared
with the rest of the Netherlands, considerable more Friesian horses are kept. As
mentioned before, it is thought that the Friesian breed has a distinct genetic
12
predisposition for developing IBH and therefore explaining the higher prevalence
than pony’s in that particular area.
The higher overall prevalence as well as the greater prevalence range in pony’s
could be explained by the housing method. Often, pony’s are kept outdoors day
and night and are therefore a much easier target for the Culicoides spp. than horses
that are (partially) kept indoors. According to van Grevenhof, horses continuously
kept indoors showed more IBH than horses kept stabled part-time or kept
continuously on pasture. However, as considered by van Grevenhof, this is
probably a consequence rather than a causative association, because horses with
signs of IBH are often kept stabled as a therapeutic matter.
The finding that dunes did not have a significant influence on the prevalence of
IHB in horses and pony’s, was also reported by van Grevenhof (2007). On the
contrary, van Grevenhof reported that clay soils combined with heather had an
increasing effect on IBH prevalence. That was not found in the present study.
The finding of the significant influence of the forest-city landscape combination on
the IBH prevalence could be explained by the assumption that these two landscape
types can be considered as ideal environment for Culidoides spp. to reproduce and
survive within the Netherlands. As reported by Gortel (1998) Culicoides spp. are
mostly weak flyers and prefer warm, dry weather with no considerable wind.
Considering that, forest and city environment offer good shelter from the weather
and because of the shelter of for instance tree’s and buildings, the warmth is kept in
the environment offering better (higher) temperatures for the midges. Therefore
these two landscape types offer better conditions for Culicoides spp. than the other
landscape types (pasture, dunes, heath land and mixed grove-pasture). It was tried
to separate the influences of the two landscape types, but the influence of this
combination appeared to be so intertwined, that the separate influences on the
prevalence could not be set.
The influence of the non-flowing water areas could easily be explained by the fact
that Culicoides spp. use non-flowing water in their reproduction cycle (Nelson and
Bellamy 1971). The higher the non-flowing water percentage, the better the
reproduction conditions and the more midges are able to reproduce. Beside this it
must be mentioned that the city landscape could easily contribute to this matter,
considering the non-flowing water on for instance roofs and in gutters.
13
In conclusion: The present study indentified the IBH prevalence and a number of
factors that appear to play a role in the prevalence of IBH in horses and pony’s in
the Netherlands. Coastal line areas are identified as low risk areas for IBH and
´Noord-Brabant` and ´Limburg` are high risk areas for both horses and pony´s. The
´Achterhoek and Twente` region is a high risk area just for pony´s.
Literature
1. Anderson, G. S., P. Belton, et al. (1988). "The Hypersensitivity of Horses to
Culicoides Bites in British Columbia." Can Vet J 29(9): 718-723.
2. Baker, K. P., Quinn, P.J. (1978). "A report on clinical aspects and
histopathology of sweet itch." Equine Vet J 22: 243-248.
3. Baselgia, S., M. G. Doherr, et al. (2006). "Evaluation of an in vitro
sulphidoleukotriene release test for diagnosis of insect bite hypersensitivity
in horses." Equine Vet J 38(1): 40-6
4. Baylis, M., H. el Hasnaoui, et al. (1997). "The spatial and seasonal
distribution of African horse sickness and its potential Culicoides vectors in
Morocco." Med Vet Entomol 11(3): 203-12.
5. Beuk, P. L. T. (2002). Checklist of the Diptera of the Netherlands. Utrecht,
KNNV Uitgeverij: 1-448.
6. Bouayoune, H., J. Touti, et al. (1998). "The Culicoides vectors of African
horse sickness virus in Morocco: distribution and epidemiological
implications." Arch Virol Suppl 14: 113-25.
7. Braverman, Y. (1994). "Nematocera (Ceratopogonidae, Psychodidae,
Simuliidae and Culicidae) and control methods." Rev Sci Tech 13(4): 117599.
8. Capela, R., B. V. Purse, et al. (2003). "Spatial distribution of Culicoides
species in Portugal in relation to the transmission of African horse sickness
and bluetongue viruses." Med Vet Entomol 17(2): 165-77.
9. Caracappa, S., Torina, A., Guerico, A., Vitale, M., Calabro, A., Purpari, G.,
Vitale, F., Mellor, P.S., (2003). "Identification of a novel bluetongue virus
vector species of Culicoides in Sicily." Vet. Rec. 153: 71-74.
10. Coetzer, J. A. W., Erasmus, B.J. (1994). African horse sickness. Infectious
diseases of livestock with special reference to southern Africa. J. A. W.
14
Coetzer, Thompson G.R., Tustin R.C. (Eds). Cape Town, Oxforf University
Press. 1: 460-475.
11. de Raat, I. J., R. van den Boom, et al. (2008). "The effect of a topical
insecticide containing permethrin on the number of Culicoides midges
caught near horses with and without insect bite hypersensitivity in the
Netherlands." Tijdschr Diergeneeskd 133(20): 838-42
12. Fadok, V. A. and E. C. Greiner (1990). "Equine insect hypersensitivity:
skin test and biopsy results correlated with clinical data." Equine Vet J
22(4): 236-40.
