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Metacestodes of sheep with special reference to their epidemiological status, pathogenesis and economic implications in Fars Province, Iran
Veterinary Parasitology, 51 (1994) 231-240 0304-4017/94/$07.00 © 1994 - Elsevier Science B.V. All rights reserved
231
Metacestodes of sheep with special reference to their epidemiological status, pathogenesis and economic implications in Fars Province, Iran A. Oryan*, N. Moghaddar, S.N.S. Gaur Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran (Accepted 30 March 1993 )
Abs~a~
This study was undertaken over a period of 2 years. Of 7992 sheep examined, 2088 (26.12%), 2266 (28.36%), 15 (0.19%) and 738 (9.8%) were infected with Echinococcusgranulosus, Taenia hydatigena, Taenia ovis and Taenia multiceps metacestodes, respectively. The prevalence was higher in animals belonging to migratory tribal people than in those owned by the permanent residents of Fars Province. Dogs in the former group also showed significantly higher levels of infection with E. granulosus (33.3%) and Taenia spp. (40.7%) than those in the latter group. The metacestodes caused tissue damage in different organs, resulting in condemnation of meat or viscera valued at 10.2 million rials. The migration of tribal people has a direct bearing on the transmission of these parasites and must be taken into account in control planning. Key words: Echinococcus granulosus; Pathogenesis-Cestoda; Economics
Taenia spp., Sheep-Cestoda;
Epidemiology-Cestoda;
Introduction
Reports on the prevalence of Taenia multiceps in Iran have been made by Toofanian and Ivoghli (1976), and on Echinococcus granulosus by Hoghoughi (1963, 1971), Hoghoughi and Jalayer, (1967) and Mobedi et al. (1971 ). There are no similar published records on Taenia hydatigena, or Taenia ovis except for a mention by Eslami ( 1991 ). No systematic studies have yet been made on transmission dynamics of these metacestodes, their correlation with sheep and dogs and on any pathogenic effect in sheep. The present paper reports the epidemiologicalstatus of different metacestodes of sheep, their transmission patterns, pathogenesis and economic implications in Fars Province, Iran. The status of the strobilate phase of these cestodes in dogs is also reported. *Corresponding author. SSDI 0 3 0 4 - 4 0 1 7 ( 9 3 ) 0 0 5 14-Y
232
A. Oryan et aL / Veterinary Parasitology 51 (1994) 231-240
Materials and methods
Animals The animals studied were reared in various parts of Fars Province, Iran, but pastured under very different climatic and socio-economic conditions. The majority belonged to migratory tribal people (Assyrians) who purchase sheep from different areas of the province representing very different agroand geoclimatic conditions. Out of a total of 7992 sheep examined, 5536 belonged to Assyrians, 1707 belonged to private breeders of Zarghan, Marvdasht, Sheikh Alichoopan, Koohsabz and adjacent places and 749 were maintained at slaughterhouses. A few sheep which had died from unknown causes in nearby villages were also subjected to postmortem examination. The sheep examined were of indigenous breeds (Mehraban, Turkey, Gharagoul, Bakhtiari, Khamseai and Belagi ). The dogs examined in this study belonged to the Assyrians and accompanied them during migration; also examined were non-migratory animals and stray dogs living near slaughterhouses, towns or livestock farms.
Clinical parasitological and pathological examinations Regular antemortem examinations of sheep were carried out to observe any specific clinical sign (s). Animals with any abnormality in their posture, behaviour or showing clinical signs were segregated and followed until slaughtered. At postmortem, the animals were thoroughly examined for the presence of any larval cestodes. The gross lesions in the tissues/organs caused by cystic stages were observed and in specific cases, the suitable tissue pieces were collected, fixed in 10% formol saline and embedded in paraffin wax. Sections 6/tm thick were cut and stained with haematoxylin and eosin for histopathological examination. Faecal samples from the dogs were collected and examined for the presence of eggs or proglottids of taeniid worms. After identifying the taeniid eggs, complete faecal samples of the positive animals were collected for 24 h on one or more occasions and analysed for the proglottids of Taenia spp. and E. granulosus. In doubtful cases, the dogs were either treated or slaughtered and the proglottids/tapeworms recovered. All the tapeworms thus recovered were relaxed, flattened, fixed and stained. Specific identification of the worms was done after detailed examination. The tapeworms recovered from the dead dogs were similarly examined. Statistical analysis of the data by t-test and the Z 2 test established the level of significance between the different groups at P < 0.01.
