Diseases

Poultry Red Mite

Download as PDF Download as XLS Download summary

Chapter select

Control Tools

  • Diagnostics availability

  • Commercial diagnostic kits available worldwide

    Traps exist and work, some commercially available (e.g. red mite trap https://www.avivet.nl/en/red-mite-trap-2/; and automated mite counter https://www.hotraco-agri.com/en/news/1565358412/hotraco-agri-presents-mitealert

    Measuring can be done also with simple visual scoring methods. There are various types of mite-trap which can be used to monitor populations. These rely on regular checking for presence of live mites and some companies offer a counting service.

    GAP :

    Products available but most diagnosis is simple, by visual inspection of shed furniture (undersides of feeding troughs etc). Some potential for environmental sampling methods to assess scale of infestation.

  • Commercial diagnostic kits available in Europe

    Traps exist and work, some commercially available (e.g. red mite trap https://www.avivet.nl/en/red-mite-trap-2/; and automated mite counter https://www.hotraco-agri.com/en/news/1565358412/hotraco-agri-presents-mitealert

    Measuring can be done also with simple visual scoring methods. There are various types of mite-trap which can be used to monitor populations. These rely on regular checking for presence of live mites and some companies offer a counting service.

    GAP :

    Products available but most diagnosis is simple, by visual inspection of shed furniture (undersides of feeding troughs etc). Some potential for environmental sampling methods to assess scale of infestation.

  • Commercial potential for diagnostic kits in Europe

    Limited: If cost would be higher than existing visual systems or traps, limited commercial potential.

    GAP :

    It is conceivable that mite traps could be replaced with an electronic detection system which would allow continuous monitoring (Mul et al., 2015 now commercially available; https://www.hotraco-agri.com/en/news/1565358412/hotraco-agri-presents-mitealert). While it is conceivable that tests done on the hens could identify a serological response (antibody or acute phase protein as in Kaab et al., 2019) it is very unlikely that this would provide benefits over mite trapping.

  • DIVA tests required and/or available

    Not required until vaccine available.

    GAP :

    Unlikely to be required even after vaccine becomes available as serological testing is unlikely as a diagnostic procedure.

  • Opportunities for new developments

    Any improvement that is more cost effective and with better specificity will be useful: A recent (unpublished as yet) study describes the sampling of airborne particles sampled from poultry farms using a specific cyclonic biosampler followed by detection (and/or /measurement of abundance) of DNA fragments from D. gallinae (18S or 16S rRNA coding genes) by Illumina sequencing which correlated to mites numbers found in both manure and from traps.

    GAP :

    The method suggested might be an opportunity to effectively monitor mite numbers before triggering a treatment threshold though it is not currently adapted to routine use (only research use to date).

  • Vaccines availability

  • Commercial vaccines availability (globally)

    None. An experimental autogenous vaccine based on soluble mite extract has demonstrated some efficacy (reduction in mite populations by >75%) in an experimental setting but is not suitable for large-scale commercial production (Bartley et al., 2017).

    GAP :

    Vaccines are likely to have an important niche in future red mite control but none are yet sufficiently advanced to be commercialised. The two largest areas of growth in the development of novel interventions for poultry red mite control have been in the development of vaccines (13 published papers since 2007) and novel acaricides/novel uses for existing acaricides (41 published papers since 2007). This reflects the importance of these areas but we lack basic knowledge on how effective vaccines need to be (modelling work required) and the most effective recombinant antigens to employ. The recent publication of the genome (Burgess et al., 2018), development of RNAi (Nisbet et al., in prep) and novel on-hen methodologies for rapidly screening vaccine candidates (Nunn et al., 2019) should accelerate this process.

  • Commercial vaccines authorised in Europe

    None. An experimental autogenous vaccine based on soluble mite extract has demonstrated some efficacy (reduction in mite populations by >75%) in an experimental setting but is not suitable for large-scale commercial production (Bartley et al., 2017).

    GAP :

    yet sufficiently advanced to be commercialised. The two largest areas of growth in the development of novel interventions for poultry red mite control have been in the development of vaccines (13 published papers since 2007) and novel acaricides/novel uses for existing acaricides (41 published papers since 2007). This reflects the importance of these areas but we lack basic knowledge on how effective vaccines need to be (modelling work required) and the most effective recombinant antigens to employ. The recent publication of the genome (Burgess et al., 2018), development of RNAi (Nisbet et al., in prep) and novel on-hen methodologies for rapidly screening vaccine candidates (Nunn et al., 2019) should accelerate this process.

  • Marker vaccines available worldwide

    None.

    GAP :

    Effective vaccine required before considering marker vaccine.

  • Marker vaccines authorised in Europe

    None.

    GAP :

    Effective vaccine required before considering marker vaccine.

  • Effectiveness of vaccines / Main shortcomings of current vaccines

    Current autogenous vaccine requires large quantities of mites from same premises as infestation for its formulation. Has shown field efficacy but much more testing required. May be insufficiently effective under field conditions to provide practical control – requires individual injection and would require long-term immunity. Severity of mite challenge is seasonal in the warmer months, but hens are placed all year around – this makes it difficult to achieve uniform immunity. The most effective vaccines to date are composed of crude antigens produced from collected mites. This is unlikely to be a practical option for commercial vaccines.

    GAP :

    Opportunities for development of effective recombinant vaccines/DNA vaccines with long lasting immunological cover in appropriate adjuvants/delivery systems.

  • Commercial potential for vaccines in Europe

    Very high, particularly for recombinant/DNA vaccines. If a high degree of immunity is established and maintained then it might be possible to prevent parasite build-up and reduce the need for acaricides.

    GAP :

    Opportunities/gaps in knowledge surrounding antigen identification, adjuvant, level of protection required.

  • Regulatory and/or policy challenges to approval

    For recombinant or DNA vaccines the regulatory and policy challenges are no greater than for any other recombinant vaccine and there are multiple precedents. While autogenous vaccines can be used, they are mainly used for bacterial and viral pathogens for which it is easier to ensure that the seed material is free of pathogens or the product is sterile. While autogenous vaccines can be used, they are mainly used for bacterial and viral pathogens for which it is easier to ensure that the seed material is free of pathogens or the product is sterile.

    GAP :

    Regulatory authorities well versed in registration of recombinant vaccines and viral-vectored vaccines in target species.

  • Commercial feasibility (e.g manufacturing)

    For recombinant or DNA vaccines, highly feasible, all major manufacturers have capacity to produce. Commercial feasibility of autogenous vaccine relatively low because of antigen supply method and manufacturing requirements.

    GAP :

    If multiple recombinant antigens require to be incorporated to bring about adequate control. This might present challenges in cost of goods to manufacture. Important that correct antigens/mix of antigens is identified and manufacturers consulted about what upper limits of antigen numbers in any cocktail may be.

  • Opportunity for barrier protection

    Our understanding of “Barrier protection” would suggest that all birds in a flock should be vaccinated to prevent disease ingress.

    GAP :

    Knowledge of how different vaccination regimens affects parasite population build-up is lacking; opportunity for modelling and also practical studies once effective vaccine is developed.

  • Opportunity for new developments

    Opportunities for Reverse Vaccinology approach now possible with the recent publication of the genome (Burgess et al., 2018), development of optimised RNAi (Kamau et al., 2013; Price et al., in prep), adjuvant optimisation (Price et al., 2019) and novel on-hen methodologies for rapidly screening vaccine candidates at low cost (Nunn et al., 2019) should accelerate this process. One key element will be the potential for a booster vaccination during the egg-laying cycle – this cannot be done by injection so technology (mists/oral delivery etc) needs to be exploited to deliver booster vaccinations.

    GAP :

    Majority of tools are now in place for a rational reverse vaccinology approach and, to some extent, this has begun (see Lima-Barbero et al., 2019) but opportunities exist for acceleration of process by in silico and in vitro analyses.

