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Prevalence of microfilariae in cattle at slaughter in Zaria, Nigeria
Veterinary Parasitology, 36 (1990) 171-175 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
171
Short C o m m u n i c a t i o n
P r e v a l e n c e of M i c r o f i l a r i a e in Cattle at S l a u g h t e r in Zaria, N i g e r i a ¥.C. OGBOGU*, 3.M. BABL1S and O.J. AJANUSI
Department of Veterinary Parasitology and Entomology, Ahmadu Bello University Zaria (Nigeria) (Accepted for publication 12 October 1989)
ABSTRACT Ogbogu, V.C., Bablis, J.M. and Ajanusi, O.J., 1990. Prevalence of microfilariae in cattle at slaughter in Zaria, Nigeria. Vet. Parasitol., 36: 171-175. Skin snips and blood taken from 372 randomly selected slaughtered cattle in Zaria, Nigeria were examined for microfilariae. A total of 293 (78.8%) skin snips and 218 (58.6%) blood samples were positive for microfilariae. Two types of microfilariae, identified as Onchocerca armiUata, with a percentage prevalence of 64%, and O. gutturosa with a prevalence of 40% were isolated from the skin. The blood microfilariae were identified as those of Setaria labiatopapillosa
INTRODUCTION
The occurrence of a variety of filarial species in cattle is well documented and they are known to be of wide geographical distribution (Nelson, 1966). In Nigeria, filarial infections are common in domestic animals (Schillhorn van Veen, 1974). Although local surveys are concerned mostly with bovine onchocercosis (Schillhorn van Veen and Robl, 1975; Ogunrinade, 1980; Braide, 1981), little knowledge exists about the different species of Onchocerca and other filarial species present in cattle in Nigeria. This investigation was done as part of wider studies on the host-parasite relationships of both animal and human filariasis in Zaria, Nigeria. MATERIALS AND METHODS
The cattle from which samples were taken were those slaughtered at the main Zaria abattoir. The major breed of cattle encountered was white Fulani (Bunaji). Because most of the animals were trade cattle owned by nomadic or semi-nomadic herdsmen, the origins of the animals could not be determined. However, in recent times, there appears to have been an increase in the number 0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
172
V.C. OGBOGU ET Air.
of sedentary livestock operations, which are managed by non-nomadic herdsmen. A total of 372 randomly selected cattle were sampled. At slaughter, the sex of each animal was recorded. The ages could not be determined owing to the speed of activities on the slaughter floor. However, most of the animals slaughtered were mature. Following the removal of the hide, skin samples were collected from the ear, umbilical area, neck region, dewlap, scrotum or udder of all the cattle sampled. Examination and palpation of the brisket, adjacent abdominal and chest areas for nodules were carried out. In the laboratory, skin tissues of approximately 1 cm ~ were excised from the strips of skin, and were minced with dissecting needles and scapel before incubation in isotonic saline at 37°C for 24 h. Microfilariae were stained with 1% brilliant cresyl blue in ethyl alcohol (Schillhorn van Veen and Blotkamp, 1972) or Giesma before examining for morphological characteristics. For microfilarial densities in different parts of the skin, microfilariae that emerged from I cm 2 skin tissues of 50 positive skin samples each were counted. For blood microfilariae, 10 ml of blood samples were collected from each cattle at slaughter and put into bottles containing EDTA. In the laboratory, 4 ml of each blood sample was examined for microfilariae using wet mounts and the micro-haematocrit methods. Blood smears were made from positive samples. These were stained with either Giemsa or brilliant cresyl blue and were later examined for morphological characteristics. Fifty randomly selected skin or blood microfilariae were measured using an ocular micrometer. R E S U L T S AND D I S C U S S I O N
The prevalence of skin and blood microfilariae is summarized in Table 1. The difference between infection levels in males and females was not significant. Typical Onchocerca microfilariae occurred in the skin of 293 (78.8%) of the cattle sampled. This is a considerably higher number than the previously reported value of 0.3-0.8% in slaughtered cattle in Zaria, based on abattoir TABLE 1 Prevalence of microfilariae in skin and blood samples of Zaria cattle No. of
cattle examined Female Male Total
81 291 372
Skin samples
Blood samples
Mixed infections ~
No. positive
% Positive
No. Positive
% Positive
No. positive
% Positive
59 234 293
72.8 80.4 78.8
53 165 218
65.4 56.7 58.6
47 129 176
58.0 44.3 47.3
~Infections with b o t h skin a n d blood microfilariae.
