**4. Control measures**

Treatment and control of PRM infestations have until recently relied on the spraying of chemical acaricides in infested premises, and mostly still occurs despite the limited list of products licensed to be used against the PRM in the EU. In general, traditional control actions achieve only temporary effects and mite populations return to levels prior to treatment soon after treatment application. One of the main limitations in the use of pesticides is the incapacity to apply the product to a degree that does not allow the target to escape from exposure by hiding in cracks and crevices [38]. Another significant problem in the use of pesticides is the emergence of resistances [69]. The number of PRM populations with reduced sensibility to traditional pesticides as λ-Cyhalothrin or Amitraz has grown especially after 2012. In the case of Phoxim, which has been considered a highly effective compound, highly resistant populations have been detected since 2015 [70]. This is probably related to withdrawal of most of the labeled compounds from the marked and subsequent overuse and misuse of the only remaining products available. The single chemical pesticide that shows satisfactory results is a recent labeled to be used as poultry isoxazoline, Fluralaner. Fluralaner has demonstrated a nearly

100% efficacy after two applications in poultry farms [71]. The key for this product is that with the oral administration the treatment reaches the whole mite population when the mites feed on the hens. This delivery method avoids the necessity to spray the product, a way of administration that has been proven of low efficacy for the control of PRM as there are mites that escape from the treatment.

An often-neglected tool for the control of PRM infestations in a layer hen house is the monitorization of the population. Many treatments do not show the expected results because they have not been applied at the right moment. The decision for applying treatment is traditionally taken when the farm employees announce a severe infestation, which is usually too late to allow successful control [72]. A proper monitorization routine can promote early detection and quantification of the infestation level and thus allowing proper programming of control measures. There are multiple methodologies that can be used for monitorization, including both quantitative and qualitative techniques. A description of the most commonly used monitoring methods has been recently reviewed [73]. Many monitoring systems are based on the placement of traps that emulate the hiding places of the mites and that are checked periodically. In this way, depending on the technique the farmer can obtain an estimate of the mite population in the hen house and/or a trend for the mite population evolution. There appears not be a single best choice for a monitoring method as it depends on the time and resources available in the farm. However, farms with monitoring programs in place can improve their capacity of PRM control [74].

Development of new control interventions is currently a priority in PRM research as a consequence of the severe impact of the mite in the egg-laying industry and the scarce resources for its control (**Figure 2**). Amongst those novel methods, treatments with essential oils and plant extracts have received significant attention. There are many studies on the effects of essential oils against PRM, but variable efficacy is observed [75]. Benefits of plant extracts and essential oils include their low mammalian and bird toxicity and short environmental persistence [75]. Several plant-based products are already commercialized against veterinary pests, and many others are in research phase. Essential oils are traditionally used for their repellence of pest arthropods [75]. The effect of essential oils can be due the influence of a number of volatile organic compounds (VOCs) in the host-recognition process [20]. Recent research found that the odor emitted by the hens can be modified through addition of plant-originated VOCs to the food and that some of those VOCs showed repellent activity against the PRM, making the hens less attractive to the mites [76]. The other approach for the use of plant derived compounds is using its insecticide properties for treating the hen house environment. Amongst those substances, neem oil is receiving special attention from researchers [75, 77]. Neem oil preparations are made of essential oil obtained from an Indian tree (*Azadirachta indica*) and have shown promising effects in PRM population reductions [77]. A disadvantage of neem oil application is the possible effects of the oily film on the farm installations and eggs, but technological improvements such as reducing the volume of solution or the droplet size can be applied to reduce these adverse effects [77].

