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Prevalence and larval burden of Oestrus ovis (Linné 1761) in sheep and goats in northern mediterranean region of France
Veterinary Parasitology 88 (2000) 269–273
Prevalence and larval burden of Oestrus ovis (Linné 1761) in sheep and goats in northern mediterranean region of France Ph. Dorchies ∗ , J.P. Bergeaud, G. Tabouret, C. Duranton, F. Prevot, Ph. Jacquiet Laboratoire de Parasitologie UMR 959, Physiopathologie des maladies infectieuses et parasitaires des Ruminants, Ecole Nationale Vétérinaire, 23, chemin des Capelles, F-31076 Toulouse Cedex 03, France Received 4 May 1999; accepted 20 October 1999
Abstract A slaughterhouse survey to determine prevalence and larval burden of Oestrus ovis larvae in sheep and goats was performed monthly during one year in Pézenas, South of France, northern mediterranean region. A total of 1303 sheep and goat heads were selected at random. O. ovis larvae were found in 274 sheep out of 631 (43.4%), and the prevalence rate varied from 14.3% in February to 65% in October. The mean number of larvae in infected sheep heads was 10.86 with 9.24 L1, 0.91 L2 and 0.71 L3. One hundred and ninety-one goats out of 672 were infected (28.4%), and the prevalence rate varied from 6.25% in September to 47.1% in April. In infected goat heads, the mean parasitic burden was 5.35 with 4.04 L1, 0.73 L2 and 0.58 L3. These results confirm worldwide observations indicating that the prevalence and the parasitic burdens are less in goats than in sheep. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Oestrus ovis; Sheep; Arthropoda; Goat; Prevalence; France
1. Introduction Oestrus ovis is a well-known parasite of the nasal cavities and adjoining sinuses of sheep and goats (Zumpt, 1965). In countries with hot and dry climate, this widespread small ruminant myiasis severely impairs health, making breathing difficult when the nasal discharge ∗ Corresponding author. Tel.: +33-5-6119-3871; fax: +33-5-6119-3944. E-mail address: [email protected] (P.. Dorchies).
0304-4017/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 9 9 ) 0 0 2 1 5 - 0
270
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
becomes caked with dust. Some sheep and goats develop mouth breathing, which interferes with grazing and rumination. Subsequently this local naso-sinusal infection induces lung abcesses (Dorchies et al., 1993) and signs of general disease with emaciation which may result in death. Many surveys have been done in sheep and some in goats, but few of them have compared rates of infection in sheep and goats living in the same area. In France, oestrosis is a major economic threat to sheep producers, yet comprehensive data on the epidemiology in goats are lacking. According to breeders, goats are not infected and oestrosis is only a sheep disease. The aim of this study was to investigate the aspects of the epidemiology of O. ovis infection in a region where it would be possible to obtain heads of sheep and goats from the same slaughterhouse in order to compare their infection rates in the same climatic area.
2. Materials and methods 2.1. Animals and study site Regular biweekly visits to the slaughterhouse of Pézenas (Hérault, south of France close to the Mediterranean sea: 43◦ 220 N, 3◦ 240 E) allowed the recovery of 1303 heads: 631 from sheep and 672 from goats. All of these animals were more than 12 months old and originated from the south-east of France. 2.2. Examination procedure The cranial examination procedure used has been validated previously (Yilma and Dorchies, 1991). Briefly, sagittal sections of each head were made and larvae were collected from the five major sites (nasal cavities, septum, middle meatus, conchae and sinuses). After all the heads of a given batch were processed, larvae were counted and identified to instar under a stereomicroscope for using the keys of Zumpt (1965). 2.3. Statistical analysis Comparisons between sheep and caprine O. ovis prevalences were performed with the chi-square test (Stat ITCF Software) and comparisons between ovine and caprine O. ovis larval burdens with the non-parametric Kruskall Wallis and Mann–Whitney test (Simstat Software).