233
A. Oryan et al./Veterinary Parasitology 51 (1994) 231-240
Results
Sheep Prevalence The details of metacestodes observed in different body parts of sheep are presented in Table 1. The most common bladder worms were E. granulosus (26.12%) and 7'. hydatigena (28.36%), followed by T. ovis (0.19%) and T. multiceps (9.80%). There was no difference in the occurrence of any of these metacestodes in male and female animals. However, the rate of infection was higher in animals over 2 years of age. The animals owned by Assyrians showed significantly high ( P < 0.01 ) prevalences of all metacestodes compared with the animals owned by the permanent population. The animals maintained in the slaughterhouses had the lowest levels of infection (Fig. 1 ). Infection with all metacestodes was highest in the summer than in other seasons of the year.
Site of predilection The distribution of E. granulosus cysts in the liver, lungs, spleen and kidneys was 49.320%, 49.28%, 0.383% and 1.005%, respectively. In a few cases, the lungs had 60-211 cysts while in the liver their maximum number was 3354. The fertility rate of cysts in the liver (15%) was higher than that of cysts in the lungs (12%), whereas cysts in the spleen and kidneys were all infertile. 40 35.37
36 32 "G 28 0 o..
.E
24.54
24
~ 2o o
g16
13.65
~
13,18
e-
~ 12
L. Q
8.14 6.4
8 1.4 T/~0.058
0.25
0.4
o A
B
C
A-Assyrians, B-Local, G-Slaughter house
Fig. 1. Diagram showing the prevalence of metacestodes in sheep of Assyrians, local people and slaughterhouses.
1029
39
9
749
1030
198
217
1707
7992
792
804
5536
Lu.
8
0
0
8
Sp.
21
0
4
17
K.
2088 (26.12)
1621 (29.28) 419 (24.54) 48 (6.40)
Total
Total
583
13
48
522
1681
48
176
1475
2
0
1
1
2266 (28.36)
1980 (35.76) 225 (13.18) 61 (8.14)
3
0
0
3
12
0
1
11
15 (0.19)
14 (0.252) 1 (0.058) 0 (0.0)
50
0
1
49
731
3
23
705
2
0
0
2
783 (9.80)
756 (13.65) 24 (1.40) 3 (0.40)
H. Total
Mus. Br.
Total
Mus. H.
K.
Liv.
Mes.
Taenia multiceps
Taenia ovis
Taenia hydatigena
Liv., liver; Lu., lungs, Sp., spleen; IC, kidneys; Mes., mesentery; Ms., muscle, H., heart; Br., brain. Figures in parentheses indicate percentages. Level of significance: P< 0.01.
Toml
Animals of Assyrians Animals of local people Animals maintained in slaughter-houses
Liv.
Total no. Animals infected with metacestodes of animals examined Echinococcusgranulosus
Table 1 Metacestodes of sheep in Fars Province, Iran during 1990-1992
Z
g
¢a
t~
A. Oryan et al./Veterinary Parasitology 51 (1994.)231-240
235
Fig. 2. Heart of sheep showing the presence of Cysticercus ovis.
Of the total number of T. hydatigena cysticerci found, 74.18% were in the mesentery, 25.72% were in the liver and 0.088% in the kidneys. The cysticerci of T. ovis were more common in the heart (80.0%; Fig. 2) than in muscles (20.0%). Taenia multiceps coenurosis was noticed in the brain (93.35%), muscles (6.38%) and heart (0.223%).
Pathology The liver and lungs of most of the infected animals showed multiple cysts ofE. granulosus and the bile ducts were also compressed, resulting in obstruction in the flow of bile. The cysts caused extensive damage to the organs and in one animal, almost the whole lung tissue was replaced by multiple cysts. In T. hydatigena infection, the peritoneal cavity contained serofibrinous fluid with freely floating cysticerci. The liver parenchyma revealed haemorrhages and minute channels which were a result of the migration of cysticerci. In acute cases the organ was swollen, whereas in the chronic stage it was hard to the touch and its capsule showed whitish spots. In two animals, fully developed cysticerci were attached to the kidney without causing any gross lesion except for the whitish spots at the site of attachment. Cysticerci of T. ovis caused degeneration, necrosis and hyalinisation of
236
A. Oryan et al. /Veterinary Parasitology 51 (1994) 231-240
Fig. 3. Skeletal muscles of sheep infected with C o e n u r u s cerebralis.
