Spotlight on avian pathology: red mite, a serious emergent problem in layer hens

ABSTRACT

Dermanyssus gallinae, the poultry red mite, is currently the most important ectoparasite of the egg laying industry worldwide with an expanding global prevalence. As a blood-feeder, it causes anaemia and severe welfare issues to the hens and it is a major cause of economic losses. It is also a vector for Salmonella species, avian influenza and potentially for other vector-borne pathogens. Paradoxically, there is a notable lack of funding for research into poultry red mite and an urgent need for effective and safe control strategies, sustainable therapies, prophylactics and integrated pest management.

KEYWORDS:

• Parasite
• laying hens
• economic losses
• welfare
• research
• control

Background

Poultry red mite (PRM) is a tiny (<1 mm) blood-feeding ectoparasite of the phylum Acarina, order Mesostigmata and, unlike other mites of poultry, it feeds mainly at night and for short periods from a few minutes to a maximum of two hours. The rest of the time, mites reside in multi-stage colonies in cracks and crevices, on the undersides of ledges, perches, bars and nest boxes: essentially, anywhere that is out of reach so chickens cannot peck and eat them. Signs of PRM infestation include hen restlessness and aggression, intense scratching and feather pecking, matted and dirty feathers, marked reluctance to enter hen houses and nesting boxes, and anaemia that in severe cases causes death. In addition to these serious welfare issues, PRM infestation causes reduced egg production and egg size, and is estimated to be directly responsible for economic losses of around €231 m per year in Europe (van Emous, 2017).

PRM has a global distribution. Its impact has increased significantly in the past decade and it is now at epidemic levels in many parts of the world. Recent reports estimate on-farm prevalence of 25% in Iran (Rezaei et al., 2016), 24% in Tunisia (Gharbi et al., 2013) and 88% in China (Wang et al., 2010). In Europe, infestation rates average more than 80% (Sparagano et al., 2009; George et al., 2015) and, whilst levels in the USA are much lower, there are many web-based reports of significant recent increases. The success of PRM is due to its short reproductive life cycle and the ability to survive at a distance from the host, which means that numbers accumulate rapidly in hen houses. It may also reflect favourable conditions in modern layer production for parasite survival, including increased size of layer houses, high flock size and density, maintenance of steady temperatures, lighting and humidity, and a move away from conventional cages to more complex enriched cage and free-range units (Sparagano et al., 2014).

Current control of PRM

Strategies to control PRM increasingly use integrated pest management approaches that include general disinfection and good hygiene practices, reduced contact with wild birds, avoidance of stress and overcrowding, control of ventilation and temperature and innovative barn design (Mul et al., 2017). There is a limited choice of chemical acaricides available and farms often use these in combination/rotation with non-chemical treatments that aim to reduce mite numbers through desiccation, suffocation, trapping or predation. A growing body of evidence indicates that populations of Dermanyssus gallinae have substantial genetic resistance to the commonly applied classes of drugs including the much-used synthetic pyrethroids (Beugnet et al., 1997; Marangi et al., 2009). There are also concerns regarding the potential for accumulation of acaricide residues in poultry meat and eggs (Marangi et al., 2012). A new fluralaner-based product EXZOLT^®, introduced recently to Europe, is the first systemic acaricide for the control of PRM, administered via drinking water (Thomas et al., 2017). For all products, it is important to understand compatibilities between treatments; for instance, biological control products containing PRM predatory mites such as Androlis^®, containing Androlaelaps casalis mites, are susceptible to destruction by acaricides and desiccants, so must not be used concurrently.

What about vaccines?

Approaches to vaccine development centre on the concept of identifying mite antigens that induce circulating antibodies in hens that can damage mites when ingested with the blood meal. PRM feed and reach engorgement more rapidly than other haematophagous pests and hens are barely exposed to PRM antigens during feeding so do not naturally generate potent immunoprotective responses (Harrington et al., 2010). It is therefore difficult to identify highly immunogenic vaccine targets in the red mite. Some candidate antigens have been proposed and tested based on their similarity to promising vaccine antigens from other arthropod species (Harrington et al., 2009; Wright et al., 2016). Others have been identified by painstaking “fractionate and vaccinate” approaches that use empirical logic to separate out and test the vaccine efficacy of partially purified protein mixtures extracted directly from mites (Bartley et al., 2015; Makert et al., 2016; Bartley et al., 2017).

Other research areas

Despite the importance of PRM, the research community is very small; searching PubMed for “Dermanyssus gallinae” (13 June 2018) found 258 publications including just 16 in 2017 (six on prevalence/modelling, four on fluralaner, two on aromatic oil repellents, two on human infestation, one each on vaccines and microbiomes). Given that populations of PRM show differing levels of resistance to several acaricides, and the huge difficulties encountered in controlling this pest, an understanding of resistance mechanisms, and the frequency of resistant genotypes in populations of PRM is essential. Genome plasticity allows for the rapid selection and dissemination of mutations that have a selective advantage to a parasite. For PRM mite, this could be important in future escape from vaccines as well as for acquisition and spread of resistance to new and existing drugs. There is thus a small but emerging focus on the molecular characterization of mite sequences (for example, Schicht et al., 2014) as well as on work to characterize the structure of PRM populations and trace dissemination routes based on population genetics (Oines & Brannstrom, 2011; Roy & Buronfosse 2011).

In addition to the severe impact that PRM has on laying hens, there are two additional concerns driving new research. The first is the role that PRM has in transmitting other infectious agents, including avian influenza (Sommer et al., 2016) or bacteria (Hubert et al., 2017), between birds, and potentially to other hosts. A variety of pathogens have been isolated from red mites (see George et al., 2015 for a full review) and testing the vectorial capacity of mites to transmit infections is an important and active area of One Health research. The second is the direct impact that Dermanyssus mites can have on human health. There are numerous reports of humans being bitten by D. gallinae mites with signs that range from local swelling and itching, usually in people who work directly with infested chicken flocks, to gamasoidosis, a serious dermatitis that can persist for several months with flare-ups of urticaria (hives) and papulosquamous lesions (papules and scales). Recent morphological and molecular characterization of mites, isolated in the vicinity of people having gamasoidosis lesions, has confirmed that these belong to a cryptic lineage of D. gallinae associated specifically with pigeons and other columbiformes (Pezzi et al., 2017), a finding that fits with the epidemiology of gamasoidosis which is generally found in urban environments linked to roosting pigeons or doves. The precise distribution of this cryptic lineage, and information on whether there are similar zoonotic lineages in other geographical locations, remain to be determined.

Conclusion

PRM is a serious welfare and economic threat to the poultry layer industry that is increasing in prevalence throughout Europe and the rest of the world. Concerted action is required to increase the quantity of research carried out on this destructive pest and to develop additional effective control measures.

Acknowledgements

The authors would like to thank COST for its support of the COREMI project for “Improving current understanding and research for sustainable control of the poultry red mite Dermanyssus gallinae” (www.coremi.eu).

Disclosure statement

No potential conflict of interest was reported by the authors.