Pesq. Vet. Bras. 31(11):981-984, novembro 2011

The role of ear of the genus Raillietia (: Raillietiidae) in otitis of domestic ruminants1

Fernando R.A. Ferry2*, João L.H. Faccini3 and Tetsuo Inada4

ABSTRACT.- Ferry F.R.A., Faccini J.L.H. & Inada T. 2011. The role of ear mites of the genus Raillietia (Acari: Raillietiidae) in otitis of domestic ruminants. Pesquisa Veterinária Brasileira 31(11):981-984. Departamento de Medicina Geral, Universidade Federal do Esta- - [email protected] do doThis Rio paper de Janeiro, presents EMC/CCBS, a hypothesis Hospital on the Universitário involvement Gaffrée of species e Guinle, of the Rua genus Mariz Raillietia e Bar Trouessartros 775, Tijuca, in the Rio pathology de Janeiro, of RJ parasitic 20270-004, otitis Brazil. in domestic E-mail: ruminants. The chelicerae and

lesions. The movable digits of the chelicerae accidentally injure the epithelium that lines theclaws ear of canal, the tarsi while are the structures claws of thatthe tarsicontribute perforate significantly the epithelium, towards allowing producing the mitesprimary to

the claws favor multiplication of the bacteria that inhabit the ear canal, resulting in typical casesaffix themselves of otitis. while feeding. The lesions in the epithelium caused by the chelicerae and INDEX TERMS: Raillietia, otitis, domestic ruminants.

RESUMO.- [O papel dos ácaros do gênero Raillietia INTRODUCTION (Acari: Raillietiidae) na otite de ruminantes domés- Mites of the genus Raillietia Trouessart, 1902 are parasites ticos.] Neste trabalho apresentamos uma hipótese para that inhabit the external ear canal and the external surfa- explicar o envolvimento dos ácaros do gênero Raillietia ce of the tympanic membrane of domestic and wild rumi- na patogênese da otite parasitária em ruminantes domés- nants. Three species of Raillietia have been described in ticos. As quelíceras e unhas dos tarsos são estruturas que R. auris, R. flechtmanni and R. caprae diagnosed only in cattle, the second in buffaloes and cattle, primárias no epitélio. Os dígitos móveis das quelíceras Brazil:and the third exclusively in goats (Faccini et .al. The 1992a, first Facwas- acidentalmentecontribuem significativamente causam injúria no para epitélio produzir que asreveste lesões o cini & Ribeiro 2008). canal auditivo, enquanto as unhas dos tarsos perfuram o Perforation of the tympanum, resulting in vestibular - disease, redness, ulceration and hemorrhage of the tissue that lines the ear canal, blockage of the ear canal by plugs epitélio para permitir a fixação dos ácaros durante sua ali- of paste-like wax, ataxia (due to rupture of the tympanic riasmentação. que habitam As lesões o nocanal epitélio auditivo, causadas resultando pelas quelíceras em casos membrane and lesions to the vestibular system), anore- típicose unhas de dos otite. tarsos favorecem a multiplicação das bacté xia, restlessness, unilateral facial paralysis, debilitation, hearing loss and head shaking have all been reported in TERMOS DE INDEXAÇÃO: Raillietia, otite, ruminantes domésticos. association with ear infestations [see Krametter-Fro- 1 Received on July 2, 2011. etscher (2006) for early literature citation]. Most of these Accepted for publication on August 18, 2011. clinicopathological signs have also been reported in cattle 2 Departamento de Medicina Geral, EMC/CCBS, Universidade Federal do infested with Raillietia - Estado do Rio de Janeiro (UNIRIO), Hospital Universitário Gaffrée e Guin- eds of Zebu (Nunes et al. 1980, Leite et al. 1989b). The association between spp. in Brazil,Raillietia predominantly spp. and bacteria in bre * Corresponding author: [email protected] - le,3 Rua Mariz e Barros 775, Tijuca, Rio de Janeiro, RJ 20270-004, Brazil. Departamento de Parasitologia , Instituto de Veterinária, Uni- arte et al. 1999) and rhabditiform nematodes (Duarte et al. versidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ 23890- 2001)(Leite ethave al. been1987) reported and that in between cases of Malassezia bovine otitis spp. in (DuBra- 4 Departamento de Biologia Animal, Instituto de Biologia, UFRRJ, BR 465 Mycoplasma spp. and Raillietia 000, Brazil. Fellow of CNPq. E-mail: [email protected] caprae in goats has been reported in Australia (Cottew & zil. The association between Km 7, Seropédica, RJ 23890-000, Brazil. 981 982 Fernando R.A. Ferry, João L.H. Faccini and Tetsuo Inada

