Local investigation into the role of Culicoides species diversity (Diptera: Ceratopogonidae) in recurrent horse dermatitis cases in southwest France

doi:10.21203/rs.3.rs-5001818/v1

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Local investigation into the role of Culicoides species diversity (Diptera: Ceratopogonidae) in recurrent horse dermatitis cases in southwest France

https://doi.org/10.21203/rs.3.rs-5001818/v1

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Background. Insect bite hypersensitivity in horses (“sweet itch”) is the most common pruritic, chronic, seasonal, and recurrent dermatitis resulting from an allergic reaction in horses to the saliva of Diptera: Nematocera, primarily from the Culicoides genus. This dermatitis affects 10% of horses in France and is a major concern for the horse industry and private owners. Given the frequent occurrence of this health problem and the limited investigation in France, we conducted a field survey in the vicinity of a riding stable in south-western France with a reported chronic case of recurrent horse dermatitis to (i) characterize the Culicoides species associated with horse populations (hippophilic species) and (ii) estimate the relative abundance of the different species identified based on the trapping site location.

Methods. For this purpose, three OVI traps were set up for one night once a week, from mid-June to the end of July 2022, the known peak activity period. Traps were placed either indoors or outdoors at horse facilities.

Results. Twelve species were morphologically identified. Culicoides obsoletus and C. scoticus were predominant at all trapping sites. Culicoides circumscriptusand C. nubeculosus were the second most common species found, followed by C. punctatus, C. festivipennis, and C. pulicaris. Importantly, certain species (C. obsoletus / C. scoticus and C. circumscriptus) were found in significant quantities indoors.

Conclusions. The presence of these insects indoors in substantial numbers raises questions about the main prevention recommendation, which advises stabling horses from the end of the afternoon until the next morning.

insect bite hypersensitivity

Culicoides

France

Culicoides are small hematophagous biting midges (1-2.5 mm) with scale-free wings and a distinctive light and dark wing pattern, which is used with other morphological features in species identification. In addition to the nuisance to human and animal populations, these insects can impact livestock and human health by transmitting various pathogens. In France, the species list for biting midges includes 83 species for mainland France and 61 species for Corsica. Recently, four new species have been recorded in mainland France: Culicoides manchuriensis, Culicoides abchazicus, Culicoides ibericus, and Culicoides saevus (1–3).

In mainland France, the most commonly collected species are Culicoides obsoletus and Culicoides scoticus. These two species are usually referred to collectively as Culicoides obsoletus / Culicoides scoticus because females are morphologically indistinguishable. Other prevalent species include Culicoides chiopterus, Culicoides dewulfi, Culicoides pulicaris, Culicoides newsteadi, and Culicoides punctatus (2, 4, 5). Additionally, some species are widely collected in specific regions, such as Culicoides brunnicans in western France (6). In contrast, Culicoides chiopterus and Culicoides dewulfi are rarely found in Corsica, indicating regional variations in species distribution.

Some biting midge species of the genus Culicoides play a crucial role in the transmission of parasitic filariae (7) and act as vectors for several economically significant viruses that affect livestock worldwide, including Bluetongue virus (BTV), Epizootic Hemorrhagic Disease Virus (EHDV), Schmallenberg virus (SBV), Akabane virus (AKAV) and African Horse Sickness virus (AHS), (8–10). AHSV is closely related to EHDV and BTV, with both viruses currently emerging in Europe. The most recent introduction of AHSV into Europe occurred in Spain in 1987 (11). The European Food Safety Authority (EFSA) stresses the importance of collecting data on local populations of Culicoides to help prepare the best measures in case of a new AHSV introduction (12). In addition to their impact on livestock, Culicoides are vectors for the Oropouche virus, which affects human populations in Central and South America.

Culicoides are also responsible for causing seasonal allergic dermatitis in horses, commonly known as summer itch or sweet ich. This condition is triggered by allergens present in the saliva of the midges, leading to the most common pruritic dermatitis in horses. In France, 10% of horses are affected by this hypersensitivity (13), which causes severe itching and results in self-inflicted lesions mainly along the dorsal midline (14, 15). The ventral midline, head, and ears can also be affected (16), leading to secondary infections and impacting the horses' behavior and activity (17). The first clinical signs of this condition in horses born in Europe are generally observed between 2 and 5 years old (18).

