Abstracts

Introduction

Oestrus ovis (Diptera: Oestridae), the sheep nasal bot fly, is a cosmopolitan parasite whose larvae develop in the head sinuses and nasal passages of sheep and goats in all sheep-farming areas worldwide. The female fly is viviparous and deposits larvae in or around the nostrils of its host; these early first instars attach to the mucous membrane inside the nasal cavities, change to second instars, and move up to the sinuses where they develop into mature third instars, which are expelled by pupation in the soil (ZUMPT, 1965Zumpt P. Myiasis in man and animals in the Old World. London: Butterworths; 1965. PMid:14272962.). The duration of this parasitic portion of the life cycle varies considerably: from a few weeks to several months, depending on the season and climatic conditions (COBBETT; MITCHELL, 1941Cobbett NG, Mitchell WC. Further observations on the life cycle and incidence of the sheep bot, Oestrus ovis, in New Mexico and Texas. Am J Vet Res 1941; 2: 358-366.). Clinical respiratory signs such as seromucous or purulent nasal discharge, frequent sneezing, and dyspnea may severely impair the health of affected animals (DORCHIES et al., 1998Dorchies P, Duranton C, Jacquiet P. Pathophysiology of Oestrus ovis infection in sheep and goats: a review. Vet Rec 1998; 142(18): 487-489. PMid:9612915. http://dx.doi.org/10.1136/vr.142.18.487
http://dx.doi.org/10.1136/vr.142.18.487... ).

O. ovis can thrive in different environments and has adapted to the climate prevailing wherever sheep are kept (HORAK, 1977Horak IG. Parasites of domestic and wild animals in South Africa. I. Oestrus ovis in sheep. Onderstepoort J Vet Res 1977; 44(2): 55-64. PMid:614524.), and this ability to adapt to different environments allows for the natural persistence of infestation and makes it difficult to control it (ALCAIDE et al., 2005Alcaide M, Reina D, Frontera E, Navarrete I. Epidemiology of Oestrus ovis (Linneo, 1761) infestation in goats in Spain. Vet Parasitol 2005; 130(3-4): 277-284. PMid:15899552. http://dx.doi.org/10.1016/j.vetpar.2005.03.022
http://dx.doi.org/10.1016/j.vetpar.2005.... ). Several researches have demonstrated the high prevalence of ovine oestrosis in numerous areas all over the world, e.g. Zimbabwe (PANDEY, 1989Pandey VS. Epidemiology of Oestrus ovis infection of sheep in the highveld of Zimbabwe. Vet Parasitol 1989; 31(3-4): 275-280. http://dx.doi.org/10.1016/0304-4017(89)90077-0
http://dx.doi.org/10.1016/0304-4017(89)9... ), France (YILMA; DORCHIES, 1991Yilma JM, Dorchies P. Epidemiology of Oestrus ovis in southwest France. Vet Parasitol 1991; 40(3-4): 315-323. http://dx.doi.org/10.1016/0304-4017(91)90111-8
http://dx.doi.org/10.1016/0304-4017(91)9... ), Italy (CARACAPPA et al., 2000Caracappa S, Rilli S, Zanghi P, Di Marco V, Dorchies P. Epidemiology of ovine oestrosis (Oestrus ovis Linné 1761, Diptera: Oestridae) in Sicily. Vet Parasitol 2000; 92(3): 233-237. http://dx.doi.org/10.1016/S0304-4017(00)00317-4
http://dx.doi.org/10.1016/S0304-4017(00)... ), Spain (ALCAIDE et al., 2003Alcaide M, Reina D, Sánchez J, Frontera E, Navarrete I. Seasonal variations in the larval burden distribution of Oestrus ovis in sheep in the southwest of Spain. Vet Parasitol 2003; 118(3-4): 235-241. PMid:14729171. http://dx.doi.org/10.1016/j.vetpar.2003.09.021
http://dx.doi.org/10.1016/j.vetpar.2003.... ) and Greece (PAPADOPOULOS et al., 2010Papadopoulos E, Chaligiannis I, Morgan ER. Epidemiology of Oestrus ovis L. (Diptera: Oestridae) larvae in sheep and goats in Greece. Small Rumin Res 2010; 89(1): 51-56. http://dx.doi.org/10.1016/j.smallrumres.2009.12.004
http://dx.doi.org/10.1016/j.smallrumres.... ). Oestrosis is commonly found in sheep in Brazil, but there are few studies on the epidemiology of this parasite and most of them are restricted to the south region of the country, where favorable climatic conditions are observed throughout the year. The prevalence of oestrosis in sheep was of 85.4% in Bagé (RIBEIRO et al., 1990Ribeiro VLS, Oliveira CMB, Branco FPJA. Prevalência e variações mensais das larvas de Oestrus ovis (Linneus, 1761) em ovinos no município de Bagé, RS, Brasil. Arq Bras Med Vet Zootec 1990; 42(3): 211-221.) and in Encruzilhada do Sul, both in the State of Rio Grande do Sul; the mean intensity of infestation was 23.8 larvae (OLIVEIRA et al., 1999Oliveira CMB, Oliveira LO, Torres JR. Oestrus ovis larvae distribution in the head of naturally infested sheep. Arq Fac Vet UFRGS 1999; 27(2): 87-92.). In the State of Santa Catarina, O. ovis infestation intensity was greater during the spring and summer months and no larvae were recovered from tracer sheep when the temperature was lower than 9 °C (RAMOS et al., 2006Ramos CI, Bellato V, Souza AP, Avila VS, Coutinho GC, Dalagnol CA. Epidemiologia de Oestrus ovis (Diptera: Oestridae) em ovinos no Planalto Catarinense. Cienc Rural 2006; 36(1): 173-178. http://dx.doi.org/10.1590/S0103-84782006000100026
http://dx.doi.org/10.1590/S0103-84782006... ).