Mite communities constituted by different mite species are able to establish themselves in layer farm buildings, mainly associated with manure [78]. These communities include mite species that are predators of free-living nematodes and arthropods, including mites [78]. Some *Hypoaspis* species identified in starling nests are considered putative predators of *D. gallinae* [79] and two mite species are already commercialized to be used in layer farms: *Androlaelaps casalis* (Androlis, APPI-group Koppert. France) and *Cheyletus eruditus* (Taurrus,

**241**

*Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*)*

APPI-group Koppert. France). *A. casalis* have shown to control, but no to eradicate, PRM populations under laboratory conditions but was more efficient at temperatures under 30°C [80]. The authors suggested that predation can occur over other mite species when *D. gallinae* is hiding in safe places, basically at different heights (*D. gallinae* was on high areas of the cages while predators remained on the floor) [80]. Predatory mites are already effectively used in the control of phytophagous mites in greenhouses and in pig farms for the control of non-hematophagous arthropods. Biocontrol of PRM in layer farmhouses is based upon the massive release of predatory mites. The effectivity of predatory mites to control PRM infestations is variable, probably due to variations in environmental conditions [79]. The main disadvantage of using predatory mites as a control tool of *D. gallinae* is their high sensitivity to acaricides used to treat PRM infestations [78]. Thus, biocontrol using predatory mites is not compatible with the use of

Another control method is based upon a perch design (Q-perch), which prevents

Vaccination against ectoparasites is not solely focused on the prevention of the infestation but also on the reduction of the parasite population [85]. Vaccination have demonstrated to provide high levels of protection against blood-feeding ectoparasites by reducing cattle tick populations and prevalence of certain tick-borne pathogens [86]. The only commercial vaccines against ectoparasites (TickGard and Gavac) were developed with recombinant tick midgut antigens Bm86 and Bm95 and registered for the control of cattle tick infestations [87]. This vaccines demonstrated their efficacy for the control of tick infestations while reducing the use of acaracides and encourage further research for the identification of new effective protective

Vaccine development relies on the identification of proteins that can act as protective antigens to which the host develops an immune response. The identification of protective antigens in *D. gallinae* has been limited by the lack of molecular research about the mite. The description on the mite transcriptome [89] and, more recently, its genome [90] can enhance the understanding of the host–parasite relationship and the identification of protective antigens. Two approaches have been followed for PRM vaccines development, testing of mite extracts and the production of vaccines based on recombinant proteins (**Table 1**). Vaccination against PRM recombinant proteins has induced antigen specific IgY responses but variable results have been obtained when mites fed in *in vitro* tests on blood from immunized hens or blood enriched with antibodies extracted from egg yolk. Another limitation for the assessment of efficacy of a candidate antigen has been the high background effects observed in the *in vitro* tests due to the feeding physiology of the PRM. A recent optimization of an on-hen feeding device allows a more physiological evaluation of the vaccine effects allowing a better

the mite from reaching the hens by an electrified wire placed just beneath the perch where the bird is roosting [81]. Various desiccant dusts, diatomaceous earth and synthetic silica products are commonly used in commercial layer farms [74]. Generally, it is a measure used as a temporal constraint of PRM infestation and to reduce the number of treatments with synthetic acaricides. Inert dust kills the mite by dehydration and probably, by cuticle damage by destroying its protective wax layer [82]. The main limitation of the use of inert dusts is the limited efficacy in environments with high levels of relative humidity [82]. A synergistic effect between inert dusts and entomopathogenic fungi have been described [83]. The use of entomopathogenic fungus for the control of PRM is recent and there is limited research. Laboratory tests show promising results, and some have been tested with

*DOI: http://dx.doi.org/10.5772/intechopen.90439*

acaricides.

some success in field trials [84].

antigens using different approaches [88].

#### *Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*) DOI: http://dx.doi.org/10.5772/intechopen.90439*

*Parasitology and Microbiology Research*

ity of PRM control [74].

100% efficacy after two applications in poultry farms [71]. The key for this product is that with the oral administration the treatment reaches the whole mite population when the mites feed on the hens. This delivery method avoids the necessity to spray the product, a way of administration that has been proven of low efficacy for the

An often-neglected tool for the control of PRM infestations in a layer hen house is the monitorization of the population. Many treatments do not show the expected results because they have not been applied at the right moment. The decision for applying treatment is traditionally taken when the farm employees announce a severe infestation, which is usually too late to allow successful control [72]. A proper monitorization routine can promote early detection and quantification of the infestation level and thus allowing proper programming of control measures. There are multiple methodologies that can be used for monitorization, including both quantitative and qualitative techniques. A description of the most commonly used monitoring methods has been recently reviewed [73]. Many monitoring systems are based on the placement of traps that emulate the hiding places of the mites and that are checked periodically. In this way, depending on the technique the farmer can obtain an estimate of the mite population in the hen house and/or a trend for the mite population evolution. There appears not be a single best choice for a monitoring method as it depends on the time and resources available in the farm. However, farms with monitoring programs in place can improve their capac-