3. Results Due to the recent problems of B. S. E. and Scrapie, it is now very difficult to perform slaughterhouse surveys of small ruminant heads in France. This explains why some results are missing (goats for November).
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Table 1 Monthly prevalences and mean larval burdens
Number of heads per month Sheep Goats Number of larval positive heads Prevalence
Mean larval burdens
Sheep Goats
Jan Feb Mar Apr May Jun
Jul
Aug Sep
Oct
Nov Dec
Total
40 42 168 66
41 60
87 70
61 91
55 71
68 32
24 13
64 16
70 75
40 39 NDb 10
631 672
14 60
15 14
31 33
23 26
26 8
26 7
11 2
29 1
46 20
23 24 ND 2
274 191
6 18
Sheep 35 14.3 36.6 35.6 37.9 47.3 38.2 45.8 45.8 65 57.5 61.5 43.4 Goats 35.7 27.3 23.3 47.1 28.6 11.3 21.9 15.4 6.3 26.7 ND 20 28.4 Difference NS NS NS NS NS <0.001 NS 0.06 0.004 <0.001 – 0.018 <0.001 Sheep SDa Goats SD Difference
7.9 4.8 6 7 NS
27.3 52c 9.2 7.1 0.06
9.8 7 6.7 3.9 NS
5.4 5.2 4.1 3 NS
6 4.5 2.7 1.7 NS
3.6 3 4.8 2.9 NS
6.4 5 4.6 3.1 NS
4.4 3.3 3.5 1.4 NS
20.2 50c 6 2.8 0.012
17.4 15.1 5.4 3.7 0.043
13.3 13.8 10.9 14.5 12.4 14.7 ND 5.5 5.35 2.2 3.5 – 0.017 0.019
SD = Standard Deviation. ND = not done. c These two very important standard deviations are due only to one sheep for each month harbouring more than 200 larvae. a
b
Table 1 shows that out of the total of 631 heads of adult sheep examined, 274 (43.4%) were found to be infected with O. ovis larvae, and 191 (28.4%) out of 672 heads of adult goats. The mean monthly infection rate varied from 14.3 to 65% for sheep and from 6.25 to 47.1% for goats. The difference in infection rates between sheep and goats is significant (p < 0.0001). The mean larval burdens in infected animals were 10.87 for sheep with 9.24 L1, 0.91 L2 and 0.71 L3. In goats, the mean parasitic burden was 5.35 with 4.04 L1, 0.73 L2 and 0.58 L3. The difference between sheep and goats was also significant (p = 0.0195) for this parameter. Percentages of first, second and third instars are reported in Fig. 1 for sheep and Fig. 2 for goats for each month. 4. Discussion In the northern mediterranean climatic conditions and region of this survey, the first and second instars of O. ovis are present in sheep throughout the year, but the L2 occur in low numbers from September to February. In this case, the hypobiotic L1 accumulation in sheep as observed previously is not so obvious (Yilma and Dorchies, 1991). The larval burdens of all instars are closer to those observed in Tunis where L3 were also present all year round indicating a continuous cycle of parasite development (Kilani et al., 1986). Compared with previous results obtained in the south of France (Yilma and Dorchies, 1991),where the climate is colder and altitudes higher than in Pézenas, it appears that the
272
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
Fig. 1. Percentage distribution of the different instars in sheep.
cycle of L1 to L2 and L3 begins earlier during the winter, as early as January. The relative percentages of L1 decrease until May or June, then increasing again reaching 100% in goats and 99% in sheep in September. This study clearly indicates that O. ovis larvae are less prevalent in goats than in sheep. The life cycle of the parasite appears to develop faster in goats during summer, with less L1 in goats than in sheep. These results confirm those of the literature (Chhabra and Ruprah, 1976; Horak and Butt, 1977a,b; Belem and Rouille, 1988; Gabaj et al., 1993). In countries where surveys have been done in sheep and goats, the prevalence of oestrosis and the
Fig. 2. Percentage distribution of the different instars in goats.