  • Pharmaceutical availability

  • Current therapy (curative and preventive)

    Treatments

    Most acaricides on the market are regulated under COPR (pesticide) regulations and are registered as biocides. Most are not for direct application to birds so the number of authorised treatment options is quite limited. There are sprayed pesticides for application to the premises and one oral acaricide, supplied through the drinking water and licensed as a veterinary medicine (fluralaner). Efficacy of the latter is high currently. Efficacy of the sprayed chemical treatments is variable and dependent on multiple factors including operator skill level and existence of resistant mite populations.

    Authorized veterinary drugs: a sprayed organophosphate (Phoxim), an orally-administered isooxazoline (Fluralaner).Authorized pesticide: a sprayed spinosyn (Spinosad)

    Prevention tools (some also used as treatments)

    Biological control agents: Release of mass-reared predatory mites.Substances of “natural” origin: Plant-based feed or drink additives; sprayed silica dust, plant-based products.Standard hygiene measures: on farm and biosecurity through introduction of animals and materials “free of PRM” asked by farmers to the suppliers (e.g. layers, egg trays, containers)Mechanical action: Use of detergent and water to clean hen houses and equipment.Physical action: Physical barrier systems (adhesive strips for example) are used in small-scale set-ups. Other commercially-available prevention systems involve modified perches with electric wires running underneath to exterminate host-seeking mites. Elevation and sustained high (45℃) temperature during the empty period has been used. In industry there are a range of remedies available, some of which are claimed to work mainly or entirely by physical mechanisms. They can be very effective in delaying parasite build-up, particularly where well applied to clean, empty housing and equipment (e.g. Recommended national (Norway) protocol for heat/chemical sanitationhttps://www.animalia.no/contentassets/6c47d07128674c4784b418d02e1aad80/rad-om-sanering-med-varmebehandling-og-sproyting.pdf). Other physical interventions include traps, for example: https://patents.justia.com/patent/9572337.

    GAPS :

    Potential for International standardisation of sanitation/treatment methodologies and adoption of Integrated pest management strategies (IPM) for different housing systems rather than reliance on single (pesticide) approach. A current IPM strategy is available in Dutch and also in English from 2020) but more IPM tools are necessary (e.g. frequent removal of manure to suppress populations; entomopathogenic fungi e.g. Wang et al., 2019; repellents/attractants for “push-pull strategy”).

    Consideration should be given to the ecosystem scale instead of just the host-parasite axis. Dermanyssus gallinae mostly spends life off of the poultry host, in hard-to-reach parts of the shed, making sprayed acaricidal products unsatisfactory in many cases and potentially impacting on predatory species. In addition, poultry manure is commonly spread on crops and, depending on the toxicity of the residues left by the treatments (especially oral treatments) in the droppings, treatments in livestock buildings could have an environmental impact but knowledge around this is currently lacking.

    A single product is currently potent (Fluralaner), with resistance reported against phoxim (Pugliese et al., 2019) as well as other frequently-used acaricides (Thomas et al., 2018). This represents an issue for when resistance develops to fluralaner; opportunities exist for development of novel actives to extend the lifespan of Fluralaner and in the analysis of resistance threat/emergence against fluralaner for which we don’t currently have sufficient knowledge.

    Because of the biological habits of D. gallinae, oral therapeutics are highly desirable – further compounds/products with this delivery method would be highly sought after but status of development pipeline is unknown outside of pharmaceutical companies.

  • Future therapy

    • Oral application only one product currently, more would be helpful to increase competition as price for product may be a constraint and only one molecule available increases risk for high pressure on resistance development. Environmentally-applied products less likely to be successful due to difficult application.
    • More Integrated Pest Management (IPM) tools are necessary (e.g. predators; entomopathogenic fungi e.g. Wang et al., 2019)
    • Increased focus on monitoring and prevention – may current tools used in a reactive way when mite populations are high.
    • Hot spot treatment
    • Use of environmental friendly treatments
    • Management tools to suppress population growth
    • Some work has been done on essential oils and feed composition with a view to achieve a repellent effect after oral administration ( e.g. El Adouzi et al., 2019).

    GAPS :

    Five main emerging gaps/opportunities around future therapies :

    • Systemic acaricides with extended efficacy without impacting consumer and environmental safety.
    • Effects on ecosystem of existing treatment unknown.
    • Spatio-temporal population dynamics of the mite in response to climate (weather and in-house) and treatments in different housing systems.
    • Refine our understanding of the factors that affect the mite-bird chemical interactions in such a way as to have more efficient repellent and/or “attract and kill” tools.
    • Further development of IPM tools and how they can be integrated with current and emerging therapies to bring about sustainable control.
  • Commercial potential for pharmaceuticals in Europe

    Very High - One of most important control approaches in the poultry industry worldwide.

    GAP :

    The vaccines and the plant products may never replace the pharmaceuticals. There may always be a potential for the pharmaceuticals and their use in IPM systems needs to be evaluated alongside other treatment/prevention opportunities.There is potential for effective natural compounds for organic production.

  • Regulatory and/or policy challenges to approval

    The registration process in Europe, at least, is highly regulated. It addresses all aspects of a product (quality; animal, consumer, user and environmental safety; efficacy). Thus, addressing all aspects including ecotoxicity, residues in eggs, target animal safety, withdrawal period after use (especially orally-delivered actives), results in expense and long approval times.

    Novel “green” products are often not protected by patents and thus producers do not pay for high approval costs.

    Several mechanical means (especially the introduction of soapy water or grease into the mite’s preferred microhabitats) are potentially of interest and may have local efficacy. However, regulation and approval of these is out of scope for pesticide or veterinary drug approval.

    GAPS :

    Currently available products, as mentioned in their product specifications, are either persistent in the soil, affect fishes and aquatic invertebrates and some have long term consequences. To avoid long term consequences products should be developed which are more specific to poultry red mite and ideally do not affect the aquatic life.

    Potential to initiate the creation for animal production of a category similar to the “Natural preparations of low concern” (NPLC) regulatory category in crop protection. This would not only regulate practices but also ensure that a minimum level of evidence of effectiveness is required.

    There are more and more products claimed to be of "natural origin" for use against red mites, without belonging to any categories, whose effect has not been demonstrated at all. The NPLC category could make it possible to identify uses of substances of low concern and for which substantial experience reasonably suggests that it is at least somewhat effective (long-standing use, with satisfied, long-standing returns). Indeed, these companies in general cannot pay for very advanced experiments, but this at least makes it possible not to eliminate useful and healthy practices while limiting “charlatan” products.

    No legal “green“ products or methods/ environmental friendly products are available. Current EU regulations highly restrict the approval of new products, induce high approval costs and take a long time until obtaining an approval. In order to get more “green” products (for example, those for which it may not be possible to establish intellectual property protection through a patent) in the toolboxes for control of pests, new EU regulation should be adopted. This regulation is not specific to Poultry red mite, affecting all pests in agriculture.

  • Commercial feasibility (e.g manufacturing)

    Manufacturing of pharmaceuticals is generally not the major concern as long as the manufacturing price is compatible with the market.Use of predators/entomopathogenic fungi etc and “green” products are necessary but registration studies are costly.

    GAP :

    Cost/benefit analyses of many emerging products for IPM not yet investigated.

  • Opportunities for new developments

    Further systemic acaricides (registered as a veterinary medicine) with high efficacy, specificity for the parasite and biological and ecological safety.

    Opportunities for identifying novel targets with the recent publication of the genome (Burgess et al., 2018) and development of optimised RNAi (Kamau et al., 2013; Price et al., in prep), and in vitro and in vivo testing (e.g. see Thomas et al., 2018; Nunn et al., 2019).