The first study on O. ovis epidemiology in the State of São Paulo was carried out recently in Botucatu, where prevalence was 50% with mean intensity of 16.8 larvae per animal, with higher infestation rates during spring and summer (SILVA et al., 2012Silva BF, Bassetto CC, Amarante AFT. Epidemiology of Oestrus ovis (Diptera: Oestridae) in sheep in Botucatu, State of São Paulo. Rev Bras Parasitol Vet 2012; 21(4): 386-90. PMid:23295819. http://dx.doi.org/10.1590/S1984-29612012000400008
http://dx.doi.org/10.1590/S1984-29612012... ). The State of São Paulo presents different climatic conditions in each of its regions and small sheep farms are found in most areas of this State. Therefore, detailed research on the epidemiology of parasitic infestation is required to recommend the best strategies of oestrosis prophylaxis in small ruminants. This study aimed to determine O. ovis prevalence in slaughtered sheep from five counties of Central region of the State of São Paulo, Brazil.

Materials and Methods

The heads of 139 slaughtered sheep were examined from July 2009 to February 2010. The animals were originated from Itápolis, Ibitinga, Borborema, Guarantã and Tapinas, municipalities in the Central region of the State of São Paulo. The monthly amount of sheep slaughtered in an abattoir in the municipality of Itápolis was variable and the heads of all slaughtered animals were examined. Most of the sheep were ≤ 1 year old (89.2%), with predominance of Santa Ines breed (80.6%) and its crosses with Dorper breed. Information on prior antiparasitic treatment and sheep management were not available.

Climate data from Itápolis were obtained from a study performed by the Center of Meteorological and Climate Research Applied to Agriculture (CEPAGRI, 2012).

The heads of the slaughtered sheep were separated from the carcasses, put into individual plastic bags to avoid transfer of larvae from one head to another and to collect those that came out of the nasal cavities. They were transported to the laboratory inside a cool box with ice. The heads were cut open along their longitudinal and sagittal axes. All larvae present in the nasal cavity (nasal passage, septum, middle meatus and conchae) and paranasal sinus (frontal and maxillary) were carefully examined; all larvae found were collected and counted. The larvae were preserved in 70% alcohol and identified according to their stage of development based on the descriptions by Zumpt (1965)Zumpt P. Myiasis in man and animals in the Old World. London: Butterworths; 1965. PMid:14272962. and Capelle (1966)Capelle KJ. The occurrence of Oestrus ovis L. (Diptera: Oestridae) in the bighorn sheep from Wyoming and Montana. J Parasitol 1966; 52(3): 618-621. PMid:5942536. http://dx.doi.org/10.2307/3276337
http://dx.doi.org/10.2307/3276337... .

1.Statistical analyses

Spearman's rank correlation coefficient was estimated between larval burden and climatic conditions (mean temperature and rainfall) using Minitab release 11.

Descriptive statistical analyses were performed in agreement withBush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
http://dx.doi.org/10.2307/3284227... . The following terms were used:

Prevalence: the number of hosts infested with O. ovis larvae divided by the number of hosts examined;

Intensity of infestation: the number of O. ovislarvae in a single infested host;

Mean intensity of infestation: the total number of O. ovis larvae found divided by the number of hosts infected with that parasite.

