Prevalence of Toxoplasma gondii antibodies in pastoral camels (Camelus dromedarius) in the Butana plains, mid-Eastern Sudan

Prevalence of Toxoplasma gondii antibodies in pastoral camels (Camelus dromedarius) in the Butana plains, mid-Eastern Sudan

Veterinary Parasitology, 43 (1992) 171-175 Elsevier Science Publishers B.V., Amsterdam 171 Prevalence of Toxoplasma gondii antibodies in pastoral ca...

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Veterinary Parasitology, 43 (1992) 171-175 Elsevier Science Publishers B.V., Amsterdam

171

Prevalence of Toxoplasma gondii antibodies in pastoral camels ( Camelus dromedarius) in the Butana plains, mid-Eastern Sudan E.A. Elamin a, S. Elias a, A. Daugschies b and M. Rommel b aDepartment of Parasitology, Faculty of Veterinary Science, University of Khartoum, PO Box 32, Khartoum-North, Sudan blnstitut fur Parasitologie, Tieriirztliche Hochschule Hannover, Biinteweg 17, W-3000 Hannover 71, Germany (Accepted 19 December 1991 )

ABSTRACT Elamin, E.A., Elias, S., Daugschies, A. and Rommel, M., 1992. Prevalence of Toxoplasma gondii antibodies in pastoral camels (Camelus dromedarius) in the Butana plains, mid-Eastern Sudan. Vet. Parasitol., 43: 171-175. A total of 482 serum samples from pastoral camels in the Butana plains, mid-Eastern Sudan, were tested for Toxoplasma antibodies by the latex agglutination test (LAT). Sixty-seven percent of the camels were seroreactive. The prevalence rate of seroreactivity increased significantly with age (P< 0.01 ) and was highest among camels aged over 7 years (74.2%). The prevalence rate of seropositivity decreased proportionally with the level of serum dilution. At dilutions of 1 : 32 and above, the prevalence rate was 25.9%. There were no sex-linked differences in seroreactivity. This study suggests widespread infection with Toxoplasma gondii among pastoral camels, a finding that warrants a closer look into the possible ways infection is acquired by camels in their arid environment, its economic impact, as well as its public health significance, especially among the nomads who consume cameline milk and liver raw.

INTRODUCTION

Toxoplasma gondii is a heteroxenous coccidian parasite. The definitive hosts are domestic cats and various species of wild felids. The intermediate hosts are m a m m a l s and birds. The infection has been found in many zoogeographic regions and high reactor rates were found among domestic animals (reviewed by Dubey and Beattie (1988). In camels, Toxoplasma antibodies were reported in India (Gill and Prakash, 1969), in Egypt (Michael et al., 1977; Fahmy et al., 1979), in Saudi Arabia (Hossain et al., 1987; Hussein et al., Correspondence to: A. Daugschies, Institut ftir Parasitologie, Tier~irztliche Hochschule Hanhover, Biinteweg 17, W-3000 Hannover 71, Germany.

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E.A. ELAMIN ET AL.

1988) and in the Sudan (El Din et al., 1985; Bornstein and Musa, 1987; Abbas et al., 1987). Most of the samples evaluated for Toxoplasma antibodies in these studies were from farm-kept camels or from slaughtered camels with an unknown history of management conditions. The purpose of this study was to determine the prevalence of Toxoplasma antibodies in pastoral camels of the Butana plains, mid-Eastern Sudan. MATERIALS AND METHODS

Camels owned by nomads in the Butana plains were surveyed for serum antibodies against Toxoplasma. The territory is largely semi-arid, and provides a traditional grazing and browsing domain for camels. Blood was obtained from camels pasturing the area, wherever they were encountered, by jugular venipuncture into a plain vacutainer (Becton-Dickinson, Meylan, France). Blood samples were left to clot overnight at 4 °C and sera were decanted into plastic tubes. Separated sera were stored at - 2 0 ° C . The age of the camels was estimated from the dentition. A total of 482 serum samples were tested for Toxoplasma antibodies by the latex agglutination test (LAT) using Toxoreagent, Eiken Test Kit (Eiken Chemical Co., Tokyo, Japan ). The test was performed on U-shaped microtiter plates (Titertek, Flow Laboratories, Meckenheim, Germany). Each serum sample was screened at two-fold dilution ranging from 1 : 8 to 1 : 256. The data were analyzed statistically by the M a n n - W h i t n e y U-test. Correlation of seroreactivity with age a n d / o r sex was estimated by calculation of Kendall's r. RESULTS