    Some further novel ideas emerging: https://www.wur.nl/upload_mm/7/5/e/9a7c8a07-10aa-4514-b61d-97d71f7aa2e9_4-8%20Design%20approach%20meeting%20summary.pdf

    GAP :

    Requirement for further classes of actives to help combat resistance and prolong lifespan of current actives.

  • New developments for diagnostic tests

  • Requirements for diagnostics development

    Current tools adequate but assessment of economic loss not easy with current tools.Improved monitoring traps with enhanced attractiveness (perhaps with pheromones, allowing automated monitoring, and cheap enough to deploy sufficient numbers to detect localised infestations early.

    GAPS :

    Correlation between mite trap count number and economic threshold for intervention requires to be delineated.

    Opportunities in development of enhanced traps: identification of aggregation signals/pheromones (some progress already in this area)

    Opportunities around airborne sampling of DNA and it’s quantification as a proxy of mite number (see section 1.7 above) – knowledge gaps: Need to decide which genomic region and which primer pair works best and need to optimize the sampling process and select the best and simplest device. Also a need to standardize the bioinformatic pipeline. May only prove feasible for very big companies due to software and laboratory expenses.

  • Time to develop new or improved diagnostics

    2-3 years dependent upon technology.

    GAP :

    Collaboration potential with commercial diagnostic manufacturer is an unknown – potential return on investment for diagnostic developer/manufacturer unknown.

  • Cost of developing new or improved diagnostics and their validation

    Not known, technology-dependent.

    GAP :

    Opportunities around developing knowledge on cost of development of diagnostic and economic justification for a developer/manufacturer to engage in process.

  • Research requirements for new or improved diagnostics

    Animal stress monitoring with correlation to mite numbers etc. development of further molecular tools.

    Medium-duration experimental trials to refine the DNA quantitation method and improve the protocol and devices to make the use of biosamplers and samples in farm and from farms to lab relevant and easy.

  • Technology to determine virus freedom in animals

    Layers are reared on dedicated rearing sites and moved at 16 weeks to dedicated laying sites. Pullet producers would also benefit from ‘early warning’ automated monitoring traps, or any other approach they could use to document good red mite control (if not mite-freedom) in the pullets produced.

    GAP :

    Requirement for technologies to give “early warning” in rearing sites and after transfer to egg-laying facilities.

  • New developments for vaccines

  • Requirements for vaccines development / main characteristics for improved vaccines

    Easy to apply and ideally cost of 20€ per 1000 birds maximum.

    Ideally inducing high mortality in proto- and deutonymphs and adults after a single feed, achieving 70+ weeks of control after a single application. If it could be applied orally and in lay then repeated administration would be a possibility.

    Potential for limiting population expansion by affecting fecundity as well as inducing mortality.

    See draft target product profile from PARAGONE project (https://www.paragoneh2020.eu/).

    Target Product Profile: Dermanyssus gallinae

    Active ingredient and delivery mechanism

    Adjuvanted, multi-component vaccine, for protection of laying hens against D. gallinae. Comprises no more than 3 recombinant proteins, but ideally 2 or less proteins.

    For protection of hens during rearing and laying.

    Pharmaceutical form

    Ready-to-use solution for injection. Stable for at least 12 months at 2-8°C.

    Dose and administrationfrequency

    Hens: Ideally single vaccination of 0.1ml at 12 weeks of age, or two vaccinations, 5 weeks apart, from 12 weeks of age is permissible.

    Safety

    Safe in hens from 12 weeks of age.Minor or no local vaccination-site reactions.

    Efficacy: duration of immunity and activity

    Onset of Immunity in naïve hens from 2 weeks post second vaccinationDuration of Immunity ≥ 12 months to cover the entire laying cycle

    Label claim

    A vaccine to aid in the reduction D. gallinae during hen’s laying period

    Packaging

    100ml and 250ml in bottle or pouch suitable for vaccine gun.Recycled cardboard packaging, Storage 2-8°C, shelf-life at least 12 months.

    Geographical target(s)

    Worldwide

    Species and age range

    Laying hens (all breeds) from 12 weeks of age

    Limitations of use

    Recombinant approach may not be compatible with organic systems

    Other product synergies

    Multiple viral and bacterial vaccines administered prior to egg laying in hens. Acaricidal treatments during shed preparation and any licensed “in lay” treatments

    GAPS :

    Analysis of cost of goods/potential profitability of vaccines currently lacking.

    Optimum antigen constituents not yet known

    Modelling of different vaccine efficacies/modes of action on population development not yet done.

    Opportunities exist in all above areas for underpinning vaccine development and engagement of commercial partners.

  • Time to develop new or improved vaccines

    Minimum 5 years.

    GAP :

    Gaps exist in funding mechanism for all three elements highlighted in 5.1 to drive vaccine development to a point where it is attractive for commercial exploitation.

  • Cost of developing new or improved vaccines and their validation

    €1-10M.

    GAP :

    Gaps in knowledge about cost of vaccine development.

  • Research requirements for new or improved vaccines

    Early stage processes – optimal antigen discovery; antigen formulation prior to commercial engagement.

    Investigation of potential for a booster vaccination during the egg-laying cycle – this cannot be done by injection so technology (mists/oral delivery etc) needs to be exploited to deliver booster vaccinations and/or long-lasting immunity.

    GAP :

    Gaps in funding for early-stage vaccine development. We now have most of the tools we need but funding required for early phase development.

  • New developments for pharmaceuticals

  • Requirements for pharmaceuticals development

    Low cost for high volume use.Specific for parasite.Novel classes of actives to combat emerging resistance to current classes.Satisfactory performance for regulatory requirements:Veterinary medicine:- Dossier on Chemistry, Manufacturing and Controls- Dossier on safety (target animal, consumer, user, environment)- Dossier on efficacy (pharmacokinetics, pharmacodynamics, dose justification and field studies).

    GAPS :

    Spraying acaricidal products is largely inefficient. Two constraints can be considered simultaneously = (1°) reaching the target pest with accuracy and selectivity (one successful product is fluralaner, via the blood meal) (2°) minimise residues in the manure (and/or check for innocuity of them to soil fauna, plants, micro-organisms). The latter is an important though totally neglected issue to date in poultry. Manure spreading is one of the most recommended way to mitigate the Human impact on environment due to agriculture. European regulation started to take this major issue with residues of antiparasitic products in large mammals (cows, horses…). However, to date, nothing is required about this with poultry, though poultry manure is recognized a very good organic fertilizer.

    Promotion of the development of products that are acting via oral administration AND that do not make subsequent manure deleterious to biodiversity.

  • Time to develop new or improved pharmaceuticals

    Known molecule: 5-7 years.New molecule: 8-10 years.

    GAPS :

    Improved high throughput screening systems.

    New compound libraries.

    Improved in vivo screening abilities (see Nunn et al., 2019 for recent development) .

  • Cost of developing new or improved pharmaceuticals and their validation

    Several millions EUR.

  • Research requirements for new or improved pharmaceuticals

    Testing methodologies for new natural or synthetic compounds.Testing methodologies for off-target effects.

Disease details

  • Description and characteristics

  • Pathogen

    Dermanyssus gallinae (Acari: Mesostigmata), causes primary disease by itself and can be a vector for a number of pathogens causing secondary diseases.

    Dermanyssus gallinae, a strictly hematophagous mite, behaves as a ‘micropredator’ (instead of a true parasite), as do bedbugs and female mosquitoes. It is a reservoir and/or a vector of some pathogens, just like many ‘micropredators’.Once introduced into farm buildings, it is extremely difficult to manage it. It mostly lives off of the bird host, visiting the host during darkness to feed for short periods (<1h), accumulates in diverse (and numerous) hiding places in farm buildings. Its local distribution is restricted to the farm buildings in close proximity to hens because mites need blood meals to complete their life cycle and to reproduce and are unable to persist on host due to the temperature of the host.