BOVINE FILARIASIS IN ZARIA,NIGERIA
173
records, (Ogunrinade, 1980). Two types of microfilariae with the morphological characteristics of O. armillata (mean length 295 + 28.5 ttm) and O. gutturosa (mean length 218 + 12.6/~m ) were encountered in the skin. Their prevalence rates are summarized in Table 2. Clearly O. armiUata which occurred in 81.2% of the positive skin samples, but with an overall prevalence of 64%, was the most common. The overall prevalence rates of the two Onchocerca species differed little from previously recorded findings in Zaria (Schillhorn van Veen and Robl, 1975) and in some neighbouring countries (Chodnik, 1957; Graber et al, 1966; Hussein et al., 1975). In addition to infecting cattle, O. armiUata has been found to infect camels in Nigeria (Schillhorn van Veen et al., 1976 ). Onchocerca gibsoni an important species of Onchocerca owing to its use in chemotherapeutic research in human onchocerciasis was not encountered in this study. It seems very likely that this species is not present in Nigeria and other parts of Africa. Although the occurrence of O. gibsoni had been reported from North Eastern parts of Nigeria (Nigeria, 1958), the accuracy of the identification of the isolated worm is open to doubt. This is because the morphological characteristics described for the worms, did not compare completely with the known morphology of O. gibsoni (Schillhorn van Veen, 1974). The densities of O. armiUata and O. gutturosa microfilariae in different skin sites are shown in Table 3. For O. armiUata, the highest density was recorded in the scrotum and the lowest in the umbilicus. For O. gutturosa the highest density was in the neck region and the lowest in the udder. It has been suggested that the concentration of microfilariae in the skin is influenced by the biting habits of the vector host (Eichler and Nelson, 1971). However, in Nigeria, the intermediate hosts for the Onchocerca species are not yet known. Blood microfilariae were present in 218 (58.6%) of the cattle sampled. The microfilariae were sheathed and had a mean length of 215 + 7.06 ttm. They were identified as those of Setaria labiatopapillosa. The adult worms inhabit the peritoneal cavity and are non-pathogenic. However, the larvae have been shown TABLE 2 Prevalence of O. arrnillata and O. gutturosa microfilariae in positive skin samples No. of positive cattle Females Males Total
59 234 293
O. armiUata
O. gutturosa
Mixed infections
No. positive
% Positive
No. Positive
% Positive
No. Positive
% Positive
46 192 238
78.0 82.1 81.2 (64) 1
27 144 171
45.8 61.5 58.4 (46)
15 93 108
25.4 39.7 36.9 (29.0)
1Figures in parenthesis indicate percentage prevalence in total n u m b e r of cattle sampled.
174
V.C. OGBOGUET AI..
TABLE 3 Microfilarial densities in skin specimens (mean counts of microfilariae per 1 cm ~ of skin) Skin sample site
No. of positive skin specimens taken
O. armillata
O. gutturosa
Ear Umbilicus Neck Dewlap Scrotum Udder
50 50 50 50 50 20
8.12+ 4.4 18.96_+ 9.8 10.18_+ 5.2 6.64_+ 3.7 41.3 +25.04 12.8 +11.2
22.72+ 7.8 9.8 _+ 6.3 33.2 +14.0 34.64_+ 7.36 7.2 + 3.9 3.2 +_ 2.5
to cause filarial cerebrospinal nematodiasis in abnormal hosts such as sheep, goats and horses (Shoho, 1960). The significance of finding high prevalence rates of Onchocerca (with skindwelling microfilariae) and Setaria (with blood-dwelling microfilariae) in an area where human onchocercosis and elephantosis are endemic cannot be speculated on. However, suffice it to say that it has been proposed that the course of human filariasis may be influenced by the history of exposure to animal filariae, since man is exposed to a variety of infective larvae of non-human filariae that are present in man-biting arthropods (Nelson, 1974).