Fig. 4. Heart of sheep showing the extensive damage caused by C o e n u r u s cerebralis.
76
Total
aRepresentative of Fars Province. Level of significance: P < 0.01.
2p, postmortem examination; F, faecal examination.
'Males and females of different age groups.
1991 - 1992
40 10 17 9
Shiraz Assyrians' animals 3 Shiraz Assyrians' animals 3
1990-1991
%
533
206 105 126 96 609
246 115 143 105 28
15 6 3 4 175
24 67 28 56 203
39 73 31 60 33.3
15.8 63.48 21.6 57.1 33
17 6 4 6 225
61 79 38 47
F
P
Total
P
F
Taenia spp.
Echinococcus granulosus
Total
P
F
No. of animals infected
No. of animals examined 2
Location/ownership
Year
Table 2 Prevalence of taeniid worms in dogs ~of Fars Province, Iran
258
78 85 42 53
Total
40.7
31.3 73.04 29.37 50.5
%
t~
g~
2 38
A. Oryan et al./Veterinary Parasitology 51 (1994) 231-240
Table 3 Details of viscera and mutton rejected and economic losses due to metacestode infections in sheep Year
Animals +Ve
Liver
Lungs
Heart
Weight (kg)
Cost (Rls 1800 kg- t )
No.
Cost (Rls 200 each)
Weight (kg)
Cost (Rls 2000 kg- 1 )
1990-1991 1991-1992
3731 1421
2797 984
5034600 1771200
1248 826
249600 165200
8 2
16000 4000
Total
5152
3781
6805800
2074
414800
10
20000
Total number of animals examined: 7992. Total cost: Rls. 10 218 250 (approximately US$15 700.0).
skeletal muscle fibres. The normal contour of the muscles was lost in the vicinity of the cysticerci and at certain places there was serofibrinous exudate. The sections of cysticerci in the heart were surrounded by a zone of degenerative, necrotic changes and leukocytic infiltration by lymphocytes and eosinophils predominated. Macrophages and giant cells were also seen. Myocardial tissue showed extensive damage. Multiple Coenurus cerebralis in the brain caused extensive damage to meninges and surrounding tissues, including pressure atrophy and necrosis. Oedema and swellings were also observed. Microscopically, the brain revealed degenerative and necrotic lesions with sections of metacestode cut in various planes and surrounded by marked necrotic tissue and a zone of chronic cellular reaction. The metacestodes in skeletal muscles (Fig. 3 ) caused extensive damage, focal to diffuse mononuclear infiltration, degenerative and necrotic changes and hyalinisation. The metacestode in the heart of sheep (Fig. 4) caused necrosis and fibrosis. Cardiac tissue became loose at places and there was infiltration of eosinophils and lymphocytes.
Prevalence of taeniid worms in dogs The results are presented in Table 2. Out of 609 dogs, 203 ( 33.3%) and 258 (40.7%) were positive for E. granulosus and Taenia spp. respectively. The dogs maintained by Assyrians showed a significantly high (P< 0.01 ) infection rate of these taeniid worms.
Economic implications The details of viscera and muscles rejected owing to metacestode infections in sheep are shown in Table 3. Out of a total of 7992 sheep examined at slaughter during 1990-1992, the approximate economic loss incurred was 10.2 million rials (US $15 700).
