**3. One health: poultry industry, environment and human health**

#### **3.1 Poultry industry**

The PRM is not a significant issue in the broiler industry, mainly due to its short production cycle, but it poses a substantial threat to the egg-laying industry worldwide, except for layer farms in the USA where *Ornythonyssus sylviarum* is the main mite species affecting layer hens [28]. However, recent reports suggest significant increase of *D. gallinae* infestations in the USA [15]. Although *O. sylviarum* is also present in wild birds of European countries, *D. gallinae* is the specie responsible for farm infestations. However, mixed infestations have been reported in countries out of Europe [29]. Infestations can reach high prevalence in Europe, where the average prevalence is more than 80% with several countries reaching higher than 90% [30]. However, PRM prevalence can be more related to certain areas rather than a country as different prevalence has been observed in different regions of the same country [31]. PRM infestations have been described in every production system. Less-intensive farming systems present higher risks of infestation which usually is inversely proportional to the level of intensification [32]. Therefore, PRM prevalence is generally higher in backyard and free-range units, followed by barns and, ultimately, by enriched systems [33]. Enriched cages usually show higher levels of infestation when compared to traditional pens in those countries where they are still allowed [32]. These systems improve mite survival by providing more safe areas to the mite far from the reach of the hens and the treatments at the same time as they promote hen welfare.

Temporal dynamics of PRM infestations vary greatly between laying hen houses. Specific environmental conditions and differences in laying hen house management are responsible for these variations. The age of the flock is another modulating factor according to a model developed for forecasting the population dynamics in a hen house [34]. The age of the flock has a negative effect on the growth of the mite population as mite populations decline as the age of the hens increases despite the fact that the immune response of the hen against a PRM infestation has not been well characterized. An experimental infestation developed an increase of the serum amyloid-A [35], but hens do not generate natural potent immunoprotective responses [36]. The development of an immune response by the bird after a chronic exposure is a plausible explanation which has been proposed that requires further research [34, 37]. The type of hen hybrid and how they were raised as pullets seem to have some effects on the vertical distribution of the mite infestation in aviaries, which is explained by differences in the space use by different hybrids [38].

Infestation levels vary seasonally [38]. Seasons prone to more severe infestations also differ depending on the climate of each region [38]. Usually, seasons with mild temperatures and high relative humidity can be correlated with lower fluctuations of these parameters inside the layer house, providing more ideal conditions for the mite to grow and therefore show more severe infestations. In this way, in northern countries the infestation peak usually happens in summer months while in more temperate climates the most prevalent seasons are spring and autumn.

Moderate and low infestations do not seem to have an effect on the production parameters independently of the layer hen productive system [39]. Instead, severe infestations are associated with important production losses albeit variations between housing systems [21]. Therefore, PRM has been demonstrated to negatively affect the proportion of laying hens, egg weight and the amount of first-choice eggs in enriched cages facilities while detrimental effects have been observed on egg mass, first-choice eggs and bodyweight of hens housed in aviary

**237**

laying hen [54].

**3.2 Environment and wildlife**

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

systems [39]. The impact on egg production can cause reductions of up to 20% [8]. PRM infestations are also responsible for devaluation of eggs when these are blood spotted. The spots are the result of fed mites getting crushed beneath the eggs while

PRM is also responsible for health and welfare issues for egg-laying hens. When asked, most egg-producers commonly state that PRM is the major issue concerning hen welfare [41]. The main sign of a severe infestation is the anemia observed in the birds. An adult mite can ingest 0.2 μl of blood in a blood meal [42]. It is described that a laying hen can lose more than 3% of its blood volume every night [8]. In cases of severe infestations, increased bird mortality is observed due to exsanguination. The mortality due to a PRM infestation has been estimated to increase between 4 and 50% [43], and correlates with an increased mite burden. Several studies find significant relationships between PRM infestation and hen mortality [7, 44]. PRM infestation increases food and water intake. Hens under infestation suffer restlessness, agitation, sleep deprivation and increased preening and feather pecking [9, 45]. Thus, the infestation puts the hens into chronic distress making them more