For examination of the infested external ear canal, the material (Ribeiro et al. 1995) and in Mexico (Otero et al. 2009), whi- was prepared as described by Nunes & Nunes (1975), consisting leYeats Mycoplasma 1982), in thespp. United and Raillietia States (DaMassa auris and 1983), R. flechtmanni in Brazil - - initially of fixation in formaldehyde 10% and decalcification in ni ral thesis (Santos 2009). tric acid 5% for 47 days. After that, the material was embedded haveThe also objective been found of this in cattlepaper in was Brazil to present [unpublished a hypothesis docto in paraffin, microtomed and stained with hematoxylin and eosin. on the probable mechanisms involved in the feeding and RESULTS Raillietia and their asso- The morphological examination of the structures involved in ciation with the pathology of otitis in domestic ruminants. affixationThe morphology of species of R.of flechtmanni the genus and the association be- Fig.1C,D) of Raillietia flechtmanni permits a hypothesis to be tween Raillietia spp. and cattle were used as a model. madethe feeding on how process the process (chelicerae: of mechanical Fig.1A,B) injury and fixation to the epithe (tarsi:- lium of the host’s ear canal may develop. The third segment MATERIALS AND METHODS of the chelicerae (Fig.1B) is composed of the movable digit, - The specimens of Raillietia flechtmanni used in this study were sitioned dorsally. The movable digit is scythe-shaped, is arti- obtained from the external ear canal of cattle slaughtered at the culatedwhich is with positioned the second ventrally, segment and atthe its fixed basal digit, portion which and is haspo three fang-like projections in the distal portion (arrow). The establishedSanta Cruz industrialby Leite etslaughterhouse al. (1989a), which, (no longer in brief, in business) consists inof morphology of the movable digit suggests an adaptation for the city of Rio de Janeiro, Brazil, in accordance with the method- perforating and cutting the epithelium of the ear canal as sho- der pressure into the ear canal immediately following slaughter. wn in Figures 2A and 2B. With respect to the tarsus (Fig.1C,D), Theflushing mites the collected ears of werethe cattle stored with in closed 100ml jars, of watertransported injected to unthe laboratory and submitted to preparation for scanning electron claws are seen in R. flechtmanni (arrow). These structures are microscopy (SEM) in accordance with the method described by presentthe final on segment the eight of legsthe ofleg species of the mites,of Raillietia the presence. Figure 2C of sugtwo- gests that the claws may be used by the parasite to cling to the - epithelium of the ear canal while feeding. Ferry et al. (1994). The following sequence was carried out: first seriesthe mites of alcohol, were cleaned, dried at fixed the criticalin glutaraldehyde point in liquid and CO2, cleaned mounted in ul ontrasound; aluminum then supports post-fixed using with double-sided osmium tetroxide, adhesive dehydrated tape, metali in a- DISCUSSION AND CONCLUSION Although the chelicerae of Raillietia spp. are adapted to produced. perforate and cut the epithelium, the species included in zed with gold and analyzed, after which SEM micrographies were

A B

C D

Fig.1 (A) Lateral view of the gnathosoma of a female of Raillietia flechtmanni, showing the chelicerae (arrow). (B) Figure 1 shows the left chelicerae in greater detail. The mobile digit is shaped like a scythe when seen from the side and has three pointed projections (arrow). (C) Extremity of the tarsus of a female of Raillie- tia flechtmanni , viewed from the side, showing the claw (arrow). (D) Extremity of the tarsus of a female of Raillietia flechtmanni, ventral view, showing the two claws (arrow).