239
A. Oryan et aL /Veterinary Parasitology 51 (1994) 231-240
Brain
Kidney Weight (kg)
Mesentery and fat
Muscles
Cost (Rls 2100 kg -1 )
Weight (kg)
Cost (Rls 850kg -~ )
Weight (kg)
Cost (Rls 1800 kg -1 )
Weight (kg)
Cost (Rls 1750 kg -1 )
325 75
568750 131250
6 5
12600 10500
1376 315
1169600 267750
376 78
676800 140400
400
700000
11
23100
1691
1437350
454
817200
Discussion
The infection rate of metacestodes was higher in the sheep of Assyrians, followed by those of local people and those maintained in slaughterhouses. This is because Assyrian dogs, which also had significantly high (P< 0.01 ) infection rates of adult taeniid worms, live very close to sheep and play an important role in the transmission of these infections: consequently, these dogs pose a public health problem. The highest level of infection of these metacestodes occurred in the summer season, mainly because most of the animals slaughtered during this period belonged to Assyrians. This pattern of infection for E. granulosus metacestodes was also observed by Hoghoughi (1963), Mobedi et al. ( 1971 ) and Motakefet al. (1976). Echinococcusgranulosus cysts caused extensive tissue damage and production losses in the sheep industry, which corroborated the observations of Mobedi et al. ( 1971 ) on the mutton industry in Iran. The lesions caused by T. hydatigena metacestodes in the liver of sheep in our studies were comparable to those observed by Pathak et al. (1982) in goats. Extensive damage to the liver resulted in the condemnation of this organ at slaughter and amounted to heavy economic losses. Tress et al. (1985) and Peris et al. (1987) also reported that this metacestode was the main cause of liver condemnation. In the present studies, T. ovis cysticercosis in skeletal muscles and heart and T. multiceps coenurosis of brain, skeletal muscles and heart of sheep resulted in extensive damage and condemnation of these parts of the carcass at slaughter. Although our observations were limited to the dog-sheep cycle, the involvement of a sylvatic cycle cannot be ruled out, as the migration route followed by the Assyrians also includes areas inhabited by wild animals. This view was also supported by Toofanian and Ivoghli (1976) who observed coenurosis in wild sheep in Iran. Our observations further showed that the animals of Assyrians carry maximum infection of all these metacestodes and since these people migrate from one place/region to another in different sea-
240
,4. Oryanet al./VeterinaryParasitology51 (1994)231-240
sons of the year, their animals may pose serious health problems to local animals and to the human population. As shown in Table 3, these infections are responsible for the condemnation of a large quantity of viscera and muscles of sheep in this area. Though no comparable statistical figures on such losses due to these metacestodes are yet available, the overall production losses could be still enormous. The present study is the first of its kind to be carried out in Iran, particularly in relation to the Assyrian lifestyle and route of migration. The data obtained on the epidemiology and pathogenesis of different metacestodes of sheep could be taken as a baseline for the planning of a programme to control these infections in this region, as was advocated by Schwabe ( 1979 ) for hydatidosis elsewhere. The latter disease continues to pose a serious threat to human health in Iran (Saidi, 1976; Kumar and Jahanshahi, 1987) and thus these studies could be utilised in efforts to contain this infection. Acknowledgements The authors are grateful to Dr. K. Mokhtary and other authorities of Shiraz meat complexes for providing facilities. Thanks are also due to Ladan Joukar of the computer section of the Agriculture Research Centre for her help in processing the data and to R. Shahangian for technical assistance. References Eslami, A., 1991. Cestoda. Veterinary Helminthology, Vol. 2. Publ. No. 2030/2, Tehran University, Iran, 104 pp. Hoghoughi, N., 1963. The dog and the danger it poses in the transmission of hydatid cyst in Shiraz. D.V.M. Thesis, School of Veterinary Medicine, Tehran University. (In Persian.) Hoghoughi, N., 197 I. A study of the prevalence ofEchinococcus granulosus in dogs and hydatid cyst in sheep, goats, cattle and man in Isfahan. Pahlavi Med. J., 2:670-676. Hoghoughi, N. and Jalayer, T., 1967. The prevalence of Echinococcus granulosus in dogs in Shiraz, Iran. Ann. Trop. Med. Parasitol., 61:437. Kumar, P.V.N. and Jahanshahi, Sh., 1987. Hydatid cyst of testes: A case report. J. Urology, 137:511-512. Mobedi, I., Arfaa, F. and Farahmandian, I., 1971. Studies on Echinococcus granulosus in Iran. Acta Med. Iran., XIV:221-229. Motakef, M., Minou, A.A. and Lari, M., 1976. An epidemiological approach to the study of Echinococcus in north east region of Iran (Khorasan). Pahlavi Med. J., 7:503-515. Pathak, K.M.L., Gaur, S.N.S. and Sharrna, S.N., 1982. The pathology of Cysticercus tenuicollis infection in goats. Vet. Parasitol., l 1:131-139. Peris, P.B., Garclamorla, J.F. and Badiola Delez, J.J., 1987. Ovine visceral cysticercosis: main cause of liver condemnation in fat lambs. Lesions and incidence. Med. Vet., 4:289-296. Saidi, F., 1976. Surgery of Hydatid Disease. W.B. Saunders, Philadelphia, PA, p. 2. Schwabe, C.W., 1979. Epidemiological aspects of the planning and evaluation of hydatid disease control. Aust. Vet. J., 55:109-117. Toofanian, F. and Ivoghli, B., 1976. Coenurus cerebralis in wild sheep. J. Wildl. Dis., 2:550551. Tress, A.J., Owen, R.R., Craig, P.S. and Purvis, G.M., 1985. Taenia hydatigena, a cause of persistent liver condemnation in lambs. Vet. Rec., I 16:512-516.