Many dermanyssoid mites are confirmed vectors of bacterial and viral pathogens. Several pathogens have been isolated from *D. gallinae*, thus confirming its role as mechanical vector. Several reports have detected pathogenic bacteria in PRM such as *Coxiella burnetii*, *Erysipelothrix rhusiopathiae*, *Listeria monocytogenes*, *Pasterella multocida Mycoplasma gallisepticum, Chlamydophila psittaci* and Spirochetes [46–48]. However, its role as a biological vector for these pathogens is not yet fully elucidated and requires further research. The PRM has been demonstrated under laboratory conditions to act as a vector for *Salmonella enteritidis* where they showed the oral transmission after ingestion of washed mites contaminated by cuticular contact or during blood meal [49]. Additionally, *S*. *enterica* subsp. *enterica* serovar gallinarum biovar gallinarum (*S. gallinarum*), the etiological agent of the fowl typhoid, was found to survive for up to 4 months in infected mites [50]. Recently, Pugliese et al. [51] showed the maintenance of *S. gallinarum* in two different productive cycles where after an outbreak of fowl typhoid, the mites remained infected even after a sanitary break and vaccination of the second flock. An interesting finding of this work was that the number of bacteria found in the mites varied according to the antibody titers of the vaccinated hens. This finding illustrates the complex relationship between host, parasite and bacterial pathogen. PRM has an experimentally confirmed potential capacity for acting as a mechanical vector of avian influenza virus after a bloodmeal on infected hens [52]. Other viral agents such as avipox virus, fowl adenovirus, Marek's disease virus, avian paramyxovirus type I and the Eastern, Western and Venezuelan equine encephalo-

In summary, PRM is responsible for economic losses of around 231 million Euros annually in Europe considering the combination of the production losses, health issues and cost of mite infestation control [53]. Other reports estimate the economic impact of PRM infestations in Europe between 0.5 and 0.6 Euros per

Historically, wild birds were considered as the main source of the mite infestation in the poultry houses. However, mitochondrial cytochrome oxidase I *(mt-COI*) gene sequencing, which allowed secured *Dermanyssus* species identification, demonstrated that none of the *Dermanyssus* species that specifically parasitize wild birds were found in poultry farms and concluded that only *D. gallinae*

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

walking or hiding on the conveyor belt [40].

susceptible to diseases and reducing vaccine efficacy.

myelitis viruses have been isolated from PRM [7].

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

*Parasitology and Microbiology Research*

**3.1 Poultry industry**

promote hen welfare.

ent hybrids [38].

**3. One health: poultry industry, environment and human health**

The PRM is not a significant issue in the broiler industry, mainly due to its short production cycle, but it poses a substantial threat to the egg-laying industry worldwide, except for layer farms in the USA where *Ornythonyssus sylviarum* is the main mite species affecting layer hens [28]. However, recent reports suggest significant increase of *D. gallinae* infestations in the USA [15]. Although *O. sylviarum* is also present in wild birds of European countries, *D. gallinae* is the specie responsible for farm infestations. However, mixed infestations have been reported in countries out of Europe [29]. Infestations can reach high prevalence in Europe, where the average prevalence is more than 80% with several countries reaching higher than 90% [30]. However, PRM prevalence can be more related to certain areas rather than a country as different prevalence has been observed in different regions of the same country [31]. PRM infestations have been described in every production system. Less-intensive farming systems present higher risks of infestation which usually is inversely proportional to the level of intensification [32]. Therefore, PRM prevalence is generally higher in backyard and free-range units, followed by barns and, ultimately, by enriched systems [33]. Enriched cages usually show higher levels of infestation when compared to traditional pens in those countries where they are still allowed [32]. These systems improve mite survival by providing more safe areas to the mite far from the reach of the hens and the treatments at the same time as they