Development of new control interventions is currently a priority in PRM research as a consequence of the severe impact of the mite in the egg-laying industry and the scarce resources for its control (**Figure 2**). Amongst those novel methods, treatments with essential oils and plant extracts have received significant attention. There are many studies on the effects of essential oils against PRM, but variable efficacy is observed [75]. Benefits of plant extracts and essential oils include their low mammalian and bird toxicity and short environmental persistence [75]. Several plant-based products are already commercialized against veterinary pests, and many others are in research phase. Essential oils are traditionally used for their repellence of pest arthropods [75]. The effect of essential oils can be due the influence of a number of volatile organic compounds (VOCs) in the host-recognition process [20]. Recent research found that the odor emitted by the hens can be modified through addition of plant-originated VOCs to the food and that some of those VOCs showed repellent activity against the PRM, making the hens less attractive to the mites [76]. The other approach for the use of plant derived compounds is using its insecticide properties for treating the hen house environment. Amongst those substances, neem oil is receiving special attention from researchers [75, 77]. Neem oil preparations are made of essential oil obtained from an Indian tree (*Azadirachta indica*) and have shown promising effects in PRM population reductions [77]. A disadvantage of neem oil application is the possible effects of the oily film on the farm installations and eggs, but technological improvements such as reducing the volume of solution or the droplet size can be applied to reduce these

Mite communities constituted by different mite species are able to establish themselves in layer farm buildings, mainly associated with manure [78]. These communities include mite species that are predators of free-living nematodes and arthropods, including mites [78]. Some *Hypoaspis* species identified in starling nests are considered putative predators of *D. gallinae* [79] and two mite species are already commercialized to be used in layer farms: *Androlaelaps casalis* (Androlis, APPI-group Koppert. France) and *Cheyletus eruditus* (Taurrus,

control of PRM as there are mites that escape from the treatment.

**240**

adverse effects [77].

APPI-group Koppert. France). *A. casalis* have shown to control, but no to eradicate, PRM populations under laboratory conditions but was more efficient at temperatures under 30°C [80]. The authors suggested that predation can occur over other mite species when *D. gallinae* is hiding in safe places, basically at different heights (*D. gallinae* was on high areas of the cages while predators remained on the floor) [80]. Predatory mites are already effectively used in the control of phytophagous mites in greenhouses and in pig farms for the control of non-hematophagous arthropods. Biocontrol of PRM in layer farmhouses is based upon the massive release of predatory mites. The effectivity of predatory mites to control PRM infestations is variable, probably due to variations in environmental conditions [79]. The main disadvantage of using predatory mites as a control tool of *D. gallinae* is their high sensitivity to acaricides used to treat PRM infestations [78]. Thus, biocontrol using predatory mites is not compatible with the use of acaricides.

Another control method is based upon a perch design (Q-perch), which prevents the mite from reaching the hens by an electrified wire placed just beneath the perch where the bird is roosting [81]. Various desiccant dusts, diatomaceous earth and synthetic silica products are commonly used in commercial layer farms [74]. Generally, it is a measure used as a temporal constraint of PRM infestation and to reduce the number of treatments with synthetic acaricides. Inert dust kills the mite by dehydration and probably, by cuticle damage by destroying its protective wax layer [82]. The main limitation of the use of inert dusts is the limited efficacy in environments with high levels of relative humidity [82]. A synergistic effect between inert dusts and entomopathogenic fungi have been described [83]. The use of entomopathogenic fungus for the control of PRM is recent and there is limited research. Laboratory tests show promising results, and some have been tested with some success in field trials [84].