231
Metacestodes of sheep with special reference to their epidemiological status, pathogenesis and economic implications in Fars Province, Iran A. Oryan*, N. Moghaddar, S.N.S. Gaur Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran (Accepted 30 March 1993 )
Abs~a~
This study was undertaken over a period of 2 years. Of 7992 sheep examined, 2088 (26.12%), 2266 (28.36%), 15 (0.19%) and 738 (9.8%) were infected with Echinococcusgranulosus, Taenia hydatigena, Taenia ovis and Taenia multiceps metacestodes, respectively. The prevalence was higher in animals belonging to migratory tribal people than in those owned by the permanent residents of Fars Province. Dogs in the former group also showed significantly higher levels of infection with E. granulosus (33.3%) and Taenia spp. (40.7%) than those in the latter group. The metacestodes caused tissue damage in different organs, resulting in condemnation of meat or viscera valued at 10.2 million rials. The migration of tribal people has a direct bearing on the transmission of these parasites and must be taken into account in control planning. Key words: Echinococcus granulosus; Pathogenesis-Cestoda; Economics
Taenia spp., Sheep-Cestoda;
Epidemiology-Cestoda;
Introduction
Reports on the prevalence of Taenia multiceps in Iran have been made by Toofanian and Ivoghli (1976), and on Echinococcus granulosus by Hoghoughi (1963, 1971), Hoghoughi and Jalayer, (1967) and Mobedi et al. (1971 ). There are no similar published records on Taenia hydatigena, or Taenia ovis except for a mention by Eslami ( 1991 ). No systematic studies have yet been made on transmission dynamics of these metacestodes, their correlation with sheep and dogs and on any pathogenic effect in sheep. The present paper reports the epidemiologicalstatus of different metacestodes of sheep, their transmission patterns, pathogenesis and economic implications in Fars Province, Iran. The status of the strobilate phase of these cestodes in dogs is also reported. *Corresponding author. SSDI 0 3 0 4 - 4 0 1 7 ( 9 3 ) 0 0 5 14-Y
232
A. Oryan et aL / Veterinary Parasitology 51 (1994) 231-240
Materials and methods
Animals The animals studied were reared in various parts of Fars Province, Iran, but pastured under very different climatic and socio-economic conditions. The majority belonged to migratory tribal people (Assyrians) who purchase sheep from different areas of the province representing very different agroand geoclimatic conditions. Out of a total of 7992 sheep examined, 5536 belonged to Assyrians, 1707 belonged to private breeders of Zarghan, Marvdasht, Sheikh Alichoopan, Koohsabz and adjacent places and 749 were maintained at slaughterhouses. A few sheep which had died from unknown causes in nearby villages were also subjected to postmortem examination. The sheep examined were of indigenous breeds (Mehraban, Turkey, Gharagoul, Bakhtiari, Khamseai and Belagi ). The dogs examined in this study belonged to the Assyrians and accompanied them during migration; also examined were non-migratory animals and stray dogs living near slaughterhouses, towns or livestock farms.
Clinical parasitological and pathological examinations Regular antemortem examinations of sheep were carried out to observe any specific clinical sign (s). Animals with any abnormality in their posture, behaviour or showing clinical signs were segregated and followed until slaughtered. At postmortem, the animals were thoroughly examined for the presence of any larval cestodes. The gross lesions in the tissues/organs caused by cystic stages were observed and in specific cases, the suitable tissue pieces were collected, fixed in 10% formol saline and embedded in paraffin wax. Sections 6/tm thick were cut and stained with haematoxylin and eosin for histopathological examination. Faecal samples from the dogs were collected and examined for the presence of eggs or proglottids of taeniid worms. After identifying the taeniid eggs, complete faecal samples of the positive animals were collected for 24 h on one or more occasions and analysed for the proglottids of Taenia spp. and E. granulosus. In doubtful cases, the dogs were either treated or slaughtered and the proglottids/tapeworms recovered. All the tapeworms thus recovered were relaxed, flattened, fixed and stained. Specific identification of the worms was done after detailed examination. The tapeworms recovered from the dead dogs were similarly examined. Statistical analysis of the data by t-test and the Z 2 test established the level of significance between the different groups at P < 0.01.