    Dermanyssus gallinae, adults are about 1 mm in size. There are 5 lifestages of which 3 are blood-feeing.

    GAPS :

    Although the general life traits are well known (strict hematophagy, number of developmental stages, duration of the cycle at different temperatures) a number of gaps in our understanding exist:

    Chemical interactions with the host and with the remaining environment.

    Chemical interactions between mites (aggregation and oviposition pheromones) :

    • Interactions with natural enemies, especially naturally-occurring predatory mites, in the farm buildings.
    • Parameters of the temporal dynamics of populations.
    • Factors that affect the spatial distribution (and dynamics) of its populations.
  • Variability of the disease

    Prevalence studies exist for most European countries, Japan, China and molecular epidemiology studies have been published from France, UK, Norway, Sweden, Italy, Turkey, Japan, China, mostly poultry industry focused. (Brannstrøm et al 2008, Roy et al 2011, Øines & Brannstrøm 2011, Marangi et al 2014, Chu 2015). Based on DNA sequences from a few gene regions (Co1, 16S, Tropomyosin intron), its seems that the intraspecific genetic variation is high (huge allelic and haplotypic variation), though quite limited in the population that infests layer farms in Europe and at least Asia, Brazil, Australia (Roy et al. 2010, Roy & Buronfosse 2011, Øines & Brännström 2011, Chu et al. 2015). The general structure of populations of mites is as follows: strongly differentiated populations (a metapopulation pattern), with the strongest differentiation between mites sampled in wild bird nests and in poultry farms (obviously almost no gene flow has occurred between farms and the wild avifauna for a long time).D. gallinae is a species complex, encompassing at least 2 cryptic species: D. gallinae s.s. and D. gallinae L1 (Roy et al. 2009, 2010, Roy & Buronfosse 2011). The former has a wide bird host spectrum and is able to feed on mammals (though it is unclear whether it may complete its life cycle on them). This is the species of economic importance in poultry, and populations of the same species were reported from birds belonging to nine different bird orders. Nevertheless, the populations that develop in poultry farms are strongly isolated from populations in the wild avifauna from a reproductive point of view (Roy & Buronfosse 2011, Øines & Brännström 2011). Dissemination of the species infesting commercial hens is tightly associated with human trade activity. Its main vectors are most likely inert objects such as cages and trucks. The latter species, D. gallinae L1, is associated with pigeons and is also prone to feed on man. This is at least in some cases, (perhaps in most cases), the agent responsible for urban cases of human gamasoidosis.

    GAP :

    Opportunities for more epidemiological surveys in all parts of Europe. Current evidence suggests some differences in how this varies across long/latitudes, and variation of species genetic variants in farms, in wild birds.

  • Stability of the agent/pathogen in the environment

    Stable: wide range of temperatures in which it can survive. Survives a long time without blood and under cold conditions - D. gallinae is able to survive fasting for at least nine months in the environment (without any host available; Nordenfors et al. 1999). A number of individuals die after 3 weeks of fasting, but part of the population persists and nymphs, especially, can survive several months (LR, pers. obs.).Furthermore, the time of submersion into water required to kill 50% of the population is close to 60 hours (LR unpublished data). A hypoxic coma makes mites appear to be dead, however, they recover well after a few hours out of water.

    GAP :

    Effect of low relative humidity is unknown; More experiments required on survival; starved, fed, cold/hot.

  • Species involved

  • Animal infected/carrier/disease

    Main animal infected is the domestic hen (especially commercial layer hens). The disease manifests as anaemia, an increase in irritation and restlessness, feather-pecking, cannibalism and hen mortality. Poultry red mites have also been implicated as potential reservoirs for a number of commercially-important and zoonotic diseases and can feed opportunistically on mammals, including humans.

    Main carriers are inert objects rather than host animals: The body temperature of birds, and maybe also of mammals, is highly uncomfortable to the mite. Birds are poor long-distance carriers (meters).

    The host spectrum of the species is wide (mainly birds), but transfer between wild and domestic birds is rare if not absent.

    GAP :

    Further exploring the routes of mite spread would be most valuable. Using molecular tools including population genetics studies and NGS in an epidemiological framework could help tracing the routes and subsequently develop effective prophylactic strategies.

  • Human infected/disease

    The cryptic species D. gallinae L1 is able to bite man causing human gamasoidosis (see Pezzi et al. 2017). Many gamasoidoses are reported in urban contexts (see Cafiero et al. 2019) mainly caused by D. gallinae L1 coming from synanthropic birds.

    GAP :

    The respective contribution of D. gallinae ss and D. gallinae L1 to human gamasidoises is largely unknown. An epidemiological study would be valuable to better understand the human pathologies and aetiology. Studies to evaluate the effects of occupational exposure of poultry workers would also be valuable.

  • Vector cyclical/non-cyclical

    Some sporadic information of individual pathogens, such as Salmonella (Valiente-Moro 2007), Avian Influenza (Sommer et al 2016), Borrelia and Coxiella (Raele et al 2018): Some indication of relevant pathogens present, but additional experiments needed to evaluate true vector capacity.

    GAPS :

    Some indication of relevant pathogens present, but additional experiments needed to evaluate true vector capacity and potential for longevity of survival, multiplication of organisms in mite.

    Role for transmission of E. coli?

  • Reservoir (animal, environment)

    D. gallinae reservoirs exist mainly in the environment in commercial hen houses, transiently on the birds. Reservoirs exist in the environment but populations of D. gallinae infesting commercial species seem to be distinct from those infesting local wild bird populations.

    GAP :

    No major gaps in knowledge.

  • Description of infection & disease in natural hosts

  • Transmissibility

    Highly transmissible on equipment; everything which is moved or moves may transmit D. gallinae.

    GAP :

    Adequate knowledge.

  • Pathogenic life cycle stages

    Three of the five stages (protonymph, deutonymph, adult) bite the host and may simultaneously transmit pathogens to the host.

    GAP :

    Adequate knowledge.

  • Signs/Morbidity

    Restlessness, increased scratching, increased feed intake, increased water intake, thinner egg shell, lower egg weight, feather losses, weight loss, Pale comb, bacterial disease (co-infestation), death in extreme circumstances.

    GAP :

    Adequate knowledge.

  • Incubation period

    Not known.

    GAP :

    Population dynamics under various conditions not fully understood.

  • Mortality

    In severe cases and in combination with other bacterial diseases

    GAP :

    Adequate knowledge.

  • Shedding kinetic patterns

    Not applicable

  • Mechanism of pathogenicity

    Blood loss, physical irritation, transmission of pathogens.

    GAP :

    Knowledge gap in determining the effect of numbers of mites per hen on production and mortality.

  • Zoonotic potential

  • Reported incidence in humans

    Some zoonotic potential and reports of infestations of humans (e.g. see Cafiero et al 2019).

    GAPS :

    Research gaps identified by Cafiero et al., 2019:

    • to carefully describe the symptoms and skin reactions of red mite dermatitis, although they may overlap other diseases;
    • to investigate the development of the lesions and haematological parameters (if any) over time;
    • to investigate the effects of D. gallinae on the human immune and dermal systems;
    • to uncover possible immunological host markers for setting up diagnostic tools.
  • Risk of occurence in humans, populations at risk, specific risk factors

    Gamasoidoses due to D. gallinae have occurred worldwide for some time, though maybe with an increasing frequency recently. Note that besides the underreporting due to physicians commonly ignoring the agent and the agent being very hard to observe, delusionary parasitosis (Ekbom syndrome) may be diagnosed (or misdiagnosed) (Prof. P. Delaunay, pers. comm.). Therefore one should be quite cautious when dealing with this problem in order to reduce underreporting while prevent increasing delusory parasitosis.

    GAP :

    Largely unknown (especially risk factors), opportunity for further research.