For the majority of horses, the dermatitis appears in spring, intensifies in summer, and progressively regresses in autumn until it disappears, except in chronic cases where the lesions persist even during winter (15). This seasonality corresponds to the known peak activity period of Culicoides (19). As this condition is a frequent health problem, we conducted a field survey into an riding school with reported case of recurrent horse dermatitis to (i) characterize the Culicoides species associated with horse populations (hippophilic species) and (ii) estimate the relative abundance of the different species identified during the risk period based on the trapping site location.

Study sites

The study was performed in the South of France, Toulouse region, in the veterinary school equestrian centre (43°36’10’’N, 1°22’52’’E). This region has a transitional oceanic climate, between Mediterranean and continental (20). The area is characterized by the presence of various potential Culicoides hosts, such as domestic animals (e.g. sheep, cows, horses, cats, dogs), as well as many different wild animals (e.g. foxes, rodents, reptiles, birds, amphibians). The 10-hectare facility comprises 4 hectares of forest, multiple equestrian facilities for training and competitions, and 14 paddocks. Among the 77 horses at the riding centre, 16 are stabled at night throughout the year. A third of these horses are club horses, while the others are privately owned. One of the local horses, which arrived at the facility in 2020, a 7-year-old gelding, suffers annually from insect bite hypersensitivity.

Three trapping sites were selected based on their indoor-outdoor location, access to electricity, distance from the adjacent river and forest, and the presence or absence of horses (Table 1).

Table 1

Details of the sampling stations in the study area.
Station number		A	B	C
Coordinates	North	43°36'08''N	43°36'08''N	43°36'14''N
Coordinates	East	1°22'52''E	1°22'52''E	1°22'53''E
Altitude (m)		143	142	143
Trap location		Inside	Outside	Outside
Distance (m) from	stable	0	10	190
	river	143	235	175
	forest	310	300	125
Number of horses		16 horses	Ø	21 horses

Specimen collection and identification

Individuals were collected for one night using OVI traps, once a week, between June and July 2022. The capture period targeted the Culicoides peak of activity (2) which corresponds to the highest risk period for horse dermatitis. In the three sampling sites (Table 1), one OVI trap was set up and operated between 05:30 pm and 08:30 am for one night. Traps were placed at a height of 1.70 meters, protected from rain, but exposed to other weather conditions. Each collection tray was filled with 200 mL of soapy water before capture. Nets and UV light were checked at each installation and collection. For each trap during capture and collection, data were collected on the habitat (trap position, animal presence and/or abundance), weather conditions (rain, minimum and maximum temperature.) and site characteristics.

OVI traps are one of the most efficient and sensitive traps for Culicoides, capable of capturing even less abundant species (21). They have been used in several studies and, notably, since 2001, in the Culicoides surveillance network in France (1, 22, 23). Therefore, to facilitate comparison, we used the same capture, sorting, and identification protocols.

Briefly, after each night of capture, specimens were collected through a filter, placed in a pillbox, labelled, and stored in 70% alcohol at + 4°C. If the total number of insects exceeded 3 mL, a sub-sampling was carried out following previously described protocol (24). Culicoides were identified morphologically according to the determination key of Delécolle (25) and the IIKC database (26). The following criteria were used: sensory fosse shape and size, number and arrangement of wing spots, spermathecae for female, and aedeagus or parameres for male. Identification was conducted to the species or complex level for morphologically indistinguishable species. Sex and parity were recorded, with parity determined using abdomen pigmentation (9).

Statistical analyses

Statistical analyses were performed using R studio software (27). Differences between traps and dates were analyzed with a non-parametric Kruskal-Wallis test, followed by a post-hoc analysis using Dunn's test with Bonferroni correction. The effects of the environmental and climatic variables on the Culicoides abundance were analysed using a general linear model (GLM) of analysis of variance (ANOVA) using a quasi-poisson distribution. The explanatory variables were: presence of rain, temperature (minimum and maximum), presence of horses, and trap position (indoors or outdoors).