13. Foster, A. P., Cunningham, F.M. (1998). The pathogenesis ans
immunopharmacology of equine insect hypersensitivity. Advances in
Veterinary Dermatology. the third World Congress of Veterinary
Dermatology.
14. Gortel, K. (1998). "Equine parasitic hypersensitivity." Equine Pract 20: 1416.
15. Halldordsottir, S., Larsen, H.J. (1991). "An epidemiological study of
summer eczema in Icelandic horses in Norway." Equine Vet J 23: 296-299.
16. Littlewood, J. D. (1998). "Incidence of recurrent seasonal pruritis ('sweet
itch') in British and German shire horses." Vet Rec 142: 66-67.
17. McCaig, J. A. (1973). " A survey to establish the incidence of sweet itch in
ponies in the United Kingdom." Vet Rec 93: 444-446.
18. Meiswinkel, R., T. Baldet, et al. (2008). "The 2006 outbreak of bluetongue
in northern Europe--the entomological perspective." Prev Vet Med 87(1-2):
55-63.
19. Meiswinkel, R., M. Goffredo, et al. (2008). "Endophily in Culicoides
associated with BTV-infected cattle in the province of Limburg, southeastern Netherlands, 2006." Prev Vet Med 87(1-2): 182-95.
20. Meiswinkel, R., M. Goffredo, et al. (2008). "The Culicoides 'snapshot': a
novel approach used to assess vector densities widely and rapidly during
the 2006 outbreak of bluetongue (BT) in The Netherlands." Prev Vet Med
87(1-2): 98-118.
21. Mellor, P. S., Capela, R., Hamblin, C., Hooghuis, H., Mertens, P.P.C.,
Plateau, E., Vizcaino, J.M. (1994). African horse sickness in Europe,
15
epidemiology. Conf. Equine Inf. Dis., Proc 7th Int. P. W. Nakajima N.
Tokyo, Japan, R&W Publications: 61-64.
22. Mellor, P. S. (1994). "Epizootiology and vectors of African horse sickness
virus." Comp Immunol Microbiol Infect Dis 17(3-4): 287-96.
23. Mellor, P. S., Witteman, E.J. (2002). "Bluetongue virus in the
Mediterranean Basin." Vet J 164: 20-37.
24. Mellor, P. S. (2003). Infection of the vectors and bluetongue epidemiology
en Europe. 3rd OIE Bluetongue International Symposium, Taormina,
Sicily.
25. Mellor, P. S., J. Boned, et al. (1990). "Isolations of African horse sickness
virus from vector insects made during the 1988 epizootic in Spain."
Epidemiol Infect 105(2): 447-54.
26. Mellor, P. S. and C. Hamblin (2004). "African horse sickness." Vet Res
35(4): 445-66.
27. Nelson, R. L., Bellamy, R.E. (1971). "Patterns of flight activity of
Culicoides variipennis (Coquillet) (Diptera: Ceratopogonidea)." Journal of
Medical Entomology 8: 283-291.
28. O'Neill, W., McKee, S., Clarke, A.F. (2002). "Flaxseed (Linum
usitatissimum) supplementation associated with reduced skin test lesional
area in horses with Culicoides hypersensitivity." Can J Vet Res 66: 272277.
29. Pilsworth, R. C., Knottenbelt, D.C. (2004). "Skin diseases refresher: equine
insect hypersensitivity." Equine Vet Educ 16: 324-325.
30. Savini, G., Goffredo, M., Monaco de Santis, P., Meiswinkel, R. (2003).
"Transmission of bluetongue virus in Italy." Vet. Rec. 152: 119.
31. Sloet van Oldruitenborgh-Oosterbaan, M. M. (2001). Immune mediated and
allergic diseases. Practitioners's guide to equine dermatology. K. D. C.
Sloet van Oldruitenborgh-Oosterbaan M. M. Leeuwarden, The Netherlands,
Libre: 52-53.
32. Steinman, A., G. Peer, et al. (2003). "Epidemiological study of Culicoides
hypersensitivity in horses in Israel." Vet Rec 152(24): 748-51.
16
33. van den Boom, R., B. Ducro, et al. (2008). "Identification of factors
associated with the development of insect bite hypersensitivity in horses in
The Netherlands." Tijdschr Diergeneeskd 133(13): 554-9.
34. van der Rijt, R., R. van den Boom, et al. (2008). "Culicoides species
attracted to horses with and without insect hypersensitivity." Vet J 178(1):
91-7.
35. van Grevenhof, E. M., B. Ducro, et al. (2007). "Identification of
environmental factors affecting the prevalence of insect bite
hypersensitivity in Shetland ponies and Friesian horses in The
Netherlands." Equine Vet J 39(1): 69-73.
36. Wellby, M. P., Baylis, M., Rawlings, P., Mellor, P.S. (1996). "Effects of
temperature on the rate of virogenesis of Afrivan horse sicjness virus in
Culicoides (Diptera: Ceratopogonidae) and its significance in relation to the
epidemiology of the disease." Med Vet Entomol 86: 715-720.
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