REFERENCES Braide, E.J., 1981. Evidence of bovine onchocerciasis in Kaduna, Nigeria. Niger. J. Parasitol. 2: 21 23. Chodnik, K.S., 1957. Aortic onchocerciasis due to Onchocerca armiUata in cattle in Ghana, with special reference to the morphology of the parasite. Ann. Trop. Med. Parasitol., 51: 216-224. Eichler, D.A. and Nelson, G.S., 1971. Studies on Onchocerca gutturosa (Neuman, 1910) and its development in Simulium ornatum (Meigen, 1818). 1. Observations on O. gutturosa in cattle in South-East England. J. Helminthol., 45: 245-258. Graber, M., Fernagut, R. and Oumatie, O., 1966. Helminthes des Zebus adultes de la region de Maroua (Nord-Dameroun). Rev. Elev. Med. Vet. Pays Trop., 10: 149-152. Hussein, M.F., Nur, O.A., Gassouma, M.S. and Nelson, G.S., 1975. Onchocerca gutturosa (Neuman, 1910) infection in Sudanese cattle. Br. Vet. J., 131: 76-84. Nelson, G.S., 1966. The pathology of filarial infections. Helminthol. Abstr., 35: 311-336. Nelson, G.S., 1974. Zooprophylaxis with special reference to schistosomiasis and filariasis. In: E.J.L. Soulsby (Editor), Parasitic Zoonoses. Clinical and Experimental Studies. Academic Press, London, pp. 273-285. Nigeria, 1958. Annual Report of the Department of Veterinary Research Nigeria (1956 1957), Government Printers, Lagos, pp. 37 41. Ogunrinade, A.F., 1980. Bovine onchoeerciasis in Nigeria. Ann. Trop. Med. Parasitol. 74:367 368. Schillhorn van Veen, T., 1974. Filariasis in domestic animals in Northern Nigeria and its relation
BOVINEFILARIASISIN ZARIA,NIGERIA
175
to human health. In: E.J.L. Soulsby (Editor), Parasitic Zoonoses. Clinical and experimental Studies. Academic Press, London, pp. 287-293. Schillhorn van Veen, T. and Blotkamp, J., 1972. Rapid staining for microfilariae. J. Parasitol., 58: 446. Schillhorn van Veen, T. and Robl, M.G., 1975. Aortic onchocerciasis in cattle in Zaria (Nigeria). Rev. Elev. Med. Vet. Pays Trop., 28: 305-310. Schillhorn van Veen, T., Bello, S.I. and Folaranmi, D.O.B., 1976. Onchocerca armillata (Railliet and Henry, 1909) from a new hot, Camelur dromedari. Rev. Elev. Med. Vet. Pays Trop., 2: 227 228. Shoho, C., 1960. Studies on cerebrospinal nematodiasis in Ceylon. VII. Experimental production of cerebrospinal nematodiasis by the inoculation of infective larvae of Setaria digitata into susceptible goats. Ceylon Vet., J., 8: 2-12.
171
Short C o m m u n i c a t i o n
P r e v a l e n c e of M i c r o f i l a r i a e in Cattle at S l a u g h t e r in Zaria, N i g e r i a ¥.C. OGBOGU*, 3.M. BABL1S and O.J. AJANUSI
Department of Veterinary Parasitology and Entomology, Ahmadu Bello University Zaria (Nigeria) (Accepted for publication 12 October 1989)
ABSTRACT Ogbogu, V.C., Bablis, J.M. and Ajanusi, O.J., 1990. Prevalence of microfilariae in cattle at slaughter in Zaria, Nigeria. Vet. Parasitol., 36: 171-175. Skin snips and blood taken from 372 randomly selected slaughtered cattle in Zaria, Nigeria were examined for microfilariae. A total of 293 (78.8%) skin snips and 218 (58.6%) blood samples were positive for microfilariae. Two types of microfilariae, identified as Onchocerca armiUata, with a percentage prevalence of 64%, and O. gutturosa with a prevalence of 40% were isolated from the skin. The blood microfilariae were identified as those of Setaria labiatopapillosa
INTRODUCTION
The occurrence of a variety of filarial species in cattle is well documented and they are known to be of wide geographical distribution (Nelson, 1966). In Nigeria, filarial infections are common in domestic animals (Schillhorn van Veen, 1974). Although local surveys are concerned mostly with bovine onchocercosis (Schillhorn van Veen and Robl, 1975; Ogunrinade, 1980; Braide, 1981), little knowledge exists about the different species of Onchocerca and other filarial species present in cattle in Nigeria. This investigation was done as part of wider studies on the host-parasite relationships of both animal and human filariasis in Zaria, Nigeria. MATERIALS AND METHODS
The cattle from which samples were taken were those slaughtered at the main Zaria abattoir. The major breed of cattle encountered was white Fulani (Bunaji). Because most of the animals were trade cattle owned by nomadic or semi-nomadic herdsmen, the origins of the animals could not be determined. However, in recent times, there appears to have been an increase in the number 0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
172
V.C. OGBOGU ET Air.