  • Symptoms described in humans

    Summarised from Cafiero et al., 2019; Erythematous eruptions consisting of 1–3 mm papules sometimes with a visible central puncture mark or vesicles; urticarioid manifestations have also been described. Bites can be painful and skin lesions may occur in any area of the body, except in the interdigital spaces, genitals or skin folds; itching is commonly intense, with reported cutaneous excoriations due to scratching.

    GAPS :

    Highlighted gaps described by Cafiero et al., 2019:

    • greatly improved awareness of the problem among medical doctors;
    • enhanced knowledge of D. gallinae taxonomy and eco-biological aspects;
    • closer collaboration of doctors with entomologists/acarologists/veterinarians.
  • Likelihood of spread in humans

    The likelihood of spread from the roof to the inside of a house where pigeons are nesting is high. The likelihood of human to human spread is unknown/unlikely.

    GAP :

    Largely unknown, opportunity for further research.

  • Impact on animal welfare and biodiversity

  • Both disease and prevention/control measures related

    Infestations, especially with high mite numbers, result in lower animal welfare; anaemia, death, sleeplessness, weight loss increased injured picking.

    Control measures: Use of diatomeceous earth may result in respiratory problems for hens and poultry workers. Chemical control methods largely reduce the biodiversity in hen house as well as in the environment (via cleaning water and manure) as such products are not selective for D. gallinae only and are highly persistent: The arthropod fauna that live in barn farms was shown to be quite diverse at least in France (Roy et al. 2017) and some of the naturally-occurring mites were shown to be extremely sensitive to deltamethrin (ibid.).

    GAP :

    Since poultry manure is one of the best organic fertilizers, it is commonly spread on crops. Land application of recycled livestock manures is a major route by which veterinary drugs enter the environment (Kaczala and Blum, 2016). Depending on the toxicity of the residues left by the treatments in the droppings, treatments in livestock buildings could well have a dramatic impact on soil biodiversity. To our knowledge, no study has been conducted/published on that issue with poultry manure, although this has been done on large herbivores’ droppings and resulted in regulatory requirements. Therefore, to date, a gap in knowledge exists. We only know that some (the only tested to date) of the mites that develop inside poultry houses are extremely sensitive to a pyrethroid. There is a pressing need for information on the susceptibility to other insecticide molecules that are commonly used in farms not only amongst henhouse-dwelling arthropods, but also amongst coprophilous and soil arthropods.

  • Endangered wild species affected or not (estimation for Europe / worldwide)

    Not known.

    GAP :

    A number of soil animals (insects, collembolans, mites, earth worms) and of pollinators such as domestic and wild bees might be affected (see above). The huge lack of knowledge makes possibly deleterious impact of anti-mite products on important parts of biodiversity unnoticed.

  • Slaughter necessity according to EU rules or other regions

    No.

  • Geographical distribution and spread

  • Current occurence/distribution

    Distribution is currently worldwide, with a quite homogeneous intraspecific genetic structure in poultry farms on different continents resulting from long distance spread via trade activity (see above and Roy et al. 2010, Roy & Buronfosse 2011, Øines & Brännström 2011, Chu et al. 2015). An invasion event was reported in Brazil from mid nineteenth century to early 2000, a period during which the initially indigenous main hematophagous mite in poultry seems to have been gradually replaced by D. gallinae (see Tucci et al. 2008). To date, invasions events appear to have ended in many countries, and infestations in large commercial units seem to have originated in most cases from Europe (consistent with the history of poultry trade at the world scale).

    GAP :

    Gaps in knowledge: There is a perception that Ornithonyssus sylvarium (Northern Fowl Mite) largely displaces D. gallinae as the major commercially-relevant species in North America– is this true and, if so, why?

  • Epizootic/endemic- if epidemic frequency of outbreaks

    Endemic and epizootic; for example in the European context 83% of egg production units report infestation (Flochlay et al 2017).

    GAP :

    Some evidence of impacts of increased summer temperatures on epizootic outbreaks, requires further investigation (see also section “Seasonal cycle”).

  • Seasonality

    In general, generation time reduces during periods of warmth with high relative humidity. According to a pilot study on arthropodofauna in poultry (Roy et al. 2017, + an article under evaluation), some seasonal fluctuation occurs in the population dynamics, in spite of the overall highly regulated farm environment. In France, this seems to be characterized by a decline in late autumn and an increase in winter with a peak in early summer.

    GAP :

    The current knowledge of seasonality is limited; could be refined and completed. International context also could be examined.

  • Speed of spatial spread during an outbreak

    Epizootic unit = henhouse; the latent period usually lasts 2-3 months (from the start of flock), then the intra-henhouse spread may be dramatically fast (ca 15 days to reach highest infestation levels, starting from low levels with almost no mite aggregate visible). The region/country-scale spread is much slower (constrained by slaughter/flock start events).

    GAP :

    Better knowledge of population dynamics (and what influences them) could assist in modelling responses to interventions.

  • Transboundary potential of the disease

    High potential linked to production systems and international trade: Genetically identical D.gallinae are present within the breeding columns of laying hens. Parts of one such column are present in a many countries. There are no boundaries for this pest when material of the egg production column and breeding column are transported all over the world.

    GAP :

    Some studies already performed on transboundary movements, potential for more in different countries with different or new trade routes.

  • Route of Transmission

  • Usual mode of transmission (introduction, means of spread)

    Inert objects such as cages and any object involved in poultry transportation (see above). Everything which is moved could transfer poultry red mite. Amongst others via crates, hens, rodents, flies, dust, transport belts. The role of wild birds is almost non-existent in Europe at least (Roy & Buronfosse 2011, Øines & Brännström 2011).

    GAP :

    Adequate knowledge.

  • Occasional mode of transmission

    Wind and dust.

    GAP :

    Farmers are surprised about new infestations even after they have taken all preventive measures.

  • Conditions that favour spread

    Lack of hygiene measures during transportation.

    GAP :

    Adequate knowledge.

  • Detection and Immune response to infection

  • Mechanism of host response

    Some production of mite-specific serum IgY during infestation (Bartley et al., 2017) and induction of acute phase proteins (Kaab et al., 2019) but unlikely to be protective or useful as a diagnostic.

    GAP :

    The population dynamics of the infestation suggest that any immune response mounted by the host is inadequate to bring about mite control. Some suggestions that after moulting mite population growth reduces but there is currently limited knowledge about this.

  • Immunological basis of diagnosis

    Not applicable.

  • Main means of prevention, detection and control

  • Sanitary measures

    Cleaning with soapy water much more efficient than with pure water (unpublished data). Removal of all soft and hard manure, remove dust and mites with compressed air, thorough cleaning with high pressure cleaning, remove all debris, cleaning with high pressure cleaning, Dry, Disinfect (when done in a very good way; can be effective).

    A homogeneous and very fast rise of the temperature above 45°C during the empty/fallow period (e.g. https://vaneckbv.nl/en/thermokill/thermokill) or just for transport instruments before transportation) can be used because the mite cannot withstand thermal shocks upwards (it can withstand cold shocks rather well on the contrary). This requires infrastructure and energy expenditure that is often inaccessible.

    Ozone treatment in combination with spinosad/phoxim/ Silica/ dusts (see http://www.henhub.eu/wp-content/uploads/2017/09/henhub-tvn-160617-IPM-for-PRM-TOTAL-step-1-to-8-EN_mm06092017.pdf).

    GAP :

    Prevention being better than cure, this is an area where novel interventions could make a big impact – gaps exist for increased research on engineering solutions; hen house design etc.

  • Mechanical and biological control

    See also “Pharmaceutical availability – Current therapy”Daily removal of manure (up to 80% reduction of population).Monthly removal of dust (vacuum cleaning, use of compressed air, brushing).Monthly cleaning (removal of hard dried manure) of protection blades for eggs and aeriation.Application of liquid silica, green soap/ethanol.Plant derived products/ essential oils.Predatory mites.Use of Q-perch.Vacuuming.Rinsing housing equipment with water and soap.

