Volume 2 No. 2 JULY 2011 • pages 41-49 Malaysian Journal of Veterinary Research

SHEEP OESTROSIS ( OVIS, DIPTERA: OESTRIDAE) IN DAMARA CROSSBRED

GUNALAN S.1, KAMALIAH G.1, WAN S.1, ROZITA A.R.1, RUGAYAH M.1, OSMAN M.A.1, NABIJAH D.2 and SHAH A.1 1 Regional Veterinary Diagnostic Laboratory Kuantan, Jalan Sri Kemunting 2, Kuantan, Pahang 2 KTS Jengka Pusat Perkhidmatan Veterinar Jengka Corresponding author: [email protected]

ABSTRACT. Oestrosis is a worldwide the field and the larvae were discovered infection caused by the larvae of in the tracheal region. The larvae was the (Diptera, Oestridae), confirmed as Oestrus ovis using the that develops from the first to the third appropriate keys for identification by stage larvae. This is an obligate parasite Zumpt. The carcass showed pulmonary of the nasal and sinus cavities of sheep edema with severe congestion of the lungs and . The Oestrus ovis larvae elicit accompanied by frothy exudation in the clinical signs of cavitary myiasis seen as bronchus. There were also signs of serious a seromucous or purulent nasal discharge, atrophy (heart muscle) and mild enteritis frequent sneezing, incoordination and (intestine histopathological examination dyspnea. Myiasis in an incidental host showed, there was pulmonary congestion may have biological significance towards and edema, centrilobular hepatic necrosis, medical and public health importance if renal tubular necrosis and myocardial the incidental host is man. This infection sarcocystosis. The sheep also showed can result in signs of generalized disease, chronic helminthiasis and Staphylococcus causing serious economic losses in spp. was isolated from organ specimens. sheep and reared for meat and dairy Oestus ovis infection is rare in Malaysia, production. Due to the large numbers of as such this case posed as an unusual case small ruminants imported into Malaysia for investigation. from countries which are endemic with Keywords: Oestrus ovis, Damara oestrosis, precautionary measures should sheep, larvae, respiratory sign, myiasis be exercised to prevent this infection from establishing here. In 2009, there was a INTRODUCTION report of respiratory distress (pneumonic sign) accompanied by high mortality in Larvae of belonging to the Oestridae Damara sheep that was imported from Family and Subfamily include Australia. Investigations showed the several genera which cause obligatory presence of Oestrus ovis larvae in affected myiasis in Artiodactyla and Equidae, sheep. The post mortem was conducted in infesting the nasopharyngeal cavities and