Pesq. Vet. Bras. 31(11):981-984, novembro 2011 The role of ear mites of the genus Raillietia (Acari: Raillietiidae) in otitis of domestic ruminants 983

A B Fig.2 (A) Histological section of the external ear canal of a cow, sho- wing a female of Raillietia sp. in a medial saggital section. The - bly used when the mite was feeding. The epithelium around the gnathosoma is shown on the left. The fixative fluid was proba material (me) can be seen on the slide containing the epithelial material,gnathosoma below is shedding and to the (arrow). left of Thethe mite,fibrin-like, occupying eosinophilic a ridge formed in the shedding epithelium (e). A claw (a) can be seen to the left, embedded in the epithelial surface. A diffuse in- B) Histological section of the external ear canal of a cow, showing Raillietiaflammatory sp. infiltratein a cross is section visible atover the the level entire of the epithelium. gnathosoma. ( Note that the chelicerae (q) are in contact with the epithelium (e), which shows degenerated cells. Note the red blood cells

- C inside-like and the purulent. capillaries Sensory dilated palpiby the (p). inflammatory (C) Histological reaction. section The of the external ear canal of a cow, showing a tarsus of Raillietia sp. eosinophilic material (me) that surrounds the mite is fibrin eosinophilic material (me) surrounding it. The lamina propria is hemorrhagic and thick. Epithelium (e). Figures are not to scale. embedded in the epithelium and compressing it. The tarsus (p) is shown in the center of the image. Note the fibrin-like, purulent the external ear canal during the feeding process would be - accidental albeit common, since the chelicerae are in direct tingthis genusof the mitesapparently for microscopic do not feed examination, specifically ononly tissue an am or- contact with the epithelium (Figure 2A). ber-colored,blood, since duringcheese-like the process mass was of clarificationfound inside and the mounmites, As in parasite infestations by Raillietia spp., the claws of which was suggestive of earwax rather than tissue or blood the tarsi of some species of the Rhinonyssidae, nasal para- from the host. Nevertheless, the complex structure of the sites of birds, are used by the mites to cling to the nasal epi- gnathosoma of the mites of the genus Raillietia suggests thelium, perforating and tearing the tissue of the nasal ca- that these mites may predigest food prior to ingesting it, vity of birds (Feider & Mironescu 1972). The lesions caused which would justify the absence of host tissue inside the in the epithelium of the ear canal and the tympanic mem- mites. Therefore, the type of food ingested by these mites brane of cattle and other domestic ruminants are probably the result of the combined action of the chelicerae and the Feeding behavior in mites ranges from claws of the tarsi, the former involved directly in the feeding still remains to be confirmed. Haemogamasus ambulans, process, while the claws of the tarsi are used by the mites to fecesgeneralized and living feeders or dead such as (Furman 1958), to very epithelium that lines the ear canal and the tympanic mem- which feeds on the fluid orDermanyssus dried blood of gallinae vertebrates,, a blood flea- affix themselves during feeding. The resultant injury to the areas by resident microorganisms, consequently evolving feederspecific mites feeders rarely such penetrate as the skin of vertebrate hosts. tobrane otitis. facilitates Leite et the al. infiltration(1987) reported and colonization having found of 28these di- With-sucking respect mite. to According the feeding to habits Furman of the (1958), ear mites generalized of the fferent types of bacteria in the auditory system of cattle genus Raillietia, the species may be included somewhere infected by Raillietia auris, those of the genera Proteus and Pseudomonas being the most commonly found. Both the- species included in the genus Raillietia probably feed basi- se genera and also Corynebacterium pyogenes are always callybetween on earwax, the two microorganisms extremes of Furman’s that live classification. on the surface The of the epithelium of the ear canal and residue from the she- dding epithelium. Perforation of the epithelium that lines speciesfound in of association Malassezia with, which chronic consisted inflammatory of M. globosa processes, (12), whereas Duarte et al. (1999) presumptively identified 24