    GAP :

    See “Pharmaceutical availability – Current therapy”

  • Diagnostic tools

    Monitoring methods through traps (see section “Diagnostic availability - Commercial diagnostic kits available in Europe”). Monitoring methods are listed in Mul, 2017.

    GAP :

    see section “Diagnostic availability - Commercial diagnostic kits available in Europe”.

  • Vaccines

    None commercially available, though the use of autogenous vaccine based on soluble mite extract (Bartley et al., 2017) might be useful on small-scale units.

    GAP :

    Multiple gaps/opportunities exist (see sections “Vaccines availability” and “New developments for vaccines”) in both vaccine design and deployment.

  • Therapeutics

    Integration of several treatment approaches: e.g. systemic treatment + spray treatment in the places which are far from the hens + empty manure would be an effective preventative measure but therapeutics options are limited: Authorized veterinary drugs: a sprayed organophosphate (Phoxim), an orally-administered isooxazoline (fluralaner) Authorized pesticide: a sprayed spinosyn (Spinosad). No selective pesticides are available and thus a treatment also kills the natural enemies.

    GAP :

    Key opportunities for development of novel classes/compounds with high efficacy and selectivity.

  • Biosecurity measures effective as a preventive measure

    Standard hygiene measures (known from practice; if you do not take all hygiene measures mites are introduced). As a result of involvement of the whole egg production chain.

    Most important points of introduction of pathogen:New flock of hens ;Containers/crates ;Employees/visitors/poultry farmer ;Egg containers/pallets ;Egg trays ;Pests, Rodents, Flies.

    Pathogen is present in the whole egg production chain.Avoid spread between links of the chain.Most important points of spread of pathogen:Cross belts/ Manure belts ;Egg cross belts/ conveyor belts ;Aeration pipes ;Air mixing box ;Removal of cadavers ;Employees/visitors/poultry farmer ;Pests, Rodents, Flies ;Feeding system through the barn ;Shared materials/ equipment.

    Message:everything moving moves red mites.

    Mul and Koenraadt 2009

  • Border/trade/movement control sufficient for control

    Not present.

    GAP :

    Pathogen is endemic in all egg production areas.

  • Prevention tools

    Consider several measures in parallel: chemical treatment, mechanical measures (e.g. manure, egg tray).

    GAP :

    Gaps in major areas: vaccines; novel therapeutics; integration of IPM

  • Surveillance

    On a local level only (i.e. on-farm): Monitoring tools are present; from fully automated (including models and an advice algorithm) to visual methods and traps requiring a lot of labour.

    GAP :

    See section ”Diagnostics availability”.

  • Past experiences on success (and failures) of prevention, control, eradication in regions outside Europe

    Successful on-farm control can be brought about by the integration of good biosecurity with timely interventions with treatments. No known instances of attempts at eradication (e.g. on a national level).

  • Costs of above measures

    Not expensive in themselves. They just require additional time for the farmer and changes in their processes.

    GAP :

    Cost/benefit analysis of all potential control measures and their integration.

  • Disease information from the WOAH

  • Disease notifiable to the WOAH

    No.

  • WOAH disease card available

    Not available.

  • WOAH Terrestrial Animal Health Code

    Not available.

  • WOAH Terrestrial Manual

    Not available.

  • Socio-economic impact

  • Zoonosis: impact on affected individuals and/or aggregated DALY figures

    Not known.

    GAP :

    Gap in knowledge for socio-economic impact.

  • Zoonosis: cost of treatment and control of the disease in humans

    Not known.

    GAP :

    Gap in knowledge for socio-economic impact.

  • Direct impact (a) on production

    Estimated productivity losses €0.5 - €2.50 per hen in Europe annually.

    GAP :

    Updated impacts per year could be useful.

  • Direct impact (b) cost of private and public control measures

    Estimated private treatment costs €0.03 - €0.65 per hen in Europe annually.

    €231 million per year in the European Union in control and production losses (Sigognault Flochlay et al., 2017).

    GAP :

    Updated impacts per year could be useful.

  • Indirect impact

    With increased focus on sustainable intensification of agriculture, food provenance and animal welfare, consumers may respond negatively due to the negative impacts of this pathogen on bird welfare.

    The illegal use of some products (e.g. Fipronil) https://www.bbc.co.uk/news/world-europe-40878381 to control this pathogen may result in consumer rejection of the product (eggs) and may threaten food security.

    The egg retail industry is particularly sensitive to societal-driven changes in practice; for example, the move away from retailing eggs produced in cage systems by large supermarkets was driven by strong consumer pressure (https://www.theguardian.com/world/2016/jul/14/tesco-to-stop-selling-caged-hens-eggs-by-2025-after-petition.

    The introduction of new legislation or welfare standards designed to increase hen welfare may force producers to “upgrade” production facilities to get rid of mite, with an important economic impact on them.

    GAPS :

    Egg consumption per capita in developing countries has risen faster than any other major food item, including meat, since 1961 and global egg production has tripled since 1970 (FAO figures). Throughout expanding markets in Europe and Asia, poultry red mite remains an intractable problem, with 65% of premises in China reporting infestation; 85% in Japan; 100% in Poland, for example. The scale of this issue is therefore considerable and this is reflected in the number of novel interventions currently under development. Improved interventions will therefore deliver direct positive economic impact to organisations and companies developing such products.

    Societal impacts of the development of better interventions will allow the delivery of a high nutritional value, low cost, healthy food item which has been produced in hens with lower levels of parasitism (and thus higher welfare standards).

  • Trade implications

  • Impact on international trade/exports from the EU

    None.

    GAP :

    Increased trade may increase potential for pathogen to transfer between regions if levels of sanitary measures does not secure elimination of live mite.

  • Impact on EU intra-community trade

    None.

    GAP :

    Increased trade may increase potential for pathogen to transfer between regions if levels of sanitary measures does not secure elimination of live mite.

  • Impact on national trade

    None.

    GAP :

    Increased trade may increase potential for pathogen to transfer between regions if levels of sanitary measures does not secure elimination of live mite.

  • Main perceived obstacles for effective prevention and control

    Lack of connectivity of control measures across the production chain: The pathogen is present in the whole egg production chain; to solve the problem all links should be working very intensively together on the problem.

    Diagnostics are adequate but infestations are not dealt with quickly enough to suppress population growth effectively.

    Good pharmaceuticals exist but the perception may be that they are too expensive for routine use. Currently available biocides and veterinary products have potential to affect off-target organisms and ecosystems with long term consequences.

    No vaccines are currently commercially available.

    GAP :

    Opportunities and gaps around biosecurity, improved use of existing pharmaceuticals and vaccines, and development of novel products in this area in particular should be addressed.

  • Main perceived facilitators for effective prevention and control

    Independent information and advice.Outreach services.Restrict or decrease movement of infested birds and equipment.Adoption of IPM practices.Sober habits for chemical use.Good sanitary conditions.

    GAP :

    Gaps and opportunities in all areas listed.

  • Links to climate

    Seasonal cycle linked to climate

    Higher temperatures -> shorter lifecycle -> increase of problem is faster (see also Section “Seasonal cycle”).

    GAP :

    Impact of climate change unknown.

  • Distribution of disease or vector linked to climate

    Because the temperature of most commercial hen houses is tightly regulated, this is not really applicable, though, in colder areas (if the temperatures of the sheds are not well-regulated) the life cycle may be longer resulting in lower numbers of pests and better control of the pest. The opposite is true during summer when temperature management systems in commercial sheds may not cope with increased environmental temperatures.

    GAP :

    Dependent on nature of production system.

  • Outbreaks linked to extreme weather

    Extremes of temperature will result in death of the pathogen.