233
A. Oryan et al./Veterinary Parasitology 51 (1994) 231-240
Results
Sheep Prevalence The details of metacestodes observed in different body parts of sheep are presented in Table 1. The most common bladder worms were E. granulosus (26.12%) and 7'. hydatigena (28.36%), followed by T. ovis (0.19%) and T. multiceps (9.80%). There was no difference in the occurrence of any of these metacestodes in male and female animals. However, the rate of infection was higher in animals over 2 years of age. The animals owned by Assyrians showed significantly high ( P < 0.01 ) prevalences of all metacestodes compared with the animals owned by the permanent population. The animals maintained in the slaughterhouses had the lowest levels of infection (Fig. 1 ). Infection with all metacestodes was highest in the summer than in other seasons of the year.
Site of predilection The distribution of E. granulosus cysts in the liver, lungs, spleen and kidneys was 49.320%, 49.28%, 0.383% and 1.005%, respectively. In a few cases, the lungs had 60-211 cysts while in the liver their maximum number was 3354. The fertility rate of cysts in the liver (15%) was higher than that of cysts in the lungs (12%), whereas cysts in the spleen and kidneys were all infertile. 40 35.37
36 32 "G 28 0 o..
.E
24.54
24
~ 2o o
g16
13.65
~
13,18
e-
~ 12
L. Q
8.14 6.4
8 1.4 T/~0.058
0.25
0.4
o A
B
C
A-Assyrians, B-Local, G-Slaughter house
Fig. 1. Diagram showing the prevalence of metacestodes in sheep of Assyrians, local people and slaughterhouses.
1029
39
9
749
1030
198
217
1707
7992
792
804
5536
Lu.
8
0
0
8
Sp.
21
0
4
17
K.
2088 (26.12)
1621 (29.28) 419 (24.54) 48 (6.40)
Total
Total
583
13
48
522
1681
48
176
1475
2
0
1
1
2266 (28.36)
1980 (35.76) 225 (13.18) 61 (8.14)
3
0
0
3
12
0
1
11
15 (0.19)
14 (0.252) 1 (0.058) 0 (0.0)
50
0
1
49
731
3
23
705
2
0
0
2
783 (9.80)
756 (13.65) 24 (1.40) 3 (0.40)
H. Total
Mus. Br.
Total
Mus. H.
K.
Liv.
Mes.
Taenia multiceps
Taenia ovis
Taenia hydatigena
Liv., liver; Lu., lungs, Sp., spleen; IC, kidneys; Mes., mesentery; Ms., muscle, H., heart; Br., brain. Figures in parentheses indicate percentages. Level of significance: P< 0.01.
Toml
Animals of Assyrians Animals of local people Animals maintained in slaughter-houses
Liv.
Total no. Animals infected with metacestodes of animals examined Echinococcusgranulosus
Table 1 Metacestodes of sheep in Fars Province, Iran during 1990-1992
Z
g
¢a
t~
A. Oryan et al./Veterinary Parasitology 51 (1994.)231-240
235
Fig. 2. Heart of sheep showing the presence of Cysticercus ovis.
Of the total number of T. hydatigena cysticerci found, 74.18% were in the mesentery, 25.72% were in the liver and 0.088% in the kidneys. The cysticerci of T. ovis were more common in the heart (80.0%; Fig. 2) than in muscles (20.0%). Taenia multiceps coenurosis was noticed in the brain (93.35%), muscles (6.38%) and heart (0.223%).
Pathology The liver and lungs of most of the infected animals showed multiple cysts ofE. granulosus and the bile ducts were also compressed, resulting in obstruction in the flow of bile. The cysts caused extensive damage to the organs and in one animal, almost the whole lung tissue was replaced by multiple cysts. In T. hydatigena infection, the peritoneal cavity contained serofibrinous fluid with freely floating cysticerci. The liver parenchyma revealed haemorrhages and minute channels which were a result of the migration of cysticerci. In acute cases the organ was swollen, whereas in the chronic stage it was hard to the touch and its capsule showed whitish spots. In two animals, fully developed cysticerci were attached to the kidney without causing any gross lesion except for the whitish spots at the site of attachment. Cysticerci of T. ovis caused degeneration, necrosis and hyalinisation of
236
A. Oryan et al. /Veterinary Parasitology 51 (1994) 231-240
Fig. 3. Skeletal muscles of sheep infected with C o e n u r u s cerebralis.
Fig. 4. Heart of sheep showing the extensive damage caused by C o e n u r u s cerebralis.