Temporal dynamics of PRM infestations vary greatly between laying hen houses. Specific environmental conditions and differences in laying hen house management are responsible for these variations. The age of the flock is another modulating factor according to a model developed for forecasting the population dynamics in a hen house [34]. The age of the flock has a negative effect on the growth of the mite population as mite populations decline as the age of the hens increases despite the fact that the immune response of the hen against a PRM infestation has not been well characterized. An experimental infestation developed an increase of the serum amyloid-A [35], but hens do not generate natural potent immunoprotective responses [36]. The development of an immune response by the bird after a chronic exposure is a plausible explanation which has been proposed that requires further research [34, 37]. The type of hen hybrid and how they were raised as pullets seem to have some effects on the vertical distribution of the mite infestation in aviaries, which is explained by differences in the space use by differ-

Infestation levels vary seasonally [38]. Seasons prone to more severe infestations also differ depending on the climate of each region [38]. Usually, seasons with mild temperatures and high relative humidity can be correlated with lower fluctuations of these parameters inside the layer house, providing more ideal conditions for the mite to grow and therefore show more severe infestations. In this way, in northern countries the infestation peak usually happens in summer months while in more

temperate climates the most prevalent seasons are spring and autumn.

Moderate and low infestations do not seem to have an effect on the production parameters independently of the layer hen productive system [39]. Instead, severe infestations are associated with important production losses albeit variations between housing systems [21]. Therefore, PRM has been demonstrated to negatively affect the proportion of laying hens, egg weight and the amount of first-choice eggs in enriched cages facilities while detrimental effects have been observed on egg mass, first-choice eggs and bodyweight of hens housed in aviary

**236**

systems [39]. The impact on egg production can cause reductions of up to 20% [8]. PRM infestations are also responsible for devaluation of eggs when these are blood spotted. The spots are the result of fed mites getting crushed beneath the eggs while walking or hiding on the conveyor belt [40].

PRM is also responsible for health and welfare issues for egg-laying hens. When asked, most egg-producers commonly state that PRM is the major issue concerning hen welfare [41]. The main sign of a severe infestation is the anemia observed in the birds. An adult mite can ingest 0.2 μl of blood in a blood meal [42]. It is described that a laying hen can lose more than 3% of its blood volume every night [8]. In cases of severe infestations, increased bird mortality is observed due to exsanguination. The mortality due to a PRM infestation has been estimated to increase between 4 and 50% [43], and correlates with an increased mite burden. Several studies find significant relationships between PRM infestation and hen mortality [7, 44]. PRM infestation increases food and water intake. Hens under infestation suffer restlessness, agitation, sleep deprivation and increased preening and feather pecking [9, 45]. Thus, the infestation puts the hens into chronic distress making them more susceptible to diseases and reducing vaccine efficacy.

Many dermanyssoid mites are confirmed vectors of bacterial and viral pathogens. Several pathogens have been isolated from *D. gallinae*, thus confirming its role as mechanical vector. Several reports have detected pathogenic bacteria in PRM such as *Coxiella burnetii*, *Erysipelothrix rhusiopathiae*, *Listeria monocytogenes*, *Pasterella multocida Mycoplasma gallisepticum, Chlamydophila psittaci* and Spirochetes [46–48]. However, its role as a biological vector for these pathogens is not yet fully elucidated and requires further research. The PRM has been demonstrated under laboratory conditions to act as a vector for *Salmonella enteritidis* where they showed the oral transmission after ingestion of washed mites contaminated by cuticular contact or during blood meal [49]. Additionally, *S*. *enterica* subsp. *enterica* serovar gallinarum biovar gallinarum (*S. gallinarum*), the etiological agent of the fowl typhoid, was found to survive for up to 4 months in infected mites [50]. Recently, Pugliese et al. [51] showed the maintenance of *S. gallinarum* in two different productive cycles where after an outbreak of fowl typhoid, the mites remained infected even after a sanitary break and vaccination of the second flock. An interesting finding of this work was that the number of bacteria found in the mites varied according to the antibody titers of the vaccinated hens. This finding illustrates the complex relationship between host, parasite and bacterial pathogen. PRM has an experimentally confirmed potential capacity for acting as a mechanical vector of avian influenza virus after a bloodmeal on infected hens [52]. Other viral agents such as avipox virus, fowl adenovirus, Marek's disease virus, avian paramyxovirus type I and the Eastern, Western and Venezuelan equine encephalomyelitis viruses have been isolated from PRM [7].