Culicoides fauna

A total of 2,181 individuals from 14 species (C. obsoletus / C. scoticus, C. circumscriptus, C. nubeculosus, C. punctatus, C. festivipennis, C. pulicaris, C. riethi, C. parroti, C. lupicaris, C. dewulfi, C. brunnicans, C. flavipulicaris, and C. picturatus) were identified in this study. We considered C. lupicaris as a distinct species, despite its current acceptance as a synonym of C. delta, as evidence supports that these two are indeed valid and distinct species (28). The species of the Obsoletus complex, C. obsoletus and C. scoticus, were the predominant species in the study area (1,272 individuals; 58.3%). Following these, C. circumscriptus and C. nubeculosus were the second and third most common species (12.1% and 11.5%, respectively). C. punctatus (5.6%), C. festivipennis (3.8%), C. pulicaris (2.3%), C. riethi (2.3%), and C. parroti (2.2%) were less abundant. The remaining species (C. lupicaris, C. dewulfi, C. brunnicans, C. flavipulicaris, and C. picturatus) represented only 1.4% of captures (Table 2 and Table 3). A small number of specimens (0.6%) could not be identified due to degradation, and the parity of some females could not be determined (2%). As expected, females (N = 2,017; 92.5%) were more abundant than males (N = 164; 7.5%) across all species and capture sites (Table 2 and Table 3). Indeed, OVI traps are known to preferentially capture host-seeking females (21).

Table 2

*Number and relative abundance (%) of* Culicoides *species in the study area. The details of the captures by traps are summarized in* Table 3
Species	Total	Females	Males	Percentage (%)^a
C. obsoletus / C. scoticus	1272	1256	16	58.3
C. circumscriptus	263	235	28	12.1
C. nubeculosus	250	250	0	11.5
C. punctatus	123	106	17	5.6
C. festivipennis	82	65	17	3.8
C. pulicaris	51	51	0	2.3
C. riethi	50	6	44	2.3
C. parroti	49	31	18	2.2
C. lupicaris	17	13	4	0.8
C. dewulfi	9	0	9	0.4
C. brunnicans	2	1	1	0.1
C. flavipulicaris	2	2	0	0.1
C. picturatus	1	1	0	< 0.1
Culicoides sp.	10	0	10	0.6
Total	2181	2017	164	100
^a Relative abundance: (nx / N) * 100, where nx is the number of individuals belonging to species x and N is the total number of sampled individuals.

Table 3

*Number and relative abundance (%) of* Culicoides *species by trapping site.*
Trapping site	A				B				C				Overall total
Species	Total	Femelle	Male	Percentage (%)^a	Total	Femelle	Male	Percentage (%)^a	Total	Femelle	Male	Percentage (%)^a	Overall total
C. obsoletus / C. scoticus	592	577	15	77.8	138	137	1	45.8	542	542	0	48.4	1272
C. circumscriptus	30	30	0	3.9	92	81	11	30.6	141	124	17	12.6	263
C. nubeculosus	1	1	0	0.1	1	1	0	0.3	248	248	0	22.2	250
C. punctatus	54	54	0	7.1	35	35	0	11.6	34	17	17	3.0	123
C. festivipennis	36	36	0	4.7	22	17	5	7.3	24	12	12	2.1	82
C. pulicaris	17	17	0	2.2	2	2	0	0.7	32	32	0	2.9	51
C. riethi	9	0	9	1.2	6	6	0	2.0	35	0	35	3.1	50
C. parroti	1	0	1	0.1	5	5	0	1.7	43	26	17	3.8	49
C. lupicaris	0	0	0	0.0	0	0	0	0	17	13	4	1.5	17
C. dewulfi	9	0	9	1.2	0	0	0	0	0	0	0	0	9
C. brunnicans	0	0	0	0	0	0	0	0	2	1	1	0.2	2
C. flavipulicaris	2	2	0	0.3	0	0	0	0	0	0	0	0	2
C. picturatus	1	1	0	0.1	0	0	0	0	0	0	0	0	1
Culicoides sp.	9	0	9	1.2	0	0	0	0	1	0	1	0.1	10
Total	761	718	43	100	301	284	17	100	1119	1015	104	100	2181
^a Relative abundance: (nx / N) * 100, where nx is the number of individuals belonging to species x and N is the total number of sampled individuals.

Influence of trapping sites and climatic conditions

Thunderstorms (June 24th and 30th ) and heavy rains (July 23rd ) negatively impacted insect capture at the three trapping sites. Additionally, a malfunction of the black light neon prevented captures in trap A on June 30th.