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internal organs during their migration. southern Europe an unusually large number Oestrosis is a regional myiasis caused by of different spesies of bot fly suggests larvae of the fly Oestrus ovis (Diptera, a high degree of oestrid biodiversity. It Oestridae), that develop from the first to seems related to the movement of domestic the third stage larva which are obligate in association with migrating parasites of the nasal and sinus cavities of human populations in southern Europe sheep and goats. over thousands of years (Otranto et al., The larvae are obligatory parasites of 2006). Oestrus ovis can thrive in different nasal and sinus cavities of sheep and goats environments (Horak, 1977; Breev et (Zumpt, 1965). The female are larviparous, al., 1980; Pandey and Ouhelli, 1984) and depositing a number of first-instar larvae can overwinter in a diapauses state, as on the edge, or just inside the nostrils of larvae in the sinu-nasal passages of the sheep and goats. The peculiar feature of the host (Cobbett and Mitchell, 1941; Horak, O. ovis female is that it may larviposit while 1981). The ability to adapt in a different still in flight. In their normal development environment allows the natural persistence in sheep, the larvae migrate to the nasal of infestation and the difficulties for its mucosa and nasal and frontal sinuses control. Recent surveys have demonstrated where they undergo 2 moults. After 2 to 12 the high prevalence of caprine Oestrosis in months, the fully grown third instar larvae numerous areas all over the world, 48.3% are expelled and pupate on the ground. in India (Jagannath et al., 1989), 31.3% This parasite is found worldwide and in Mexico (Martinez et al., 1992), 4 % in it is especially widespread in Mediterranean Argentina (Trezeguet, 1996) and 53.8% countries of Europe and Africa (Pandey, in Nigeria (Biu and Nwosu, 1999). So far, 1989; Dorchies et al., 2000; Alcaide et al., there is no case report of Oestrus ovis in 2003; Papadopoulos et al., 2006). Despite sheep in Malaysia, a tropical rainforest the high prevalence in these countries country where large imports of sheep and and severity of infection, many breeders goats for breeding and sheep production is and veterinary practitioners still remain carried out regularly. unaware of the importance of these parasitic The O. ovis larvae elicit clinical agents. The subfamily Oestrinae mutation signs of cavitary myiasis as a seromucous is still unknown. During the last decade, or purulent nasal discharge, frequent some work on genetics, pathophysiology sneezing, incoordination and dyspnea. This and immunology was done in France, infection can result in signs of generalized Italy, Mexico and Spain and a review was disease, causing serious economic losses published by Hall and Wall (1995). in sheep and goat herds reared for meat and Extensive use of macrocyclic lactones dairy produce. The development of larvae is modifying parasitic diversity (Otranto in the nasal-sinus cavities can cause severe and Colwell, 2008), whereas in some areas of clinical signs such as breathing difficulties,

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nasal discharge and emaciation, together higher in sheep than in goats after either with the annoyance caused by the adult natural or artificial infestation (Duranton flies. This may lead to production and et al., 1996). Little is known about the economic losses (Dorchies et al., 1998, development of immunity but it is possible 2003). Oestrus ovis can severely impair that some animals are immunodeficient. breathing because it induces tenacious Respiratory disease are common in sheep nasal discharge to which grass, straw and and goats and O. ovis has been suggested dust adhere, clogging the air passages. to have an immunosuppressive effect (with Moreover, the infection may be complicated consequent association with respiratory by sinusal tumour and lung abscesses pathogens) (Dorchies et al., 1993). (Dorchies et al., 1993). Despite the fact that both Furthermore, several cases of species can be hosts of this parasite, ophthalmic and naso-pharnygeal myiasis infection prevalence and larval burdens have been reported in humans, indicating are generally higher in sheep than in goats a public health issue in certain areas (Dar after either natural or artificial infestation et al., 1980; Masoodi and Hosseini, 2003). (Duranton et al., 1996, Papadopoulos et al., The opthalmomyiasis produced in man by 2006), and this is taken to indicate higher O. ovis larvae is restricted to conjunctivae, susceptibility in sheep. sclera, eyelids, and lachrymal duct (external opthalmomyiasis) or the eye ball History of Case Report (internal opthalmomyiasis) (Hadani et al. and Dar et al., 1980; Stulting and Meyer, In 2009, a case of respiratory distress 1981; Omar et al., 1988; Amir et al., 1993). accompanied by severe mortality was Myiasis in an incidental host which may reported in Damara sheep that was have biological significance and can also recently imported into Malaysia from a be of medical and public health importance neighbouring country. The report involved if the incidental host is a man. Myiasis 25 heads of 7-month-old, female Damara caused by O. ovis may be considered as crossbred sheep imported in stages over a an occupational disease of shepherds or period of 4-5. They were sent for breeding farmers who usually keep their sheep and purposes to a commercial sheep farm. goats in close proximity to their dwellings The sheep were reared using an intensive (Amir et al., 1993). system where animals were fed grass and This infection can result in generalized pellets. Initially, a few animals exhibited disease, causing serious economic losses severe respiratory signs indicative of in sheep and goat reared for meat and dairy suspected pneumonia. Soon after, the produce. Despite the fact that both animal sheep showed signs of respiratory distress species can be host of this parasite, infection such as loud, noisy breathing, poor body prevalence and larval burdens are generally scores (severe emaciation), ill thrift and