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
273
arithmetic mean parasite burdens are consistently higher in sheep than in goats: 17.1 in sheep and 6.6 in goats. Finally this survey reveals that O.ovis is present in goats even when clinical signs are less obvious than those observed in sheep. Serological surveys conducted in many countries confirm a more extensive ELISA reaction in sheep than in goats (Dorchies et al., 1999). Mast cells and eosinophils, in the mucosæ of the upper respiratory tract are quantitatively more numerous in sheep than in goats (Nguyen et al., 1999). These observations are confirmed by the epithelial proliferation measured by Ki 67 epitope (Nguyen et al., 1998). Roughly, these parameters could appear to be linked, i.e., the greater the numbers of instars, the greater the humoral and cellular reactions in sheep. It has been observed that when a parasite is developing in a non-specific host, the reaction to it may be stronger than in the specific host who is more tolerant because of previous exposure. The results of this survey on O. ovis burdens in sympatric sheep and goats may lead to a new approach of the host–parasite relationship between this parasite and sheep and goats. Acknowledgements The authors are indebted to Doctor Bellocq, Chief of meat inspection in Pézenas slaughterhouse and Doctor Garcin, head of the Veterinary Services from Hérault, for their very kind help in the achievement of this survey. References Belem, A.M.G., Rouille, D., 1988. Oestrose des petits ruminants au Burkina. Faso. Rev. Elev. et Méd. Vét. Pays Trop. 41, 59–64. Chhabra, M.B., Ruprah, N.S., 1976. Observations on the incidence and biology of Oestrus ovis L. Indian Vet. J. 53, 180–184. Dorchies, Ph., Yilma, J.M., Savey, J., 1993. Lung involvment in ovine Oestrosis: prevalence of lung abscesses and intertitial pneumonia. Vet. Rec. 133, 325. Dorchies, Ph., Prevot, F., Duranton, C., Bergeaud, J.P., Akakpo, J., Pangui, L.J., Missohou, A., Deconinck, P., Ouatara, L., Roger, F., Achi-Yaba, L., Dia, M., Jacquiet, Ph., 1999. Oestrose du mouton et de la chèvre (Oestrus ovis Linné 1761) en Afrique: résultats d’une enquête sur 3204 sérums provenant de neuf pays. Rev. Méd. Vét. 150, 463–466. Gabaj, M.M., Beesley, W.N., Awan, M.A., 1993. Oestrus ovis myiasis in Libyan sheep and goats. Trop. Anim. Health Prod. 25, 65–68. Horak, I.G., Butt, M.J., 1977a. Parasites of domestic and wild animals in South Africa I. Oestrus ovis in sheep. Onderst. J. Vet. Res. 44, 55–64. Horak, I.G., Butt, M.J., 1977b. Parasites of domestic and wild animals in South Africa II. Oestrus ovis in goats. Onderst. J. Vet. Res. 44, 65–68. Kilani, M., Kacem, H.H., Dorchies, Ph., Franc, M., 1986. Observations sur le cycle annuel d’Oestrus ovis en Tunisie. Rev. Méd. Vét. 137, 451–457. Nguyen, V.K., Delverdier, M., Jacquiet, Ph., Dorchies, Ph., 1998. Expression tissulaire de l’épitope Ki-67 dans le compartiment épithélial de la muqueuse nasale du mouton et de la chèvre infestés naturellement par Oestrus ovis (Linné 1761). Rev. Méd. Vét. 149, 1109–1113. Nguyen, V.K., Jacquiet, Ph., Bergeaud, J.P., Duranton, C., Prévot, F., Dorchies, Ph., 1999. Réactions cellulaires des muqueuses nasales et sinusales des chèvres et des moutons à l’infection naturelle par Oestrus ovis Linné 1761 (Diptera: Oestridés). Parasite 6, 141–149. Yilma, J.M., Dorchies, Ph., 1991. Epidemiology of Oestrus ovis in southwest France. Vet. Parasitol. 40, 315–323. Zumpt, P., 1965. Myiasis in Man and Animals in the Old World. Butterworths, London, 257 pp.