76
Total
aRepresentative of Fars Province. Level of significance: P < 0.01.
2p, postmortem examination; F, faecal examination.
'Males and females of different age groups.
1991 - 1992
40 10 17 9
Shiraz Assyrians' animals 3 Shiraz Assyrians' animals 3
1990-1991
%
533
206 105 126 96 609
246 115 143 105 28
15 6 3 4 175
24 67 28 56 203
39 73 31 60 33.3
15.8 63.48 21.6 57.1 33
17 6 4 6 225
61 79 38 47
F
P
Total
P
F
Taenia spp.
Echinococcus granulosus
Total
P
F
No. of animals infected
No. of animals examined 2
Location/ownership
Year
Table 2 Prevalence of taeniid worms in dogs ~of Fars Province, Iran
258
78 85 42 53
Total
40.7
31.3 73.04 29.37 50.5
%
t~
g~
2 38
A. Oryan et al./Veterinary Parasitology 51 (1994) 231-240
Table 3 Details of viscera and mutton rejected and economic losses due to metacestode infections in sheep Year
Animals +Ve
Liver
Lungs
Heart
Weight (kg)
Cost (Rls 1800 kg- t )
No.
Cost (Rls 200 each)
Weight (kg)
Cost (Rls 2000 kg- 1 )
1990-1991 1991-1992
3731 1421
2797 984
5034600 1771200
1248 826
249600 165200
8 2
16000 4000
Total
5152
3781
6805800
2074
414800
10
20000
Total number of animals examined: 7992. Total cost: Rls. 10 218 250 (approximately US$15 700.0).
skeletal muscle fibres. The normal contour of the muscles was lost in the vicinity of the cysticerci and at certain places there was serofibrinous exudate. The sections of cysticerci in the heart were surrounded by a zone of degenerative, necrotic changes and leukocytic infiltration by lymphocytes and eosinophils predominated. Macrophages and giant cells were also seen. Myocardial tissue showed extensive damage. Multiple Coenurus cerebralis in the brain caused extensive damage to meninges and surrounding tissues, including pressure atrophy and necrosis. Oedema and swellings were also observed. Microscopically, the brain revealed degenerative and necrotic lesions with sections of metacestode cut in various planes and surrounded by marked necrotic tissue and a zone of chronic cellular reaction. The metacestodes in skeletal muscles (Fig. 3 ) caused extensive damage, focal to diffuse mononuclear infiltration, degenerative and necrotic changes and hyalinisation. The metacestode in the heart of sheep (Fig. 4) caused necrosis and fibrosis. Cardiac tissue became loose at places and there was infiltration of eosinophils and lymphocytes.
Prevalence of taeniid worms in dogs The results are presented in Table 2. Out of 609 dogs, 203 ( 33.3%) and 258 (40.7%) were positive for E. granulosus and Taenia spp. respectively. The dogs maintained by Assyrians showed a significantly high (P< 0.01 ) infection rate of these taeniid worms.
Economic implications The details of viscera and muscles rejected owing to metacestode infections in sheep are shown in Table 3. Out of a total of 7992 sheep examined at slaughter during 1990-1992, the approximate economic loss incurred was 10.2 million rials (US $15 700).