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were unproductive with poor kidding foul smell. There was also serous atrophy rates. About 10% mortality was reported of the heart coronary fat and generalized initially. The flock of sheep were treated moderate congestion in all vital organs. with antibiotics by veterinary personnel, Based on the post mortem and clinical and subsequently one of the treated sheep signs exhibited by this flock of sheep, the died 4 days after treatment prompting a differential diagnosis made were bacterial postmortem. The post mortem exhibited pneumonia, viral pneumonia, verminous findings of frothy discharge with foamy pneumonia, chronic helminthiasis and exudation (especially in the bronchus) malnutrition problem. with whitish nodules in the trachea. The most significant finding was the discovery MATERIALS AND METHOD of larvae crawling in the tracheal region toward the bronchus region. The tracheal From the post mortem, the samples were rings showed some congestion. There submitted for further examination and was severe congestion of lung lobes disease diagnosis to the Regional Veterinary (involving apex region and diaphragm Diagnosis Laboratory. The samples sent lobes) and evidence of whitish patches and were lung, liver, kidney, heart and spleen. foamy appearances on the lung surface. Specimens such as intestine, fecal sample Besides that, there was bile impression and larvae in normal saline were sent on the mildly swollen liver. Furthermore, to the laboratory. All other specimen of congestion on the serosal surface of organs went through detailed examination the small intestines and capillaries of for gross lesions and bacteriology as well mesentery was observed. The ingesta in as virology investigation. Simultaneously, the intestine was dark coloured and had a larvae and faeces were sent for parasitology

Figure 1. Migration of larvae in the lung bronchus & tissue

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examination. For histopathology with 100 e.p.g. for Strongyles spp. with no examination, the samples such as lung, larvae recovered from faeces. liver, heart and kidney tissue were sent in The lung surface showed pneumonic the 10% buffered formalin for examination. lesions along with presence of whitish patches and foamy appearances. The RESULTS kidney and liver were congested with no significant gross lesions in the heart and The laboratory diagnosis based on spleen. bacteriology and virology, did not reveal Histological examination showed that any significant result. Bacteriology the lung alveolar had collapsed, and the findings indicated no bacterial growth in lung was oedematous and congested. There the lung and heart tissue. However, there was evidence of congestion, infiltrations were presence of normal flora growth or of polymorphonuclear inflammatory opportunistic organisms growth such as cells (PMNs) in alveolar interstitium and Escherichia coli from the intestine sample proteinaceous material inter alveolar. and Staphylococcus spp. from the liver There was cardiac muscle congestion and tissue. There was no viral isolation from fragmentation. In the cardiac tissue, the the pooled samples using the tissue culture cyst of the Sarcocystis spp. parasite was technique. present in the intra cardiac muscle. In the As for the parasitology examination, liver tissue, there was presence of necrosis Faecal Egg Count (FEC) detected the and ballotment of hepatocytes, widening presence of helminths eggs and oocysts of of sinusoid space and red blood cells were coccidia. The faecal sample was positive found in between sinusoidal space. In the renal tissue, presence of picnotic nucleus of

Figure 2. Lung alveolar collapsed, Figure 3. Severe congestion, infiltration of oedematous few PMNs and congested (X10, H&E) in alveolar interstitium (X10, H&E)