Results

The maximum and minimum amount of heads examined per month was 26 in July and August 2009 and 9 in October 2009, respectively. Of the 139 heads examined, 19 (13.7 %) were infested with O. ovis larvae with minimum and maximum prevalence of the 7.7% in August 2009 and 20.0 % in February 2010, respectively (Table 1). No O. ovis larva was recovered in October 2009, coinciding with the lowest number of heads examined. The monthly mean intensity of infestation ranged from 1 to 10.2 larvae per infested head, with general mean intensity of 4.5 larvae per infested head. Means of temperature and rainfall in Itápolis are presented in Table 2. The average annual rainfall was 1416.5 mm and the average annual temperature for this period was 22.9 °C. No significant correlations were observed between monthly larval numbers and climatic variables, i.e., mean temperature and rainfall (P > 0.05).

Of the total of 85 larvae, 21.2% was L1, while L2 and L3 represented 37.6% and 41.2%, respectively. The sheep heads collected were derived mainly from young animals (≤ 1 year old), but the prevalence ofO. ovis larvae was similar between the age groups (Table 3).

Discussion

The prevalence of O. ovis infestation (13.7%) in this study was lower than those reported in similar studies carried out in other countries such as France, where 65% of sheep was infested with O. ovis larvae (YILMA; DORCHIES, 1991Yilma JM, Dorchies P. Epidemiology of Oestrus ovis in southwest France. Vet Parasitol 1991; 40(3-4): 315-323. http://dx.doi.org/10.1016/0304-4017(91)90111-8
http://dx.doi.org/10.1016/0304-4017(91)9... ); or in Sicily, with 55.8% of prevalence (CARACAPPA et al., 2000Caracappa S, Rilli S, Zanghi P, Di Marco V, Dorchies P. Epidemiology of ovine oestrosis (Oestrus ovis Linné 1761, Diptera: Oestridae) in Sicily. Vet Parasitol 2000; 92(3): 233-237. http://dx.doi.org/10.1016/S0304-4017(00)00317-4
http://dx.doi.org/10.1016/S0304-4017(00)... ); and Turkey, with 40.6% (ARSLAN et al., 2009Arslan M, Kara M, Gicik Y. Epidemiology of Oestrus ovis infestations in sheep in Kars province of north-eastern Turkey. Trop Anim Health Prod 2009; 41(3): 299-305. PMid:18523857. http://dx.doi.org/10.1007/s11250-008-9190-x
http://dx.doi.org/10.1007/s11250-008-919... ). Higher prevalence was also observed in other Brazilian studies: 85.4% in the south region of the country in sheep exposed to natural infestation for one year (RIBEIRO et al., 1990Ribeiro VLS, Oliveira CMB, Branco FPJA. Prevalência e variações mensais das larvas de Oestrus ovis (Linneus, 1761) em ovinos no município de Bagé, RS, Brasil. Arq Bras Med Vet Zootec 1990; 42(3): 211-221.) and 50% prevalence in tracer sheep in Botucatu, State of São Paulo, Brazil (SILVA et al., 2012Silva BF, Bassetto CC, Amarante AFT. Epidemiology of Oestrus ovis (Diptera: Oestridae) in sheep in Botucatu, State of São Paulo. Rev Bras Parasitol Vet 2012; 21(4): 386-90. PMid:23295819. http://dx.doi.org/10.1590/S1984-29612012000400008
http://dx.doi.org/10.1590/S1984-29612012... ).

Despite the lower prevalence observed in the present study, O. ovis larvae were present in all experimental months, except in October 2009, coinciding with the lowest number of sheep heads examined. Probably, if more heads had been monthly examined, there would have been greater chances to find infested sheep, as observed in studies carried out in other countries, where sheep are slaughtered in greater amounts and more often. In Sicily, for instance, 70 heads were examined per month (CARACAPPA et al., 2000Caracappa S, Rilli S, Zanghi P, Di Marco V, Dorchies P. Epidemiology of ovine oestrosis (Oestrus ovis Linné 1761, Diptera: Oestridae) in Sicily. Vet Parasitol 2000; 92(3): 233-237. http://dx.doi.org/10.1016/S0304-4017(00)00317-4
http://dx.doi.org/10.1016/S0304-4017(00)... ), whereas in the present study the maximum number of sheep heads examined per month was 26. In the State of São Paulo, Brazil, large slaughterhouses specialized in cattle, poultry and pigs are common; however, the slaughtering of sheep, in general, is restricted to small abattoirs with less often routine, making it difficult to collect a large number of heads to be examined.