Pesq. Vet. Bras. 31(11):981-984, novembro 2011 984 Fernando R.A. Ferry, João L.H. Faccini and Tetsuo Inada

M. slooffiae (5), M. furfur manni various species of Mycoplasma inside R. caprae, R. auris and 95-96. sp.n. (Acari: Gamasida). Mem. Inst. Oswaldo Cruz 87(Suppl.1): R. flechtmanni suggests the (5) possibility and (2). Finally, that this the species finding may of - be involved in the transmission of mycoplasmosis in goats, Raillietia Trouessart em Faccinibovinos J.L.H., no Brasil.Fonseca Revta A.H., Bras. Costa Parasitol. A.L. & Leite Vet. R.C. 1(2):109-110. 1992b. Distribuição ge as documented in Australia (Cottew & Yeats 1982), USA Facciniográfica J.L.H. e prevalência & Ribeiro V. das 2008. espécies Raillietia do capraegênero (Acari: Raillietiidae) and Psoroptes ovis (Acari: Psoroptidae) in the ears of goats in the state of (Otero et al. 2009). The hypothesis of a possible associa- tion(DaMassa between 1983), Mycoplasma Brazil (Ribeiro spp. and et species al. 1995) of Raillietia and Mexico is Feider Z. & Mironescu I. 1972. Une modalité particulière de perforer la feasible, since R. auris is a parasite commonly found in the muqueuseRio de Janeiro, nasale, Southeast utilisée Brazil. par les Revta acariens Bras. de Parasitol. la famille Vet. Rhinonyssidae 1(1):59-61. ear canal of cattle (Faccini et al. 1992b) and furthermore Trouessart, 1895. Acarologia 16(2):21-31. Santos et al. (2009) recently found seven species of Myco- Ferry F.R.A., Lanfredi R.M., Faria S.M., Inada T. & Faccini J.L.H. 1994. Méto- plasma in the ear canal of clinically normal cattle slaughte- do de preparo de ácaros do gênero Raillietia Trouessart (Acari: Gama- sida) para estudo ao microscópio eletrônico de varredura. Revta Bras. Parasitol. Vet. 3(1):65-68. Faccini et al. (1992b) reported a prevalence of Raillietia Furman D.P. 1959. Feeding habits of symbiotic mesostigmatid mites of aurisred for human consumption in Brazil. - mammals in relation to pathogen-vector potentials. Am. J. Trop. Med. ber of mites per animal may range from 1 to 146. Since Hyg. 8(1):5-12. each mitein Brazilian has two beef chelicerae cattle of and 85-100% eight tarsi and (withthat the two num cla- Krametter-Froetscher R., Leschnik M., Hoegler S., Loewenstein M. & Baum- ws on each tarsus), making a total of 16 claws per mite, it gartner W. 2006. Occurrence of the ear-mite Raillietia auris in cattle in is reasonable to speculate that the chelicerae and the tarsi Austria. Vet. J. 171(1):186-188. constitute important structures in the pathogenesis of pa- Leite R.C., Nunes V.A., Coelho A.M.B., Chiloff M.A.G. & Nunes I.J. 1987. Pa- rasitic otitis associated with species of Raillietia. Further Raillietia auris studies are necessary to investigate the probable effect of (Leidy, 1872) Trouessart, 1902 (Acari: Mesostigmata). II. Achados bacte- rianos.tologia Arq. da infecção Bras. Med. do Vet. conduto Zoot. auditivo39(2):325-332. de bovinos por additional causes of injury to the epithelium of the ear ca- Raillietia Trouessart, nalthe inenzymes ruminants. present in the