Prevalence and larval burden of Oestrus ovis (Linné 1761) in sheep and goats in northern mediterranean region of France Ph. Dorchies ∗ , J.P. Bergeaud, G. Tabouret, C. Duranton, F. Prevot, Ph. Jacquiet Laboratoire de Parasitologie UMR 959, Physiopathologie des maladies infectieuses et parasitaires des Ruminants, Ecole Nationale Vétérinaire, 23, chemin des Capelles, F-31076 Toulouse Cedex 03, France Received 4 May 1999; accepted 20 October 1999
Abstract A slaughterhouse survey to determine prevalence and larval burden of Oestrus ovis larvae in sheep and goats was performed monthly during one year in Pézenas, South of France, northern mediterranean region. A total of 1303 sheep and goat heads were selected at random. O. ovis larvae were found in 274 sheep out of 631 (43.4%), and the prevalence rate varied from 14.3% in February to 65% in October. The mean number of larvae in infected sheep heads was 10.86 with 9.24 L1, 0.91 L2 and 0.71 L3. One hundred and ninety-one goats out of 672 were infected (28.4%), and the prevalence rate varied from 6.25% in September to 47.1% in April. In infected goat heads, the mean parasitic burden was 5.35 with 4.04 L1, 0.73 L2 and 0.58 L3. These results confirm worldwide observations indicating that the prevalence and the parasitic burdens are less in goats than in sheep. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Oestrus ovis; Sheep; Arthropoda; Goat; Prevalence; France
1. Introduction Oestrus ovis is a well-known parasite of the nasal cavities and adjoining sinuses of sheep and goats (Zumpt, 1965). In countries with hot and dry climate, this widespread small ruminant myiasis severely impairs health, making breathing difficult when the nasal discharge ∗ Corresponding author. Tel.: +33-5-6119-3871; fax: +33-5-6119-3944. E-mail address: [email protected] (P.. Dorchies).
0304-4017/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 9 9 ) 0 0 2 1 5 - 0
270
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
becomes caked with dust. Some sheep and goats develop mouth breathing, which interferes with grazing and rumination. Subsequently this local naso-sinusal infection induces lung abcesses (Dorchies et al., 1993) and signs of general disease with emaciation which may result in death. Many surveys have been done in sheep and some in goats, but few of them have compared rates of infection in sheep and goats living in the same area. In France, oestrosis is a major economic threat to sheep producers, yet comprehensive data on the epidemiology in goats are lacking. According to breeders, goats are not infected and oestrosis is only a sheep disease. The aim of this study was to investigate the aspects of the epidemiology of O. ovis infection in a region where it would be possible to obtain heads of sheep and goats from the same slaughterhouse in order to compare their infection rates in the same climatic area.
2. Materials and methods 2.1. Animals and study site Regular biweekly visits to the slaughterhouse of Pézenas (Hérault, south of France close to the Mediterranean sea: 43◦ 220 N, 3◦ 240 E) allowed the recovery of 1303 heads: 631 from sheep and 672 from goats. All of these animals were more than 12 months old and originated from the south-east of France. 2.2. Examination procedure The cranial examination procedure used has been validated previously (Yilma and Dorchies, 1991). Briefly, sagittal sections of each head were made and larvae were collected from the five major sites (nasal cavities, septum, middle meatus, conchae and sinuses). After all the heads of a given batch were processed, larvae were counted and identified to instar under a stereomicroscope for using the keys of Zumpt (1965). 2.3. Statistical analysis Comparisons between sheep and caprine O. ovis prevalences were performed with the chi-square test (Stat ITCF Software) and comparisons between ovine and caprine O. ovis larval burdens with the non-parametric Kruskall Wallis and Mann–Whitney test (Simstat Software).
3. Results Due to the recent problems of B. S. E. and Scrapie, it is now very difficult to perform slaughterhouse surveys of small ruminant heads in France. This explains why some results are missing (goats for November).