Several factors can influence O. ovis epidemiology, such as sheep management practices and particular climatic conditions. The low prevalence of oestrosis in these animals may have been influenced by previous treatment with drugs, such as macrocyclic lactones, which are usually used for the prophylaxis of infections by gastrointestinal nematodes and act against O. ovislarvae instars (DORCHIES et al., 1996Dorchies P, Cardinaud B, Fournier R. Efficacy of moxidectin as a 1% injectable solution and a 0.1% oral drench against nasal bots, pulmonary and gastrointestinal nematodes in sheep. Vet Parasitol 1996; 65(1-2): 163-168. http://dx.doi.org/10.1016/0304-4017(95)00930-2
http://dx.doi.org/10.1016/0304-4017(95)0... ,1997Dorchies P, Alzieu JP, Cadiergues MC. Comparative curative and preventive efficacies of ivermectin and closantel on Oestrus ovis (Linné 1758) in naturally infected sheep. Vet Parasitol 1997; 72(2): 179-184. http://dx.doi.org/10.1016/S0304-4017(97)00052-6
http://dx.doi.org/10.1016/S0304-4017(97)... ; LUCIENTES et al., 1998Lucientes J, Castillo JA, Ferrer LM, Peribáñez MA, Ferrer-Dufol M, Gracia-Salinas MJ. Efficacy of orally administered ivermectin against larval stages of Oestrus ovis in sheep. Vet Parasitol 1998; 75(2-3): 255-259. http://dx.doi.org/10.1016/S0304-4017(97)00168-4
http://dx.doi.org/10.1016/S0304-4017(97)... ). The influence of anthelmintic treatment inO. ovis epidemiology was also observed in Botucatu, where reduction in the infestation of tracer sheep coincided with the treatment of flocks with macrocyclic lactones (SILVA et al., 2012Silva BF, Bassetto CC, Amarante AFT. Epidemiology of Oestrus ovis (Diptera: Oestridae) in sheep in Botucatu, State of São Paulo. Rev Bras Parasitol Vet 2012; 21(4): 386-90. PMid:23295819. http://dx.doi.org/10.1590/S1984-29612012000400008
http://dx.doi.org/10.1590/S1984-29612012... ).

Among the climatic factors that influence oestrid fly activity, temperature, light intensity and wind are considered the most important, but in the case of O. ovis, temperature is the main factor affecting the larvipositional activity of gravid females (CEPEDA-PALACIOS; SCHOLL, 2000Cepeda-Palacios R, Scholl PJ. Factors affecting the larvipositional activity of Oestrus ovis gravid females (Diptera: Oestridae). Vet Parasitol 2000; 91(1-2): 93-105. http://dx.doi.org/10.1016/S0304-4017(00)00265-X
http://dx.doi.org/10.1016/S0304-4017(00)... ). Although the heads of the slaughtered sheep were examined during each of the eight months, the climatic conditions are likely to be favorable to O. ovis activity throughout the year in the sheep origin region, where the mean of temperature is around 22 °C and maximum and minimum averages are around 16.3 and 29.6 °C, respectively.

It is noteworthy that mostly L2 and L3 O. ovis larval instars were recovered in this study. Probably because the climatic conditions were suitable to endogenous larval development and L1 were able to change into L2 in a short period of time. Larvae in sheep head can have a rapid development, reaching maturity in three weeks (COBBETT; MITCHELL, 1941Cobbett NG, Mitchell WC. Further observations on the life cycle and incidence of the sheep bot, Oestrus ovis, in New Mexico and Texas. Am J Vet Res 1941; 2: 358-366.). In the State of Santa Catarina, Brazil, larger L3 numbers were also recovered from tracer sheep (RAMOS et al., 2006Ramos CI, Bellato V, Souza AP, Avila VS, Coutinho GC, Dalagnol CA. Epidemiologia de Oestrus ovis (Diptera: Oestridae) em ovinos no Planalto Catarinense. Cienc Rural 2006; 36(1): 173-178. http://dx.doi.org/10.1590/S0103-84782006000100026
http://dx.doi.org/10.1590/S0103-84782006... ), but probably because those animals were exposed to infestation for 28 days and were then housed for 20 more days before slaughter, giving larvae enough time to complete their development.

In conclusion, all different O. ovis larvae instars were recovered from the animals slaughtered in this study, which demonstrates the existence of favorable climatic conditions for the fly activity and larval development of O. ovis in sheep raised in the Central region of the State of São Paulo.

Acknowledgements

The authors are grateful to the slaughterhouse workers for their fundamental cooperation during the study. Bruna F. Silva received financial support by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) and Alessandro F.T. Amarante was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil).

References

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