For the number of Culicoides captured, all species combined, differences between traps were slightly not significant (p = 0.054). Similarly not significant differences were observed for C. brunnicans, C. circumscriptus, C. dewulfi, C. festivipennis, C. flavipulicaris, C. obsoletus / C. scoticus, C. parroti, C. picturatus, C. pulicaris, C. punctatus and C. riethi (all p-value > 0.05) between traps. However, two species C. lupicaris (p = 0.01) and C. nubeculosus (p = 0.013) were captured in higher abundance in trap C than in traps A and B. All the species present at capture site B were also found in capture site A. Nevertheless, C. flavipulicaris (N = 2), C. picturatus (N = 1) and C. dewulfi (N = 9) were only recorded in trap A. The number of Culicoides captured did not significantly differ by capture date throughout the risk period for any species (all p-value > 0.01).

Regarding the impact of climatic conditions, analyses were not performed for C. lupicaris, C. dewulfi, C. brunnicans, C. flavipulicaris, and C. picturatus due to the low number of individuals captured (Table 3). The ANOVA showed a significant influence on the abundance of meteorological (presence of rain, minimum and maximum temperature) and environmental factors (presence of horses and trap position) for three species: C. circumscriptus, C. nubeculosus, and C. parroti (Table 4). These species were mainly captured in trap C, which was located outside near the paddocks and the river. Furthermore, individuals were captured in trap A (indoor trap) when there was a medium-speed wind (average of 15 km/h, Beaufort scale 3/12), but a decrease in captures was observed in each trap when winds were strong (average > 20 km/h, Beaufort scale 4/12).

Table 4

Detailed p-values obtained
Variables	Rain	T max	T min	Horse presence	Trap position
C. obsoletus / C. scoticus	0.979	0.133	0.928	0.06	0.881
C. circumscriptus	< 0.001 ***	< 0.001 ***	0.156	0.811	< 0.001 ***
C. nubeculosus	0.707	< 0.01 **	< 0.01 **	< 0.001 ***	< 0.001 ***
C. punctatus	0.224	< 0.05 *	0.135	0.676	0.442
C. festivipennis	0.094	0.09	0.893	0.672	0.605
C. pulicaris	0.134	0.925	0.337	< 0.05 *	0.414
C. riethi	0.265	0.81	0.171	0.322	0.251
C. parroti	< 0.05 *	< 0.01 **	0.868	0.055	< 0.001 ***

Parity rate

The low parity rate (53.5%) reflects a relatively young population. We observed a peak of nulliparity on July 8th, indicating an emergence of Culicoides. Breeding sites were likely located close to the traps. No significant differences in parity were found between traps (p = 0.19) or between dates (p = 0.11).

Recurrent horse dermatitis remains a significant health concern affecting a considerable number of horses. This study highlights the Culicoides species potentially responsible for this condition in southwest France and offers key recommendations to protect horses from these insects.

Culicoides fauna

A mere 7.5% of Culicoides males were captured, consistent with prior studies (23, 29). OVI traps, being attractive to nocturnal females seeking blood meals, did not capture diurnal Culicoides. The observed wave of nulliparity on July 8th suggests the proximity of larval sites, as adult dispersal is limited, with most individuals found near breeding sites (30). In Europe, Culicoides larvae are often found in muddy areas on farms, rich in organic matter and trampled by animals (9). During the study period, few species' abundances were influenced by climatic and environmental fluctuations, except for the negative impacts of strong winds and heavy rainfall, as commonly observed (31).

Species like C. obsoletus and C. scoticus, belonging to the Obsoletus complex, are predominant in France, particularly in temperate zones (19, 32). These species exhibit a wide host spectrum and thrive in the favourable climatic conditions of the region. Although their abundance was not significantly influenced by the presence of horses in our study, other research has shown their tendency to enter livestock buildings, especially in the presence of animals or during unfavorable weather conditions (4, 33).

In contrast to the national Culicoides surveillance network's findings of low abundance (2), C. circumscriptus, C. nubeculosus, C. festivipennis, and C. punctatus showed higher abundance levels in our study. These variations could be explained by differences in nearby hosts, as the surveillance network primarily targeted ruminant farms. Notably, C. circumscriptus, C. punctatus and C. festivipennis are known to feed frequently on birds (34). These species were particularly abundant in the outdoor trap near the forest, possibly due to the presence of bird nests in the vicinity. Culicoides nubeculosus, accounting for 11.5% of total captures, emerged as the fourth most frequent species. Surprisingly, only one individual was captured indoors during our study. This contrasts with its known preference for horses (35) and its higher abundance in other country (36). The discrepancy could be attributed to favourable climatic conditions and behavioral responses to weather. This species is also a potential vector for Onchocerca cervicalis. Given the similarities between Onchocerca infections and summer itch symptoms, and the few studies which investigated the prevalence in vectors, further research on parasite prevalence should be added in future studies.