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
271
Table 1 Monthly prevalences and mean larval burdens
Number of heads per month Sheep Goats Number of larval positive heads Prevalence
Mean larval burdens
Sheep Goats
Jan Feb Mar Apr May Jun
Jul
Aug Sep
Oct
Nov Dec
Total
40 42 168 66
41 60
87 70
61 91
55 71
68 32
24 13
64 16
70 75
40 39 NDb 10
631 672
14 60
15 14
31 33
23 26
26 8
26 7
11 2
29 1
46 20
23 24 ND 2
274 191
6 18
Sheep 35 14.3 36.6 35.6 37.9 47.3 38.2 45.8 45.8 65 57.5 61.5 43.4 Goats 35.7 27.3 23.3 47.1 28.6 11.3 21.9 15.4 6.3 26.7 ND 20 28.4 Difference NS NS NS NS NS <0.001 NS 0.06 0.004 <0.001 – 0.018 <0.001 Sheep SDa Goats SD Difference
7.9 4.8 6 7 NS
27.3 52c 9.2 7.1 0.06
9.8 7 6.7 3.9 NS
5.4 5.2 4.1 3 NS
6 4.5 2.7 1.7 NS
3.6 3 4.8 2.9 NS
6.4 5 4.6 3.1 NS
4.4 3.3 3.5 1.4 NS
20.2 50c 6 2.8 0.012
17.4 15.1 5.4 3.7 0.043
13.3 13.8 10.9 14.5 12.4 14.7 ND 5.5 5.35 2.2 3.5 – 0.017 0.019
SD = Standard Deviation. ND = not done. c These two very important standard deviations are due only to one sheep for each month harbouring more than 200 larvae. a
b
Table 1 shows that out of the total of 631 heads of adult sheep examined, 274 (43.4%) were found to be infected with O. ovis larvae, and 191 (28.4%) out of 672 heads of adult goats. The mean monthly infection rate varied from 14.3 to 65% for sheep and from 6.25 to 47.1% for goats. The difference in infection rates between sheep and goats is significant (p < 0.0001). The mean larval burdens in infected animals were 10.87 for sheep with 9.24 L1, 0.91 L2 and 0.71 L3. In goats, the mean parasitic burden was 5.35 with 4.04 L1, 0.73 L2 and 0.58 L3. The difference between sheep and goats was also significant (p = 0.0195) for this parameter. Percentages of first, second and third instars are reported in Fig. 1 for sheep and Fig. 2 for goats for each month. 4. Discussion In the northern mediterranean climatic conditions and region of this survey, the first and second instars of O. ovis are present in sheep throughout the year, but the L2 occur in low numbers from September to February. In this case, the hypobiotic L1 accumulation in sheep as observed previously is not so obvious (Yilma and Dorchies, 1991). The larval burdens of all instars are closer to those observed in Tunis where L3 were also present all year round indicating a continuous cycle of parasite development (Kilani et al., 1986). Compared with previous results obtained in the south of France (Yilma and Dorchies, 1991),where the climate is colder and altitudes higher than in Pézenas, it appears that the
272
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
Fig. 1. Percentage distribution of the different instars in sheep.
cycle of L1 to L2 and L3 begins earlier during the winter, as early as January. The relative percentages of L1 decrease until May or June, then increasing again reaching 100% in goats and 99% in sheep in September. This study clearly indicates that O. ovis larvae are less prevalent in goats than in sheep. The life cycle of the parasite appears to develop faster in goats during summer, with less L1 in goats than in sheep. These results confirm those of the literature (Chhabra and Ruprah, 1976; Horak and Butt, 1977a,b; Belem and Rouille, 1988; Gabaj et al., 1993). In countries where surveys have been done in sheep and goats, the prevalence of oestrosis and the
Fig. 2. Percentage distribution of the different instars in goats.