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Figure 4. Sarcocystis spp. formed in intra- Figure 5. Infiltration of RBCs, necrosis of cardiac muscle tubular and presence of rbc (X100, H&E) epithelia cells (X100, H&E) tubules indicating mild necrosis effect and problem. There was no significant bacterial urine sediments were seen. There was also growth except Staphylococcus spp. from a material such as fibrin appearing in the the organ specimen as the sheep has been renal tubular tissue. treated. In summary, there was severe DISCUSSION pulmonary congestion and mild pneumonia due to parasitic infestation and secondary Based on the clinical signs, pathology and bacterial infection. In this case, only one parasitology findings, a case of Oestrosis mature larvae (L3) of Oestrus ovis was due to Oestrus ovis was confirmed. No recovered from the sheep during post significant bacteria were isolated from mortem; this could be due to the possibility any organs. This may be due to prompt that in adult sheep, many L1 are destroyed antibiotic treatment that reduces the by immune reactions, as indicated by Bart chances for bacterial isolation. In reviewing and Minar (1992) and Marchenko and the histopathology findings, there was Marchenko (1989). The first stage larva (L1) severe pulmonary congestion, moderate to stage is more commonly found in sheep less severe pulmonary oedema involving lung. than 1 year of age due to the existence of a Centrilobular hepatic necrosis had taken period of hypobiosis. The larvae also may place in the liver tissue. Moderate to severe adapt to local climatic conditions while renal tubular necrosis was found in the in the L1 stage during hypobiosis period. kidney tissue. Myocardial sarcocystosis Consequently, the antigenic stimulation with mild congestion in heart muscle. The related to reinfestations and to the moulting sheep also showed chronic helminthiasis of the larvae in the upper respiratory cavities

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induces a strong immune reaction. First hypobiotic period (Cobbett and Mitchell, stage larvae are very sensitive to immune 1941; Horak, 1981). The stocking density reactions as indicated by Bart and Minar of the flock will also influence the infection (1992) and Marchenko and Marchenko of O. ovis. (1989, 1994) and larvae could be destroyed Differing degrees of clinical signs during moulting, resulting in low numbers can be classified as mildly affected, of third stage larvae. Furthermore, the low moderately, as well as severely affected. prevalence of third stage larvae could be More parasites recorded in the presence due to the rate of development and the brief of purulent discharge is in agreement duration of third stage larvae in the sinuses with previous observation in sheep (Abo- before they are expelled. Shehada et al., 2000). Dorchies et al. Usually older animals are more (1998) described pathology consistent likely to have heavier infestations, which with hypersensitivity responses in the is similar to the data for sheep reported by affected animals. Contrary to this case, Abo-Shehada et al. (2000.) Sheep may be no sheep has been exhibiting purulent predisposed to this problem as reported discharge, except mucopurulent discharge. by Dorchies et al. (1998) who reported Nevertheless, some authors associated that there might be an “ovine” strain and a such responses with immunopathology, “caprine” strain. Despite the fact that both and suggested that the presence of O. ovis animal species can be hosts of this parasite, larvae have an immunosuppressive effect. infection prevalence and larval burdens The hypobiotic survival of larvae during are generally higher in sheep than in goats the hot or dry season is associated with after either natural or artificial infection a sharp decrease in the severity of local (Duranton et al., 1996; Papadopoulus et al., reactions until the first instar larvae 2006), and this is taken to indicate higher resume their development. Furthermore, susceptibility in sheep. Besides that, many the pathological changes were associated factors influence the larval populations with burdens of live and dead larvae, of O. ovis found in the skull cavities of suggesting that they played an active role goats; the most important is climate which in the pathology. However, the pathological affects the number of larviparous females effects are often underestimated because to which the animal have been exposed owners and veterinarians are used to (Yilma and Dorchies, 1993). This may seeing the infection. But, the study of be due to the weather condition at high natural and experimental infections has altitudes which are not favourable for the provided information about the evolution presence and development of O. ovis, as of the disease and its pathophysiology. described Bergeaud et al. (1994). When Hypersensitivity is involved; the numbers environmental conditions are adverse, of mast cells and eosinophils increase but larvae cease their development during the changes in IgE have only recently been