of sedentary livestock operations, which are managed by non-nomadic herdsmen. A total of 372 randomly selected cattle were sampled. At slaughter, the sex of each animal was recorded. The ages could not be determined owing to the speed of activities on the slaughter floor. However, most of the animals slaughtered were mature. Following the removal of the hide, skin samples were collected from the ear, umbilical area, neck region, dewlap, scrotum or udder of all the cattle sampled. Examination and palpation of the brisket, adjacent abdominal and chest areas for nodules were carried out. In the laboratory, skin tissues of approximately 1 cm ~ were excised from the strips of skin, and were minced with dissecting needles and scapel before incubation in isotonic saline at 37°C for 24 h. Microfilariae were stained with 1% brilliant cresyl blue in ethyl alcohol (Schillhorn van Veen and Blotkamp, 1972) or Giesma before examining for morphological characteristics. For microfilarial densities in different parts of the skin, microfilariae that emerged from I cm 2 skin tissues of 50 positive skin samples each were counted. For blood microfilariae, 10 ml of blood samples were collected from each cattle at slaughter and put into bottles containing EDTA. In the laboratory, 4 ml of each blood sample was examined for microfilariae using wet mounts and the micro-haematocrit methods. Blood smears were made from positive samples. These were stained with either Giemsa or brilliant cresyl blue and were later examined for morphological characteristics. Fifty randomly selected skin or blood microfilariae were measured using an ocular micrometer. R E S U L T S AND D I S C U S S I O N
The prevalence of skin and blood microfilariae is summarized in Table 1. The difference between infection levels in males and females was not significant. Typical Onchocerca microfilariae occurred in the skin of 293 (78.8%) of the cattle sampled. This is a considerably higher number than the previously reported value of 0.3-0.8% in slaughtered cattle in Zaria, based on abattoir TABLE 1 Prevalence of microfilariae in skin and blood samples of Zaria cattle No. of
cattle examined Female Male Total
81 291 372
Skin samples
Blood samples
Mixed infections ~
No. positive
% Positive
No. Positive
% Positive
No. positive
% Positive
59 234 293
72.8 80.4 78.8
53 165 218
65.4 56.7 58.6
47 129 176
58.0 44.3 47.3
~Infections with b o t h skin a n d blood microfilariae.
BOVINE FILARIASIS IN ZARIA,NIGERIA
173
records, (Ogunrinade, 1980). Two types of microfilariae with the morphological characteristics of O. armillata (mean length 295 + 28.5 ttm) and O. gutturosa (mean length 218 + 12.6/~m ) were encountered in the skin. Their prevalence rates are summarized in Table 2. Clearly O. armiUata which occurred in 81.2% of the positive skin samples, but with an overall prevalence of 64%, was the most common. The overall prevalence rates of the two Onchocerca species differed little from previously recorded findings in Zaria (Schillhorn van Veen and Robl, 1975) and in some neighbouring countries (Chodnik, 1957; Graber et al, 1966; Hussein et al., 1975). In addition to infecting cattle, O. armiUata has been found to infect camels in Nigeria (Schillhorn van Veen et al., 1976 ). Onchocerca gibsoni an important species of Onchocerca owing to its use in chemotherapeutic research in human onchocerciasis was not encountered in this study. It seems very likely that this species is not present in Nigeria and other parts of Africa. Although the occurrence of O. gibsoni had been reported from North Eastern parts of Nigeria (Nigeria, 1958), the accuracy of the identification of the isolated worm is open to doubt. This is because the morphological characteristics described for the worms, did not compare completely with the known morphology of O. gibsoni (Schillhorn van Veen, 1974). The densities of O. armiUata and O. gutturosa microfilariae in different skin sites are shown in Table 3. For O. armiUata, the highest density was recorded in the scrotum and the lowest in the umbilicus. For O. gutturosa the highest density was in the neck region and the lowest in the udder. It has been suggested that the concentration of microfilariae in the skin is influenced by the biting habits of the vector host (Eichler and Nelson, 1971). However, in Nigeria, the intermediate hosts for the Onchocerca species are not yet known. Blood microfilariae were present in 218 (58.6%) of the cattle sampled. The microfilariae were sheathed and had a mean length of 215 + 7.06 ttm. They were identified as those of Setaria labiatopapillosa. The adult worms inhabit the peritoneal cavity and are non-pathogenic. However, the larvae have been shown TABLE 2 Prevalence of O. arrnillata and O. gutturosa microfilariae in positive skin samples No. of positive cattle Females Males Total
59 234 293
O. armiUata
O. gutturosa
Mixed infections
No. positive
% Positive
No. Positive
% Positive
No. Positive
% Positive
46 192 238
78.0 82.1 81.2 (64) 1
27 144 171
45.8 61.5 58.4 (46)
15 93 108
25.4 39.7 36.9 (29.0)
1Figures in parenthesis indicate percentage prevalence in total n u m b e r of cattle sampled.