Ph. Dorchies et al. / Veterinary Parasitology 88 (2000) 269–273
273
arithmetic mean parasite burdens are consistently higher in sheep than in goats: 17.1 in sheep and 6.6 in goats. Finally this survey reveals that O.ovis is present in goats even when clinical signs are less obvious than those observed in sheep. Serological surveys conducted in many countries confirm a more extensive ELISA reaction in sheep than in goats (Dorchies et al., 1999). Mast cells and eosinophils, in the mucosæ of the upper respiratory tract are quantitatively more numerous in sheep than in goats (Nguyen et al., 1999). These observations are confirmed by the epithelial proliferation measured by Ki 67 epitope (Nguyen et al., 1998). Roughly, these parameters could appear to be linked, i.e., the greater the numbers of instars, the greater the humoral and cellular reactions in sheep. It has been observed that when a parasite is developing in a non-specific host, the reaction to it may be stronger than in the specific host who is more tolerant because of previous exposure. The results of this survey on O. ovis burdens in sympatric sheep and goats may lead to a new approach of the host–parasite relationship between this parasite and sheep and goats. Acknowledgements The authors are indebted to Doctor Bellocq, Chief of meat inspection in Pézenas slaughterhouse and Doctor Garcin, head of the Veterinary Services from Hérault, for their very kind help in the achievement of this survey. References Belem, A.M.G., Rouille, D., 1988. Oestrose des petits ruminants au Burkina. Faso. Rev. Elev. et Méd. Vét. Pays Trop. 41, 59–64. Chhabra, M.B., Ruprah, N.S., 1976. Observations on the incidence and biology of Oestrus ovis L. Indian Vet. J. 53, 180–184. Dorchies, Ph., Yilma, J.M., Savey, J., 1993. Lung involvment in ovine Oestrosis: prevalence of lung abscesses and intertitial pneumonia. Vet. Rec. 133, 325. Dorchies, Ph., Prevot, F., Duranton, C., Bergeaud, J.P., Akakpo, J., Pangui, L.J., Missohou, A., Deconinck, P., Ouatara, L., Roger, F., Achi-Yaba, L., Dia, M., Jacquiet, Ph., 1999. Oestrose du mouton et de la chèvre (Oestrus ovis Linné 1761) en Afrique: résultats d’une enquête sur 3204 sérums provenant de neuf pays. Rev. Méd. Vét. 150, 463–466. Gabaj, M.M., Beesley, W.N., Awan, M.A., 1993. Oestrus ovis myiasis in Libyan sheep and goats. Trop. Anim. Health Prod. 25, 65–68. Horak, I.G., Butt, M.J., 1977a. Parasites of domestic and wild animals in South Africa I. Oestrus ovis in sheep. Onderst. J. Vet. Res. 44, 55–64. Horak, I.G., Butt, M.J., 1977b. Parasites of domestic and wild animals in South Africa II. Oestrus ovis in goats. Onderst. J. Vet. Res. 44, 65–68. Kilani, M., Kacem, H.H., Dorchies, Ph., Franc, M., 1986. Observations sur le cycle annuel d’Oestrus ovis en Tunisie. Rev. Méd. Vét. 137, 451–457. Nguyen, V.K., Delverdier, M., Jacquiet, Ph., Dorchies, Ph., 1998. Expression tissulaire de l’épitope Ki-67 dans le compartiment épithélial de la muqueuse nasale du mouton et de la chèvre infestés naturellement par Oestrus ovis (Linné 1761). Rev. Méd. Vét. 149, 1109–1113. Nguyen, V.K., Jacquiet, Ph., Bergeaud, J.P., Duranton, C., Prévot, F., Dorchies, Ph., 1999. Réactions cellulaires des muqueuses nasales et sinusales des chèvres et des moutons à l’infection naturelle par Oestrus ovis Linné 1761 (Diptera: Oestridés). Parasite 6, 141–149. Yilma, J.M., Dorchies, Ph., 1991. Epidemiology of Oestrus ovis in southwest France. Vet. Parasitol. 40, 315–323. Zumpt, P., 1965. Myiasis in Man and Animals in the Old World. Butterworths, London, 257 pp.