239
A. Oryan et aL /Veterinary Parasitology 51 (1994) 231-240
Brain
Kidney Weight (kg)
Mesentery and fat
Muscles
Cost (Rls 2100 kg -1 )
Weight (kg)
Cost (Rls 850kg -~ )
Weight (kg)
Cost (Rls 1800 kg -1 )
Weight (kg)
Cost (Rls 1750 kg -1 )
325 75
568750 131250
6 5
12600 10500
1376 315
1169600 267750
376 78
676800 140400
400
700000
11
23100
1691
1437350
454
817200
Discussion
The infection rate of metacestodes was higher in the sheep of Assyrians, followed by those of local people and those maintained in slaughterhouses. This is because Assyrian dogs, which also had significantly high (P< 0.01 ) infection rates of adult taeniid worms, live very close to sheep and play an important role in the transmission of these infections: consequently, these dogs pose a public health problem. The highest level of infection of these metacestodes occurred in the summer season, mainly because most of the animals slaughtered during this period belonged to Assyrians. This pattern of infection for E. granulosus metacestodes was also observed by Hoghoughi (1963), Mobedi et al. ( 1971 ) and Motakefet al. (1976). Echinococcusgranulosus cysts caused extensive tissue damage and production losses in the sheep industry, which corroborated the observations of Mobedi et al. ( 1971 ) on the mutton industry in Iran. The lesions caused by T. hydatigena metacestodes in the liver of sheep in our studies were comparable to those observed by Pathak et al. (1982) in goats. Extensive damage to the liver resulted in the condemnation of this organ at slaughter and amounted to heavy economic losses. Tress et al. (1985) and Peris et al. (1987) also reported that this metacestode was the main cause of liver condemnation. In the present studies, T. ovis cysticercosis in skeletal muscles and heart and T. multiceps coenurosis of brain, skeletal muscles and heart of sheep resulted in extensive damage and condemnation of these parts of the carcass at slaughter. Although our observations were limited to the dog-sheep cycle, the involvement of a sylvatic cycle cannot be ruled out, as the migration route followed by the Assyrians also includes areas inhabited by wild animals. This view was also supported by Toofanian and Ivoghli (1976) who observed coenurosis in wild sheep in Iran. Our observations further showed that the animals of Assyrians carry maximum infection of all these metacestodes and since these people migrate from one place/region to another in different sea-
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sons of the year, their animals may pose serious health problems to local animals and to the human population. As shown in Table 3, these infections are responsible for the condemnation of a large quantity of viscera and muscles of sheep in this area. Though no comparable statistical figures on such losses due to these metacestodes are yet available, the overall production losses could be still enormous. The present study is the first of its kind to be carried out in Iran, particularly in relation to the Assyrian lifestyle and route of migration. The data obtained on the epidemiology and pathogenesis of different metacestodes of sheep could be taken as a baseline for the planning of a programme to control these infections in this region, as was advocated by Schwabe ( 1979 ) for hydatidosis elsewhere. The latter disease continues to pose a serious threat to human health in Iran (Saidi, 1976; Kumar and Jahanshahi, 1987) and thus these studies could be utilised in efforts to contain this infection. Acknowledgements The authors are grateful to Dr. K. Mokhtary and other authorities of Shiraz meat complexes for providing facilities. Thanks are also due to Ladan Joukar of the computer section of the Agriculture Research Centre for her help in processing the data and to R. Shahangian for technical assistance. References Eslami, A., 1991. Cestoda. Veterinary Helminthology, Vol. 2. Publ. No. 2030/2, Tehran University, Iran, 104 pp. Hoghoughi, N., 1963. The dog and the danger it poses in the transmission of hydatid cyst in Shiraz. D.V.M. Thesis, School of Veterinary Medicine, Tehran University. (In Persian.) Hoghoughi, N., 197 I. A study of the prevalence ofEchinococcus granulosus in dogs and hydatid cyst in sheep, goats, cattle and man in Isfahan. Pahlavi Med. J., 2:670-676. Hoghoughi, N. and Jalayer, T., 1967. The prevalence of Echinococcus granulosus in dogs in Shiraz, Iran. Ann. Trop. Med. Parasitol., 61:437. Kumar, P.V.N. and Jahanshahi, Sh., 1987. Hydatid cyst of testes: A case report. J. Urology, 137:511-512. Mobedi, I., Arfaa, F. and Farahmandian, I., 1971. Studies on Echinococcus granulosus in Iran. Acta Med. Iran., XIV:221-229. Motakef, M., Minou, A.A. and Lari, M., 1976. An epidemiological approach to the study of Echinococcus in north east region of Iran (Khorasan). Pahlavi Med. J., 7:503-515. Pathak, K.M.L., Gaur, S.N.S. and Sharrna, S.N., 1982. The pathology of Cysticercus tenuicollis infection in goats. Vet. Parasitol., l 1:131-139. Peris, P.B., Garclamorla, J.F. and Badiola Delez, J.J., 1987. Ovine visceral cysticercosis: main cause of liver condemnation in fat lambs. Lesions and incidence. Med. Vet., 4:289-296. Saidi, F., 1976. Surgery of Hydatid Disease. W.B. Saunders, Philadelphia, PA, p. 2. Schwabe, C.W., 1979. Epidemiological aspects of the planning and evaluation of hydatid disease control. Aust. Vet. J., 55:109-117. Toofanian, F. and Ivoghli, B., 1976. Coenurus cerebralis in wild sheep. J. Wildl. Dis., 2:550551. Tress, A.J., Owen, R.R., Craig, P.S. and Purvis, G.M., 1985. Taenia hydatigena, a cause of persistent liver condemnation in lambs. Vet. Rec., I 16:512-516.