In summary, PRM is responsible for economic losses of around 231 million Euros annually in Europe considering the combination of the production losses, health issues and cost of mite infestation control [53]. Other reports estimate the economic impact of PRM infestations in Europe between 0.5 and 0.6 Euros per laying hen [54].

#### **3.2 Environment and wildlife**

Historically, wild birds were considered as the main source of the mite infestation in the poultry houses. However, mitochondrial cytochrome oxidase I *(mt-COI*) gene sequencing, which allowed secured *Dermanyssus* species identification, demonstrated that none of the *Dermanyssus* species that specifically parasitize wild birds were found in poultry farms and concluded that only *D. gallinae*

harbored synanthropic populations [11]. Additionally, the same research described that the *D. gallinae* populations associated with poultry farms belong to different genetic lineages [11]. In addition, recent research on genetic differences between *Ornithonyssus sylviarum* present in wild sparrow nests and layer houses in the USA indicated the absence of mite exchange [55]. However, wild bird nests located in the proximities of the hen house can act as a reservoir of mites and thus allow re-infestation. Mul et al. [56] performed a risk analysis in which poultry farmers and employees, followed by hen cadavers and manure aeration, represented the highest risks of introduction and spread of PRM in the farm. If the manure belts are shared amongst barns, they constitute a severe risk of spreading the PRM [56]. Rodents and insects are potential carriers of mites, and although the role of pests in the introduction and spread of PRM in layer farms has not been fully elucidated, a case of phoresy of *D. gallinae* has been described in a beetle [57].

In a recent questionnaire by free-range farmers in the UK, antiparasitics were reported as one of the three most commonly used medicines against PRM [41]. A recent scandal on the discovery of an unauthorized product in food-producing animals (Fipronil, C12H4Cl2F6N4OS) in contaminated eggs from farms in 45 countries worldwide. The concentration in the contaminated product did not reach toxic doses for humans, but a mediatic Public Health alert was raised, and a food fraud investigation was started by European authorities [58]. Only two compounds are specifically labeled to control PRM infestations while birds are present (Phoxim, C12H15N2O3PS and Spinosad, C41H65NO10 (A); C42H67NO10 (D)) by the European Union (EU), and recently a new compound (Fluralaner, C22H17Cl2F6N3O3) has been approved [59, 60]. Authorized products do not penetrate the whole egg but improper handling when breaking the shell can lead to food contamination [61]. Risks of residues of traditional and unlabeled pesticides entering the food chain are due to its presence in body tissues of hens that are slaughtered for human consumption [60]. A withdrawal period has been suggested for the skin tissue after application of Spinosad and Abamectin (C48H72O14 (B1a); C47H70O14 (B1b)), an acaricide with available formulations for spray application in some European countries, due to the detection of residues in this tissue [62]. The chemicals used to control PRM may also have adverse effects for workers directly exposed while applying the treatment. The limited availability of tools and the increase of resistance are forcing the farmers to turn to non-authorized products to face PRM infestations and underline the necessity for alternative control methods.

#### **3.3 Zoonotic risks**

*D. gallinae* is known as a bird ectoparasite but it has low host specificity [16]. This lack of specificity allows the mite to feed on mammals, including humans, when the natural host is not available [6]. Human parasitosis due to PRM is called gamasoidosis or dermanyssosis. Skin erythematous papules are the usual clinical signs for gamasoidosis and urticarial lesions have been also described [6]. Skin lesions are usually pruriginous and can be distributed throughout the entire body, but are more frequently located in the arms, legs and the upper trunk [6]. Regarding human gamasoidosis associated with *D. gallinae*, two epidemiological scenarios are described: urban cases and occupational cases [6]. *D. gallinae* is the most commonly ectoparasite identified as the causal agent of gamasoidosis, but the cases assigned to *D. gallinae* can be misdiagnosed due to the difficulty of species determination for non-trained practitioners. The geographical expansion of other similar mite species such as *Ornythonyssus* spp. [63] due to climate change, host expansion and globalization will require more precise analysis.