Vaccination against ectoparasites is not solely focused on the prevention of the infestation but also on the reduction of the parasite population [85]. Vaccination have demonstrated to provide high levels of protection against blood-feeding ectoparasites by reducing cattle tick populations and prevalence of certain tick-borne pathogens [86]. The only commercial vaccines against ectoparasites (TickGard and Gavac) were developed with recombinant tick midgut antigens Bm86 and Bm95 and registered for the control of cattle tick infestations [87]. This vaccines demonstrated their efficacy for the control of tick infestations while reducing the use of acaracides and encourage further research for the identification of new effective protective antigens using different approaches [88].

Vaccine development relies on the identification of proteins that can act as protective antigens to which the host develops an immune response. The identification of protective antigens in *D. gallinae* has been limited by the lack of molecular research about the mite. The description on the mite transcriptome [89] and, more recently, its genome [90] can enhance the understanding of the host–parasite relationship and the identification of protective antigens. Two approaches have been followed for PRM vaccines development, testing of mite extracts and the production of vaccines based on recombinant proteins (**Table 1**). Vaccination against PRM recombinant proteins has induced antigen specific IgY responses but variable results have been obtained when mites fed in *in vitro* tests on blood from immunized hens or blood enriched with antibodies extracted from egg yolk. Another limitation for the assessment of efficacy of a candidate antigen has been the high background effects observed in the *in vitro* tests due to the feeding physiology of the PRM. A recent optimization of an on-hen feeding device allows a more physiological evaluation of the vaccine effects allowing a better


**243**

**Antigen** Phosphoglycerate dehydrogenase

Serpin-1 Hemelipoglycoprotein-1

Vitellogenin-1 Peptidase C1A-like cysteine proteinase

Serpin-2 Unknown function protein 3

Paramyosin Tropomyosin Deg-SRP-1 + Deg-VIT-1 + Deg-PUF-1

Calumenin

Akirin Cathepsin D-1

Subolesin Cathepsin D-1 Cathepsin D-1 *Abbreviations: M, mortality; O, Oviposition;* ↑*, increase;* ↓*, reduction.*

*\*The effects are statistically significant.*

**Table 1.** *Antigens tested as vaccine candidates against infestations by* D. gallinae.

DNA

*D. gallinae*

*Rhipicephalus microplus*

chicken IL-21

*Eimeria tenella*

**Type** Recombinant

*D. gallinae*

**Species**

**Adjuvant**

QuilA

**Test** In vitro [93]

↑ 4.1 M ↑ 12 M\* ↑ 18.9 M \* ↑ 21.9 M\*

↑ 14.5 M

↓ 8.2 M ↑ 3.5 M ↑ 20.1 M\*

↑16.5 M\*

> ISA 70 VG

ISA 71 VG

Field

On hen [79]

↓ 35 O\* ↓ 42 O\* ↓ 50 O\* ↓ 44 O\*

—

—

[102]

[104]

[104]

[104]

[103]

[102]

—

[101]

[96]

[101]

[94]

[94]

[94]

[94]

[94]

[94]

[94]

**Effects (%)**

**Reference**

*Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*)*

*DOI: http://dx.doi.org/10.5772/intechopen.90439*


#### *Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*) DOI: http://dx.doi.org/10.5772/intechopen.90439*

*Parasitology and Microbiology Research*

**242**

**Antigen** Soluble protein mite extract

Soluble protein mite extract

IEX Group 4 IEX Group 5 IEX Group 2 IEX Group 1 IEX Group 3 PBS soluble mite extract

Membrane associated

Urea soluble Integral membrane

Mite extract Soluble protein mite extract

Akirin

Bm86 Histamine release factor

Cathepsin D-1 Cathepsin L-1 Unknown function protein 1

Unknown function protein 2

Aspartyl proteinase

Recombinant

*Aedes albopictus*

*Rhipicephalus microplus*

*D. gallinae*

QuilA

In vitro [98] In vitro [93]

↑ 6.9 M\* ↑ 2.6 M\* ↑ 18.4 M\*

↑ 0.6 M ↑ 5.6 M

[94]

[94]

[94]

[100]

[100]

↑ 4.1 M\*

[99]

**Type** Native

**Species** *D. gallinae*

**Adjuvant** Incomplete Freund's

QuilA

In vivo [92] In vitro [93]