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examined. And, there will be important abattoir should be carried out to locate inflammatory cell infiltration against the the larval stage in upper respiratory larvae in the sinu-nasal cavities as reported tract, determine the infestation rate and by Dorchies et al. (1998) and Nguyen et al. prevalence in goat or sheep. The Oestrus (1999). ovis has immunosuppressive effects with In this case, no dewormer was consequent association with respiratory administered prior to importation and upon pathogen, (Dorchies et al., 1993). The arrival. Only the antistress medication was naso-sinusal myiasis caused by O. ovis given to the sheep. Prompt use of avermectin is common in both sheep and goats, and (e.g. Ivermectin/Doramectin injection) is likely to be of importance to animal may have reduced the O. ovis burden in the production and welfare. sheep together with other sheep parasites or helminthiasis. Prognosis must be guarded CONCLUSION if the animal showed severe pneumonia and breathing difficulties. Antibiotics may In conclusion, this is a case of Oestrosis be needed should animal become pyrexic. caused by Oestrus ovis infection in the In terms of diagnosis, the newly imported upper respiratory tract with histopathology sheep must be examined with endoscope findings of severe pulmonary congestion and faecal larvae examination to determine and mild pneumonia in the crossbred the possibility of carrying Oestrus ovis. A Damara sheep. The mortality and complete serological diagnosis for other morbidity in the flock is low as no apparent concurrent diseases can also be conducted correlation was noted with other sheep as severe Oestosis can cause a reduction in which exhibited clinical signs and there immunity and hence predispose the animal was no recovery of larvae from the rest to other disease. Serology for oestrosis of the animals. This disease caused by also can be done and is available. Usually Oestrus ovis larvae needs further study the seropositive animal correlated with in terms of chronobiology and prevalence flock size, as many other authors have (seroprevalence rate), potential risk factors reported (Gupta et al., 1985; Marchenko associated with the myiasis in sheep, and Marchenko, 1989; Ribeiro et al., 1990). seasonal variations in the life cycle and the This may be due to possible higher risk of association between larvae and the weather infestation and reinfestation among herds condition. The pathophysiology of Oestrus of greater number of susceptible animals ovis in sheep and hypersensitivity results in that are crowded together. an immunodeficient state will also need to In accordance with O. ovis infection, be studied. In Malaysia, this is a rare case proper identification / morphology of myiasis which needs further attention diagnosis of this larvae using Zumpt, 1965 especially for prevention and control of an keys is important. More surveillance in