    GAP :

    Largely irrelevant due to nature of production system.

  • Sensitivity of disease or vectors to the effects of global climate change (climate/environment/land use)

    Unknown – possibility that, with rising temperatures, the infestation will increase faster, will become more persistent in larger parts of Europe, result in more losses and more problems to control.

    GAP :

    Impact of climate change unknown.

Risk

  • Direct: All egg production units are at risk of infestation. Risks are associated with movement of birds, equipment, sanitation levels, infestation levels in breeder flocks.Indirect: Because of the use of chemicals of which residues may be in the manure, the aquatic live and live in the soil may be destroyed (see description for use from the chemical products). Also application of some interventions may cause negative health effects in humans. An example is Silica dust: It is not definitively known if it is detrimental to health for humans, but farmers have become increasingly worried.

    GAP :

    Gaps in knowledge on environmental and human risk.

Main critical gaps

  • Development of novel, safe interventions (particularly new pharmaceuticals and vaccines).Understanding the environmental risks and/or effects of the use of current pharmaceuticals.Integration of IPM: what are the best methods to integrate and how?Clarity around disease vector status.

Conclusion

  • Poultry red mite is a major concern to the egg laying industry from both a production and welfare point of view. Diagnosis is usually by visual inspection either of mite traps or housing in the poultry shed. Improvements could be made to this method of diagnosis which could lead to earlier interventions to prevent population build-up. Sanitation, hygiene and biosecurity measures prior to introducing new birds into buildings can be effective measures to control the parasite but in most situations this will need to be complemented with the use of acaricides to treat the premises. After the introduction of new birds, acaricidal treatment may be by oral administration of fluralaner-based treatments via the drinking water of the birds during the laying cycle). Acaricide treatments are limited and some which act through direct contact with the mites are increasingly ineffective as resistance develops. The newer fluralaner-based acaricide which is administered orally is currently highly effective but long term effects on the environment following its use are unknown. New pharmaceutical products coming to the market to control this parasite should be developed with this method of administration in mind but should be more specific for PRM only. The ecological impacts of all pharmaceutical interventions should be investigated, particularly where manure from treated hen sheds is applied to agricultural land as a fertiliser. There are opportunities to integrate current pharmaceutical methods into integrated pest management systems (IPM) but a clearer understanding of the potential synergies and conflicts between different interventions is required. Development of new, “green” products, in the EU at least, is difficult due to legislation. An intra-communautaire dialogue about the regulations for allowing use of such products. (e.g. the use of green soap and water or the application of rape seed oil) as treatments should be initiated. Vaccines against this parasite would be an ideal intervention but current prototypes probably lack the required efficacy and longevity of action to be useful commercially. Research in this area should encompass the traditionally vaccinology questions around antigen discovery and vaccine administration but also integrate modelling to estimate the levels of efficacy required for adequate control of the parasite in IPM systems. For research to underpin both novel pharmaceutical or green products and vaccines, a number of recent developments offer great promise as elements of the toolbox for poultry red mite research: the publication of the draft genome and transcriptomes, the development of RNAi and the development of in vivo methods to test compounds and vaccines on small numbers of birds.

Sources of information

  • Expert group composition

    Alasdair Nisbet, Moredun Research Institute, UK – [Leader]

    Monique Mul, Proeftuin Zwaagdijk, The Netherlands

    Lise Roy, CEFE, France

    Øivind Øines, National Veterinary Institute, Norway

    Maarten de Gussem, VETWORKS, Belgium

    Mark Williams, British Egg Industry Council, UK

    Emmanuel Thomas, MSD Animal Health, Germany

  • Date of submission by expert group

    24th January 2020

  • References

    Bartley K, Turnbull F, Wright HW, Huntley JF, Palarea-Albaladejo J, Nath M, Nisbet AJ. Field evaluation of poultry red mite (Dermanyssus gallinae) native and recombinant prototype vaccines. Vet Parasitol. 2017 Sep 15;244:25-34. doi: 10.1016/j.vetpar.2017.06.020.

    Bensussan A, Rometti C, Pringuey D, Delaunay P, Hamm-Orlowski M, Benoit M. 2019. Delusional infestation. A psychopathological proposal, the ‘‘typology of the contaminated’. Annales médico-psychologiques, (in press) Doi : 10.1016/j.amp.2018.03.016 [in French].

    Brännström S, Morrison DA, Mattsson JG, Chirico J. Genetic differences in internal transcribed spacer 1 between Dermanyssus gallinae from wild birds and domestic chickens. Med Vet Entomol. 2008 Jun;22(2):152-5. doi: 10.1111/j.1365-2915.2008.00722.x.

    Burgess STG, Bartley K, Nunn F, Wright HW, Hughes M, Gemmell M, Haldenby S, Paterson S, Rombauts S, Tomley FM, Blake DP, Pritchard J, Schicht S, Strube C, Øines Ø, Van Leeuwen T, Van de Peer Y, Nisbet AJ. Draft Genome Assembly of the Poultry Red Mite, Dermanyssus gallinae. Microbiol Resour Announc. 2018 Nov 8;7(18). pii: e01221-18. doi: 10.1128/MRA.01221-18.

    Butler CG. 1940. The Choice of Drinking Water by the Honeybee. Journal of Experimental Biology 17: 253-261.Cafiero M.A., Camarda A., Circella E., Santagada G., Schino G., Lomuto M. 2008. Pseudoscabies caused by Dermanyssus gallinae in Italian city dwellers: a new setting for an old dermatitis, J. Eur. Acad. Dermatol. Venereol. 22, 1382–1383.

    Cafiero MA, Barlaam A, Camarda A, Radeski M, Mul M, Sparagano O, Giangaspero A. Dermanyssus gallinae attacks humans. Mind the gap! Avian Pathol. 2019 Sep;48(sup1):S22-S34. doi: 10.1080/03079457.2019.1633010.

    Chu TT, Murano T, Uno Y, Usui T, Yamaguchi T. .2015. Molecular epidemiological characterization of poultry red mite, Dermanyssus gallinae, in Japan. J Vet Med Sci. 2015 Nov;77(11):1397-403. doi: 10.1292/jvms.15-0203.

    Di Palma A, Giangaspero A, Cafiero MA, Germinara GS. A gallery of the key characters to ease identification of Dermanyssus gallinae (Acari: Gamasida:Dermanyssidae) and allow differentiation from Ornithonyssus sylvarium (Acari:Gamasida: Macronyssidae). Parasit Vectors. 2012 May 30;5:104. doi:10.1186/1756-3305-5-104.

    El Adouzi M, Arriaga-Jiménez A, Dormont L, Barthes N, Labalette A, Lapeyre B, Bonato O, Roy L. Modulation of feed composition is able to make hens less attractive to the poultry red mite Dermanyssus gallinae. Parasitology. 2019 Sep 27:1-11. doi: 10.1017/S0031182019001379.

    Sigognault Flochlay A, Thomas E, Sparagano O. Poultry red mite (Dermanyssus gallinae) infestation: a broad impact parasitological disease that still remains a significant challenge for the egg-laying industry in Europe. Parasit Vectors. 2017 Aug 1;10(1):357. doi: 10.1186/s13071-017-2292-4.

    Kaab H, Bain MM, Bartley K, Turnbull F, Wright HW, Nisbet AJ, Birchmore R,, Eckersall PD. Serum and acute phase protein changes in laying hens, infested with poultry red mite. Poult Sci. 2019 Feb 1;98(2):679-687. doi: 10.3382/ps/pey431.

    Kaczala F, Blum SE. The Occurrence of Veterinary Pharmaceuticals in the Environment: A Review. Curr Anal Chem. 2016 Jun;12(3):169-182. doi:10.2174/1573411012666151009193108.