↑ 24 M ↑ 23.5 M\* ↑ 11.4 M\*

↓ 4.2 M ↑ 19.5 M\*

↑ 13 M\* ↑ 10.1 M\*

↑ 2.2 M ↑ 0.2 M ↓ 1.5 M

> ISA 50 V

ISA 207 VG

ISA 50 V

In vitro [95]

Field In vitro [95]

↑ 35.1 M\*

↑ 23 M\*

[97]

[97]

↑ 50.7 M\* ↓ 78 Pop\*

[96]

[95]

[93]

[93]

[93]

[93]

[94]

[94]

[94]

[94]

[94]

[94]

↑ 0.1 M

[92]

**Test**

**Effects (%)**

**Reference**

**Table 1.**

*Antigens tested as vaccine candidates against infestations by* D. gallinae.

assessment of novel antigens [91]. Vaccines can be considered as an alternative and complementary intervention for PRM control, which can reduce the use of acaricides.

## **5. Conclusions and future directions**

The negative impact of the PRM infestations have become more relevant with recent changes in the production systems, and it is expected to become worse as the market demands more welfare focused systems that reduce the options for controlling poultry infestations. These changes in the production procedures should include increased concerns in biosecurity and monitorization in order to achieve a better understanding of the mite ecology on each farm. PRM infestations constitute a challenge for the modern industry to guarantee hen welfare and prevention of risks for the workers.

Omics are a promising tool for enhancing the understanding of the mite-host interactions. These techniques are needed to resolve questions that are yet to be answered such as the determination of the role of the PRM as biological vectors for both poultry and human pathogens and the different mechanisms involved in the immune response in hens or if there are any on the mite side to modulate its host response. Alternative control methods and particularly vaccine are urgently needed for the effective and sustainable control of PRM infestations with the optimization and combination of different interventions.

See methodology for bibliometric analysis.

## **6. Methodology**

#### **6.1 Bibliometric analysis**

A bibliometric analysis was performed in the web database Scopus (https:// www.scopus.com) with the search code "dermanyssus AND gallinae" (date accessed: Sep 16, 2019). The search generated a total of 418 entries, from which 56 entries (14.4%) were published in the last 2 years (2018 and 2019). After the search was completed, we selected those references that addressed the main topics reviewed in this work.

#### **6.2 Scanning electron microscope (SEM) imaging**

Images obtained by scanning electron microscope (SEM) were used in **Figure 1** to show morphological characters that are useful for species identification [14]. The adult female mite used for SEM photography was dehydrated in absolute ethanol for 24 h. Specimens were mounted onto standard aluminum SEM stubs using conductive carbon adhesive tabs. Mites were observed and photographed with a field emission scanning electron microscope (Zeiss GeminiSEM 500, Oberkochen, Germany) operating in high vacuum mode at an accelerating voltage of 2 kV in the absence of metallic coating.

#### **6.3 Points of action for control measures**

The determination of the points of action for the different control measures was obtained based on the data available in previous works [1, 20, 22, 74–77, 79, 82, 103, 104].

**245**

**Author details**

and José de la Fuente1,4\*

Ciudad Real, Spain

2 SABIOTEC, Ciudad Real, Spain

Oklahoma State University, Stillwater, OK, USA

provided the original work is properly cited.

\*Address all correspondence to: jose\_delafuente@yahoo.com

*Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*)*

supported by the University of Castilla- La Mancha (Spain).

JFLB was supported by Ministerio de Ciencia, Innovación y Universidades (Spain), Doctorado Industrial contract (DI-14-06917) and Sabiotec SA. MV was

José Francisco Lima-Barbero1,2, Margarita Villar1,3, Ursula Höfle1

1 SABIO, Institute for Game and Wildlife Research, Ciudad Real, Spain

3 Biochemistry Section, Faculty of Science and Chemical Technologies, and

Regional Centre for Biomedical Research (CRIB), University of Castilla-La Mancha,

4 Department of Veterinary Pathobiology, Center for Veterinary Health Sciences,

© 2020 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

*DOI: http://dx.doi.org/10.5772/intechopen.90439*

**Acknowledgements**

*Challenges for the Control of Poultry Red Mite (*Dermanyssus gallinae*) DOI: http://dx.doi.org/10.5772/intechopen.90439*