**239**

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

Occupational cases are those related to poultry workers. The infestation can occur both in professional workers and hobbyists. These mite attacks usually happen during the daytime, while the workers are handling birds, cages or collecting eggs or when cleaning the premises. High levels of mite infestation and lack of proper protective clothing increases the risk of mite bites. Despite the high prevalence of infestation in egg-laying farms and continued exposure of the workers to the PRM, the number of reports of occupational cases is limited [6, 64]. The low number of reported cases can be explained by the fact that the attacks occur under specific conditions (severe infestation and lack of protection) or because workers

Urban cases are not associated with poultry workers. These cases are usually linked to familiar homes or public buildings such as hospitals and halls. In these cases, synanthropic birds, generally pigeons, are the source of the infestation [6]. Most of them occur when the host has left the nest after the breeding season. At that moment, the mites search for a new host to obtain a bloodmeal. Recent investigations suggest the existence of a pigeon specific lineage (*D. gallinae* L1) that is more frequently involved in human gamasoidosis [65]. Skin lesions in urban cases tend to be more severe than those in occupational cases, basically due to extended

Reports of gamasoidosis are scarce but their frequency has increased in the recent years [6]. PRM gamasoidosis is still an underdiagnosed parasitosis mainly due to un-specific signs which do not lead the practitioners to a certain diagnosis and, generally, the fact that PRM bites cause only light to mild clinical symptoms, indistinguishable from other bug bites and do not put the patient in need of seeking medical assistance. Recently, the bacterial genera *Tsukamurella* has been identified as part of the microbiome of the PRM with an endosymbiotic relationship suggested [66]. *Tsukamurella* species are foremost saprophyte bacteria that have occasionally been identified as opportunistic organisms associated with postoperative infections [67]. This, and the avian pathogens listed earlier, together with reports of *D. gallinae* infestations in hospitals [68] highlight potential zoonotic risks associated with PRM. Thus, because of the potential vector role of PRM for zoonotic pathogens it should be included in routine medical differential diagnosis

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

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

do not report the attacks.

exposure.

for skin lesions.

**4. Control measures**

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

*Parasitology and Microbiology Research*

in a beetle [57].

the necessity for alternative control methods.

tion will require more precise analysis.

**3.3 Zoonotic risks**

harbored synanthropic populations [11]. Additionally, the same research

described that the *D. gallinae* populations associated with poultry farms belong to different genetic lineages [11]. In addition, recent research on genetic differences between *Ornithonyssus sylviarum* present in wild sparrow nests and layer houses in the USA indicated the absence of mite exchange [55]. However, wild bird nests located in the proximities of the hen house can act as a reservoir of mites and thus allow re-infestation. Mul et al. [56] performed a risk analysis in which poultry farmers and employees, followed by hen cadavers and manure aeration, represented the highest risks of introduction and spread of PRM in the farm. If the manure belts are shared amongst barns, they constitute a severe risk of spreading the PRM [56]. Rodents and insects are potential carriers of mites, and although the role of pests in the introduction and spread of PRM in layer farms has not been fully elucidated, a case of phoresy of *D. gallinae* has been described