48 Volume 2 No. 2 JULY 2011 Malaysian Journal of Veterinary Research emerging new infection which may be a 11. Dorchies, P. et al., 1998. Pathophysiology of Oestrus ovis infection in sheep and goats: a review. Vet. Rec. 142: 487- threat to local livestock farming. 489. 12. Dorchies, Ph. et al., 1999. Oestrose du mouton et de la chevre (Oestrus ovis Linne 1761) en Afrique: resultants ACKNOWLEDGEMENT d’ une enquete sur 3204 serums provenant de neuf pays. Rev. Med. Vet. 150: 463-466. 13. Dorchies, Ph et al., 2000. Oestrus ovis (Linne 1761) in The author would like to thank the sheep and goats in south of France. Vet. Parasitol. 8: 269- ex-Director and MVK Kuantan staff 273. 14. Dorchies, P. et al. 2000. Prevalence and larval burden of (pathology, parasitology and bacteriology Oestrus ovis (Linne 1761) in sheep and goats in northern section) as well as Veterinary Officer from Mediterranean region of France. Vet. Parasitol. 88: 269- 273. TAC Jengka for their help and expertise in 15. Gupta, J.R. et al., 1985. Bionomics of Oestrus ovis (sheep diagnosing this case. Last but not least, the nasal fly). Indian Vet. Med. J. 9: 71-75. 16. Horak, I.G. et al., 1981. The similarity between arrested Institute of Medical Research (Entomology development in parasitic nematodes and diapauses in Unit) and Dr. Krishanamoorthy (Consultant . J.S. Afr. Vet.Assoc. 52: 299-303. 17. Jagannath, M.S. et al., 1989. Factors influencing Oestrus Entomologist) in assisting with the the ovis infestation in sheep and goats. Curr.res. 18, 118-119. identification of the larvae. 18. Mantovani et al., 1966. Ricerche sui parassiti degli ovine della Marsica. Parassitologia 8: 103-110. 19. Mantovani, A. et al., 1964. Prime ricerche sulle REFERENCES parassitosi delle pecore delle Marsica. Atti soc. It. Sci. Vet. 8: 441-442. 20. Marchenko, V.A.m Marchenko, V.P., 1989. Survival of 1. Abo-Shehada, M.N. et al., 2000. Age and seasonal Oestrus ovis larvae depends on the state of the immune variations in the prevalence of O.ovis larvae among sheep system of sheep. Parazitologiya 2: 129-133. in northern Jordan. Prev. Vet. Med. 47, 205-212. 21. Murguia, M et al., 2000. Detection of Oestrus ovis and 2. Alcaide, M. et al., 2003. Seasonal variations in the burden associated risk factors in sheep from the central region of distribution of Oestrus ovis in sheep in the southwest of Yucatan, Mexico. Vet. Parasitol 8: 73-78. Spain. Vet. Parasitol. 118: 235-241. 22. Marsodi, M. et al., 2003. The respiratory and allergic 3. Amr, Z.S. et al., 1993. Opthalmomyiasis externa caused manifestation of human myiasis caused by larvae of the by Oestrus ovis L. in the Aljoun area of northern Jordan. sheep bot fly (Oestrus ovis): a report of 33 pharnygeal Ann. Trop. Med. Parasitol. 87: 259-262. cases from southern Iran. Ann. Trop. Med. Parsitol. 97, 4. Berrag, B. et al., 1996. Parasites of goats in the north of 75-81. Morocco. In: Proceedings of the IFS Workshop, Burkina 23. Omar, M.S. et al., 1988. External opthalmomyiasis due Faso. Parasitol. Res. Afr. 287-306. to the sheep nostril bot fly larva Oestrus ovis in Saudi 5. Biu, A.A. et al., 1999. Incidence of Oestrus ovis Arabia. Ann. Trop. Med. Parasitol., 82, 221-223. infestation in Borno-White Sahel goats in the semi-arid 24. Trezeguet, M.A., 1996. Prevalencia de enfermedades en zone of Nigeria. Vet. Res. 30: 109-112. 4000 majadas caprinas en los departamentos Atamisqui, 6. Breev, K.A. et al., 1980. Influence of constant and Ojo de Agua, Que brachos y Salavina province de variable temperature on pupal development of the sheep Santiago del Estero, Republica de Argentina. Vet. bot fly Oestrus( ovis L.). Folia Parasitol. 27: 350-365. Argentina 13, 485-489. 7. Cobbett, N.G. et al., 1941. Further observations on the 25. Yilma, J.M. 1993. Essays d’ infestations experimentales life cycle and incidence of the sheep bot, O.ovis, in New de I’ agneau par larves I d’ o.ovis. bull. Soc. France Mexico and Texas. Am. J. Vet. Res. 2: 358-366. Parasitol. 43, 43-47. 8. Dar, M.S. et al., 1980. Opthalmomyiasis caused by the 26. Zumpt, F. 1963. Opthalmomyiasis in man with special sheep nasal bot Oestrus ovis (Oestridae) larvae, in the reference to the situation in Southern Africa. Sout Afr. Benghazi area of Eastern Libya. Trans. Roy. Soc. Trop. Med J. 37, 425-428. Med. Hyg. 74: 303-306. 27. Zumpt, P., 1965. Myiasis in Man and Animals in the Old 9. Dorchies, Ph. et al., 1993. Prevalence of lung abscesses World, Butterworth et Co., London, 257 pp. and interstitial pneumonia in ovine Oestrosis. Vet. Rec. 133: 325. 10. Dorchies, P. et al., 1997. L’oestrus ovine: revue. Rev. Med. Vet. 148:565-574.

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