Although commonly the second most frequent species around horses in the Netherlands, C. pulicaris ranked seventh in our study, aligning with previous estimates of around 5% of captures [5]. Despite its lower abundance, C. pulicaris remains a species of concern due to its feeding preferences (horses and farm animals) and activity period in the South-East of France from April to September [6].

Culicoides brunnicans and C. dewulfi were captured in low numbers (2 and 9 individuals, respectively). Their biting behavior, exophagy for C. brunnicans and endophagy for C. dewulfi, might explain their low capture rates (33).

Finally, C. newsteadi, observed abundantly by the national surveillance network (10% of the capture) (2), was not collected during our study. This discrepancy could be attributed to differences in feeding preferences and habitat preferences, with C. newsteadi primarily feeding on cattle, sheep, and humans, and being more prevalent in coastal areas at lower altitudes (34, 37).

Risk and recommendations

Our study underscores the potential exposure of horses to various Culicoides species, indicating the risk of sweet itch in susceptible horses. Among the identified species, C. obsoletus / C. scoticus, C. pulicaris, C. nubeculosus, C. lupicaris, C. punctatus, and C. circumscriptus are known to be responsible for insect bite hypersensitivity in horses (14, 38–42). However, the impact of species like C. punctatus, C. pulicaris, and C. lupicaris might be minor, given their low capture percentages (5.6%, 2.3%, and 0.8%, respectively).

The basic recommendation to protect horses from Culicoides hypersensitivity is stabling horses from late afternoon until the next day. While this may be effective for species like C. nubeculosus, predominantly found outdoors, it might not be sufficient for species like C. obsoletus / C. scoticus and C. circumscriptus, which were found in large quantities indoors as previously reported in cattle farms (43). Additionally, as temperatures decrease, an increase in the number of individuals captured indoors was observed. Therefore, effective implementation of this recommendation requires ensuring no open doors or windows and using tightly-fitted mosquito nets (44, 45). Given horses' susceptibility to heat stress (46), installing light traps and vertical, high-speed fans, opposite the entrances in stables could be considered (45). Moreover, horses affected by sweet itch could be covered with anti-insect blankets impregnated with repellents like deltamethrin or permethrin. To avoid the creation of breeding sites for Culicoides, it is necessary to ensure general hygiene. Ideally, manure should be removed twice a day from the stalls and paddocks. Stagnant water, leaking irrigation pipes, overflowing troughs and wet areas should be eliminated.

Our study highlights the potential risk of sweet itch in susceptible horses due to exposure to various Culicoides species. Identified species such as C. obsoletus / C. scoticus, C. pulicaris, C. nubeculosus, C. lupicaris, C. punctatus, and C. circumscriptus are known to be common causes of insect bite hypersensitivity. However, the impact of species like C. punctatus, C. pulicaris, and C. lupicaris may be minor, given their low capture percentages. Our findings emphasize the importance of implementing protective measures such as stabling horses and using anti-insect blankets, particularly against prevalent indoor species. Effective control strategies require continuous surveillance and further research to better manage this persistent health concern affecting horses.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that there is no conflict of interest.

Funding

This work was realized with the financial support of École Nationale Vétérinaire de Toulouse.

Author contributions

C.B. realized the field work. C.B and J.P. analyzed the data and wrote the manuscript with the support of E.B., I.R., C.G. and E.L. Finally, C.B, E.B., I.R., C.G., E.L. and J.P. read, amended and approved the final version of the manuscript.

Acknowledgment

The authors wish to thank Pr Séverine Boullier, supervisor of the veterinary school equestrian centre.

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Local investigation into the role of Culicoides species diversity (Diptera: Ceratopogonidae) in recurrent horse dermatitis cases in southwest France

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Version 1

Abstract

Background

Methods

Study sites

Specimen collection and identification

Statistical analyses

Results

Culicoides fauna

Influence of trapping sites and climatic conditions

Parity rate

Discussion

Culicoides fauna

Risk and recommendations

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1