In a recent questionnaire by free-range farmers in the UK, antiparasitics were reported as one of the three most commonly used medicines against PRM [41]. A recent scandal on the discovery of an unauthorized product in food-producing animals (Fipronil, C12H4Cl2F6N4OS) in contaminated eggs from farms in 45 countries worldwide. The concentration in the contaminated product did not reach toxic doses for humans, but a mediatic Public Health alert was raised, and a food fraud investigation was started by European authorities [58]. Only two compounds are specifically labeled to control PRM infestations while birds are present (Phoxim, C12H15N2O3PS and Spinosad, C41H65NO10 (A); C42H67NO10 (D)) by the European Union (EU), and recently a new compound (Fluralaner, C22H17Cl2F6N3O3) has been approved [59, 60]. Authorized products do not penetrate the whole egg but improper handling when breaking the shell can lead to food contamination [61]. Risks of residues of traditional and unlabeled pesticides entering the food chain are due to its presence in body tissues of hens that are slaughtered for human consumption [60]. A withdrawal period has been suggested for the skin tissue after application of Spinosad and Abamectin (C48H72O14 (B1a); C47H70O14 (B1b)), an acaricide with available formulations for spray application in some European countries, due to the detection of residues in this tissue [62]. The chemicals used to control PRM may also have adverse effects for workers directly exposed while applying the treatment. The limited availability of tools and the increase of resistance are forcing the farmers to turn to non-authorized products to face PRM infestations and underline

*D. gallinae* is known as a bird ectoparasite but it has low host specificity [16]. This lack of specificity allows the mite to feed on mammals, including humans, when the natural host is not available [6]. Human parasitosis due to PRM is called gamasoidosis or dermanyssosis. Skin erythematous papules are the usual clinical signs for gamasoidosis and urticarial lesions have been also described [6]. Skin lesions are usually pruriginous and can be distributed throughout the entire body, but are more frequently located in the arms, legs and the upper trunk [6]. Regarding human gamasoidosis associated with *D. gallinae*, two epidemiological scenarios are described: urban cases and occupational cases [6]. *D. gallinae* is the most commonly ectoparasite identified as the causal agent of gamasoidosis, but the cases assigned to *D. gallinae* can be misdiagnosed due to the difficulty of species determination for non-trained practitioners. The geographical expansion of other similar mite species such as *Ornythonyssus* spp. [63] due to climate change, host expansion and globaliza-

**238**

Occupational cases are those related to poultry workers. The infestation can occur both in professional workers and hobbyists. These mite attacks usually happen during the daytime, while the workers are handling birds, cages or collecting eggs or when cleaning the premises. High levels of mite infestation and lack of proper protective clothing increases the risk of mite bites. Despite the high prevalence of infestation in egg-laying farms and continued exposure of the workers to the PRM, the number of reports of occupational cases is limited [6, 64]. The low number of reported cases can be explained by the fact that the attacks occur under specific conditions (severe infestation and lack of protection) or because workers do not report the attacks.

Urban cases are not associated with poultry workers. These cases are usually linked to familiar homes or public buildings such as hospitals and halls. In these cases, synanthropic birds, generally pigeons, are the source of the infestation [6]. Most of them occur when the host has left the nest after the breeding season. At that moment, the mites search for a new host to obtain a bloodmeal. Recent investigations suggest the existence of a pigeon specific lineage (*D. gallinae* L1) that is more frequently involved in human gamasoidosis [65]. Skin lesions in urban cases tend to be more severe than those in occupational cases, basically due to extended exposure.

Reports of gamasoidosis are scarce but their frequency has increased in the recent years [6]. PRM gamasoidosis is still an underdiagnosed parasitosis mainly due to un-specific signs which do not lead the practitioners to a certain diagnosis and, generally, the fact that PRM bites cause only light to mild clinical symptoms, indistinguishable from other bug bites and do not put the patient in need of seeking medical assistance. Recently, the bacterial genera *Tsukamurella* has been identified as part of the microbiome of the PRM with an endosymbiotic relationship suggested [66]. *Tsukamurella* species are foremost saprophyte bacteria that have occasionally been identified as opportunistic organisms associated with postoperative infections [67]. This, and the avian pathogens listed earlier, together with reports of *D. gallinae* infestations in hospitals [68] highlight potential zoonotic risks associated with PRM. Thus, because of the potential vector role of PRM for zoonotic pathogens it should be included in routine medical differential diagnosis for skin lesions.