    Kamau, L.M., Wright, H.W., Nisbet, A.J., Bowman, A.S. 2013. Development of an RNA-interference procedure for gene knockdown in the poultry red mite, Dermanyssus gallinae: Studies on histamine releasing factor and Cathepsin-D. African Journal of Biotechnology 12; 1350-1356.

    Kavallari A, Küster T, Papadopoulos E, Hondema, LS, Øines Ø, Skov J, Sparagano O, Tiligada E. (2018) Avian mite dermatitis: Diagnostic challenges and unmet needs, Parasite Immunology. 018;40:e12539. https://doi.org/10.1111/pim.12539.

    Lammers GA, Bronneberg RGG, Vernooij JCM, Stegeman JA. Experimental validation of the AVIVET trap, a tool to quantitatively monitor the dynamics of Dermanyssus gallinae populations in laying hens. Poult Sci. 2017 Jun 1;96(6):1563-1572. doi: 10.3382/ps/pew428.

    Lima-Barbero JF, Contreras M, Mateos-Hernández L, Mata-Lorenzo FM, Triguero-Ocaña R, Sparagano O, Finn RD, Strube C, Price DRG, Nunn F, Bartley K, Höfle U, Boadella M, Nisbet AJ, Fuente J, Villar M. A vaccinology Approach to the Identification and Characterization of Dermanyssus gallinae Candidate Protective Antigens for the Control of Poultry Red Mite Infestations. Vaccines (Basel). 2019 Nov 20;7(4). pii: E190. doi: 10.3390/vaccines7040190.

    Marangi M, Cantacessi C, Sparagano OA, Camarda A, Giangaspero A. Molecular characterization and phylogenetic inferences of Dermanyssus gallinae isolates in Italy within an European framework. Med Vet Entomol. 2014 Dec;28(4):447-52. doi: 10.1111/mve.12050.

    Mul MF, Koenraadt CJM (2009) Preventing introduction and spread of Dermanyssus gallinae in poultry facilities using the HACCP method. Exp Appl Acarol 48: 167-181.

    Mul MF, Van Riel JW, Meerburg BG, Dicke M, George DR, Groot Koerkamp PWG (2015). Validation of an automated mite counter for Dermanyssus gallinae in experimental laying hen cages. Exp Appl Acarol 66, 4: 589-603.

    Mul MF (2017). Advancing Integrated Pest Management for Dermanyssus gallinae in laying hen facilities. Doctoral Dissertation, Wageningen University. Retrieved from http://library.wur.nl/WebQuery/wurpubs/fulltext/394911.

    Nordenfors H, Chirico J. Evaluation of a sampling trap for Dermanyssus gallinae (Acari: Dermanyssidae). J Econ Entomol. 2001 Dec;94(6):1617-21.

    Nordenfors H, Höglund J, Uggla A. 1999. Effects of Temperature and humidity on oviposition, molting, and longevity of Dermanyssus gallinae (Acari : Dermanyssidae). Journal of Medical Entomology 36:68-72.

    Nunn F, Bartley K, Palarea-Albaladejo J, Innocent GT, Turnbull F, Wright HW, Nisbet AJ. A novel, high-welfare methodology for evaluating poultry red mite interventions in vivo. Vet Parasitol. 2019 Mar;267:42-46. doi:10.1016/j.vetpar.2019.01.011.

    Øines, Ø., Brännström, S., 2011. Molecular investigations of cytochrome c oxidase subunit I (COI) and the internal transcribed spacer (ITS) in the poultry red mite, Dermanyssus gallinae, in northern Europe and implications for its transmission between laying poultry farms. Med. Vet. Entomol. 25, 402–412. doi:10.1111/j.1365-2915.2011.00958.x

    Pezzi M., Leis M., Chicca M., Roy L. (2017) Gamasoidosis caused by the special lineage L1 of Dermanyssus gallinae (Acarina: Dermanyssidae): A case of heavy infestation in a public place in Italy. Parasitology International 66(5):666-670.

    Price DRG, Küster T, Øines Ø, Oliver EM, Bartley K, Nunn F, Lima Barbero JF, Pritchard J, Karp-Tatham E, Hauge H, Blake DP, Tomley FM, Nisbet AJ. Evaluation of vaccine delivery systems for inducing long-lived antibody responses to Dermanyssus gallinae antigen in laying hens. Avian Pathol. 2019 Sep;48(sup1):S60-S74. doi:10.1080/03079457.2019.1612514.

    Pugliese N, Circella E, Cocciolo G, Giangaspero A, Horvatek Tomic D, Kika TS, Caroli A, Camarda A. Efficacy of λ-cyhalothrin, amitraz, and phoxim against the poultry red mite Dermanyssus gallinae De Geer, 1778 (Mesostigmata: Dermanyssidae): an eight-year survey. Avian Pathol. 2019 Sep;48(sup1):S35-S43.doi: 10.1080/03079457.2019.1645295.

    Raele DA, Galante D, Pugliese N, La Salandra G, Lomuto M, Cafiero MA. First report of Coxiella burnetii and Borrelia burgdorferi sensu lato in poultry red mites, Dermanyssus gallinae (Mesostigmata, Acari), related to urban outbreaks of dermatitis in Italy. New Microbes New Infect. 2018 Feb 22;23:103-109. doi:10.1016/j.nmni.2018.01.004.

    Roy L., Dowling A.P.G., Chauve C.M. and Buronfosse T. 2009. Delimiting species boundaries within Dermanyssus Dugès, 1834 (Acari: Mesostigmata) using a total evidence approach. Molecular Phylogenetics and Evolution 50:3:446-470.

    Roy L., Dowling A.P.G., Chauve C.M., Buronfosse T. 2010. Diversity of Phylogenetic Information According to the Locus and the Taxonomic Level: An Example From a Parasitic Mesostigmatid Mite Genus.International Journal of Molecular Sciences 11(4):1704-1734.

    Roy L., Buronfosse T. 2011. Using mitochondrial and nuclear sequence data for disentangling population structure in complex pest species: a case study with Dermanyssus gallinae. PLoS ONE 6(7): e22305.

    Roy L., El Adouzi M., Lourdes Moraza M., Chiron G., Villeneuve de Janti E., Le Peutrec G., Bonato, O. (2017) Arthropod communities of laying hen houses: An integrative pilot study toward conservation biocontrol of the poultry red mite Dermanyssus gallinae. Biological Control 114: 176–194.

    Sommer, D., Heffels-Redmann, U., Kohler, K., Lierz, M., Kaleta, E.F., 2016. Role of the poultry red mite (Dermanyssus gallinae) in the transmission of avian influenza A virus. Tierarztl. Prax. G. N. 44, 26-33.

    Thomas E, Zoller H, Liebisch G, Alves LFA, Vettorato L, Chiummo RM, Sigognault-Flochlay A. In vitro activity of fluralaner and commonly used acaricides against Dermanyssus gallinae isolates from Europe and Brazil. Parasit Vectors. 2018 Jun 25;11(1):361. doi: 10.1186/s13071-018-2956-8.

    Tucci, E. C., A. P. Prado, and R. P. Araújo. 2008. Development of Dermanyssus gallinae (Acari: Dermanyssidae) at different temperatures. Vet Parasitol 155:127-132.

    Valiente Moro, C., Chauve, C., Zenner, L., 2007. Experimental infection of Salmonella Enteritidis by the poultry red mite, Dermanyssus gallinae. Veterinary Parasitology 146, 329–336. https://doi.org/10.1016/j.vetpar.2007.02.024.

    Wang C, Huang Y, Zhao J, Ma Y, Xu X, Wan Q, Li H, Yu H, Pan B. First record of Aspergillus oryzae as an entomopathogenic fungus against the poultry red mite Dermanyssus gallinae. Vet Parasitol. 2019 Jul;271:57-63. doi: 10.1016/j.vetpar.2019.06.011.