174
V.C. OGBOGUET AI..
TABLE 3 Microfilarial densities in skin specimens (mean counts of microfilariae per 1 cm ~ of skin) Skin sample site
No. of positive skin specimens taken
O. armillata
O. gutturosa
Ear Umbilicus Neck Dewlap Scrotum Udder
50 50 50 50 50 20
8.12+ 4.4 18.96_+ 9.8 10.18_+ 5.2 6.64_+ 3.7 41.3 +25.04 12.8 +11.2
22.72+ 7.8 9.8 _+ 6.3 33.2 +14.0 34.64_+ 7.36 7.2 + 3.9 3.2 +_ 2.5
to cause filarial cerebrospinal nematodiasis in abnormal hosts such as sheep, goats and horses (Shoho, 1960). The significance of finding high prevalence rates of Onchocerca (with skindwelling microfilariae) and Setaria (with blood-dwelling microfilariae) in an area where human onchocercosis and elephantosis are endemic cannot be speculated on. However, suffice it to say that it has been proposed that the course of human filariasis may be influenced by the history of exposure to animal filariae, since man is exposed to a variety of infective larvae of non-human filariae that are present in man-biting arthropods (Nelson, 1974).
REFERENCES Braide, E.J., 1981. Evidence of bovine onchocerciasis in Kaduna, Nigeria. Niger. J. Parasitol. 2: 21 23. Chodnik, K.S., 1957. Aortic onchocerciasis due to Onchocerca armiUata in cattle in Ghana, with special reference to the morphology of the parasite. Ann. Trop. Med. Parasitol., 51: 216-224. Eichler, D.A. and Nelson, G.S., 1971. Studies on Onchocerca gutturosa (Neuman, 1910) and its development in Simulium ornatum (Meigen, 1818). 1. Observations on O. gutturosa in cattle in South-East England. J. Helminthol., 45: 245-258. Graber, M., Fernagut, R. and Oumatie, O., 1966. Helminthes des Zebus adultes de la region de Maroua (Nord-Dameroun). Rev. Elev. Med. Vet. Pays Trop., 10: 149-152. Hussein, M.F., Nur, O.A., Gassouma, M.S. and Nelson, G.S., 1975. Onchocerca gutturosa (Neuman, 1910) infection in Sudanese cattle. Br. Vet. J., 131: 76-84. Nelson, G.S., 1966. The pathology of filarial infections. Helminthol. Abstr., 35: 311-336. Nelson, G.S., 1974. Zooprophylaxis with special reference to schistosomiasis and filariasis. In: E.J.L. Soulsby (Editor), Parasitic Zoonoses. Clinical and Experimental Studies. Academic Press, London, pp. 273-285. Nigeria, 1958. Annual Report of the Department of Veterinary Research Nigeria (1956 1957), Government Printers, Lagos, pp. 37 41. Ogunrinade, A.F., 1980. Bovine onchoeerciasis in Nigeria. Ann. Trop. Med. Parasitol. 74:367 368. Schillhorn van Veen, T., 1974. Filariasis in domestic animals in Northern Nigeria and its relation
BOVINEFILARIASISIN ZARIA,NIGERIA
175
to human health. In: E.J.L. Soulsby (Editor), Parasitic Zoonoses. Clinical and experimental Studies. Academic Press, London, pp. 287-293. Schillhorn van Veen, T. and Blotkamp, J., 1972. Rapid staining for microfilariae. J. Parasitol., 58: 446. Schillhorn van Veen, T. and Robl, M.G., 1975. Aortic onchocerciasis in cattle in Zaria (Nigeria). Rev. Elev. Med. Vet. Pays Trop., 28: 305-310. Schillhorn van Veen, T., Bello, S.I. and Folaranmi, D.O.B., 1976. Onchocerca armillata (Railliet and Henry, 1909) from a new hot, Camelur dromedari. Rev. Elev. Med. Vet. Pays Trop., 2: 227 228. Shoho, C., 1960. Studies on cerebrospinal nematodiasis in Ceylon. VII. Experimental production of cerebrospinal nematodiasis by the inoculation of infective larvae of Setaria digitata into susceptible goats. Ceylon Vet., J., 8: 2-12.