salivary secretion of mites as Leite R.C., Faccini J.L.H. & Costa A.L. 1989a. Avaliação de uma técnica in Both direct observations of the chelicerae and tarsal Leitevivo R.C., para Nunes medir V.A., a infestação Faccini J.L.H.,por ácaros Lopes do C.W.G., gênero Nunes I.J. & Costa A.C. claws, and histological pictures of parasitism lead us to 1989b.1902 (Acari) Aspectos em clínicosbovinos. da Mem. Raillietiose Inst. Oswaldo bovina. Cruz Arqs 84(4):309-311. Univ. Fed. Rural Rio conclude that the lesions in the epithelium caused by spe- de Janeiro 12(1/2):83-91. cies of Raillietia Nunes V.A. & Nunes I.J. 1975. Técnica de exame post-mortem do sistema of bacteria resulting in otitis. auditivo aplicada ao estudo de otites em bovinos. Arq. Esc. Vet. UFMG allow the colonization and multiplication 27(2):155-161. Acknowledgements.- The authors are grateful to Dr. Vera Nunes Alva- Nunes V.A., Nunes I.J., Santos M.N., Chiloff M.A.G. & Silva J.M.L. 1980. Pato- renga for having supplied the histological slides of the external ear canal Railletia auris (Leidy, 1872) of cattle, and to Dr. Reinalda Marisa Lanfredi (deceased) for her help with Trouessart, 1902 (Acari:Mesostigmata). Aspectos macroscópicos. Arq. the images taken from the scanning electron microscope. Esc.logia Vet. da infecçãoUFMG 32(3):325-331. do ouvido de bovinos por Otero J.N., Jaramillo L.M., Miranda E.M.R., Navarro J.A.H. & Quintero M.T.M. REFERENCES 2009. Association of Raillietia caprae with the presence of Mycoplasmas in the external ear canal of goats. Prev. Vet. Med. 92(1/2):150-153. Cottew G.S. & Yeats F.R. 1982. Mycoplasmas and mites in the ear of clini- cally normal goats. Aust. Vet. J. 59(3):77-81. Ribeiro V.R., Nascimento E.R., Faccini J.L.H., Nascimento M.G.F. & Lignon Raillietia caprae DaMassa A.J. 1983. Prevalence of mycoplasmas and mites in the external coletados do conduto auditivo externo de caprinos. Revta Bras. Med. auditory meatus of goats. Calif. Vet. 37(10):10-13. Vet.G.B. 17(1):122-124.1995. Presença de Micoplasmas em exemplares de Duarte E.P., Melo M.M., Hahn R.C. & Hamdan J.S. 1999. Prevalence of Ma- lassezia spp. in the ears of asymptomatic cattle and cattle with otitis in Mycoplasma spp. (Mollicutes: Mycoplasmataceae) em conduto auditivo Santosde bovinos S.B. 2009. e em Imunoperoxidase Raillietia spp. (Gamasida: e métodos Raillietiidae). moleculares Tesena detecção de Douto de- Duarte E.R., Melo M.M. & Hamdan J.S. 2001. Epidemiological aspects of rado, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ. 76p Brazil. Med. Mycol. 37(3):159-162. bovine parasitic otitis caused by Rhabditis spp. and/or Raillietia spp. in Santos S.B., Nascimento E.R., Faccini J.L.H. & Barreto M.L. 2009. Potentially pathogenic Mycoplasmas in the external ear canal of clinically normal Faccini J.L.H., Leite R.C. & Costa A.L. 1992a. Description of Raillietia flecht- the state of Minas Gerais, Brazil. Vet. Parasitol. 101(1):45-52. cattle in southeast Brazil: First report. Braz. J. Microbiol. 40(3):455-457.

Pesq. Vet. Bras. 31(11):981-984, novembro 2011