Out of 482 pastoral camels surveyed for Toxoplasmaantibodies, 323 (67%) were seroreactive. Figure 1 shows the frequency distribution of Toxoplasma antibodies among the surveyed population. The prevalence rate of seropositivity decreased proportionally with the level of serum dilution. Thus, reading the test at the dilution rate of 1 : 32 and above, the prevalence rate of seropositivity is 25.9%. Table 1 shows the breakdown of the seroreactor camels in relation to sex. The overall prevalence rate among female (22.7%) and male (29.1% ) camels does not indicate a sex-linked difference ( P > 0.05). This is also evident at each of the serum dilution levels tested. There were no significant sex-linked differences in mean antibody titers. The prevalence rate in each age group is shown in Table 2. The prevalence rate of seroreactor camels increased from 62.5% at 1 year and below to 74.2% in camels aged over 7 years. Seroreactivity correlated significantly with age (P
173

PREVALENCE O F TOXOPLASMA A N T I B O D I E S IN PASTORAL CAMELS tw ~Bot

32.99%

t~

26.35%

F tao p e q i~u e 80-

14.11%

14.73%

Y

I I

o

5.~.g% 3.53% .3.llg I

t6

8

I ~

, ~

, ta

Rec~.procal Titer

Fig. 1. Frequency distribution of T. gondii antibodies (LAT) for the surveyed population of pastoral camels of the Butana plains, mid-Eastern Sudan.

TABLE1 Numberofmaleand ~malecamelsseroreactiveto Z gondiiatdifferentserum dilutions Titer 1:8

1:16

1:32

1:64

1:128

2 1:256

Total

Male (%) Female (%)

59 (24.2) 68 (28.6)

41 (16.8) 30 (12.6)

39 (16.0) 29 (12.2)

16 (6.6) 9 (3.8)

9 (3.7) 8 (3.4)

7 (2.9) 8 (3.4)

244 (50.6) 238 (49.4)

Total (%)

127 (26.3)

71 (14.7)

68 (14.1)

25 (5.2)

17 (3.5)

15 (3.1)

482 (100)

TABLE2 PrevalenceofT gondiiantibodyamongdifferentagegroupsofcamels Age group (years)

Number tested

~1 2-3 4-5 6-7 >7

16 24 63 119 260

Total

482

% of total number tested 3.32 4.98 13.07 24.69 53.94 100.0

Number of seroreactors

% of seroreactivity within age group

10 II 36 73 193

62.50 45.83 57.14 61.34 74.23

323

67.01

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E.A. ELAMIN ET AL.

DISCUSSION

The results of this study indicate that Toxoplasma antibodies are widespread among pastoral camels in mid-Eastern Sudan. This is not surprising in view of the ubiquity of this protozoan parasite in other countries and its loose host specificity among various mammals and birds. Transmission and, subsequently, the infection rates in one host species depend on multiple factors that include the proximity to domestic cats, climatic conditions and the type of soil (reviewed by Fayer and Reid (1982). Acquisition of Toxoplasma infection by camels is thought to occur through ingestion or inhalation of sporulated oocysts that are shed by cats in the environment. The Butana plains, which are semi-arid, as well as all areas that the camels enter during their nomadic migration, are conspicuous by the absence of domestic cats, both roaming and pets. It seems reasonable, therefore, to associate the infection in such an environment with the existence of wild cats (Felis silvestris lybica) in the territory. Similar findings demonstrating Toxoplasma antibodies in the non-carnivorous fauna of neotropical forests (where there are no domestic cats) have been reported (Jewell et al., 1972 ). In the present study, the rate of seropositivity among nomadic herds was 25.9% using LAT (titer 1 : 32 or greater). Variable seropositivity tests were reported among camels in the Sudan and elsewhere. None of 46 camels that were slaughtered at an abattoir in Saudi Arabia with an unknown management history was seropositive for Toxoplasma (Hossain et al., 1987). Hussein et al. ( 1988 ) found a 16% prevalence rate of seropositivity among Saudi camels. The prevalence rate was much higher in farm-kept camels ( 10-63% ) than in camels from nomadic herds (5.5%). Using the indirect hemagglutination test (IHA), seropositivity rates of 12% (Abbas et al., 1987), 22.5% (Bornstein and Musa, 1987) and 54% (El Din et al., 1985) were reported in slaughter camels from Sudanese abattoirs. Our finding that there is no sex-linked difference in seroreactivity among camels is in line with the report by Fahmy et al. (1979) for camels in Egypt. Hussein et al. (1988) reported a much higher prevalence rate of seropositivity in females than in males in Saudi Arabian camels, reflecting the effects of husbandry methods on acquisition of the Toxoplasma infection. Most of the females investigated in this study were from farms where domestic cats occur. In contrast, the males are mainly kept by nomads and thus the risk of coming into close contact with domestic cats is low. In the Butana region, pastoral camels of both sexes would be at the same risk of ingesting oocysts in view of the rearing system and herd composition. A positive correlation between seroreactivity and age among camels reported in this study supports the findings o f F a h m y et al. ( 1979 ) and Hussein et al. (1988). Similar patterns of prevalence were reported in populations of man and many animal species (for the literature, see Dubey and Beattie

PREVALENCE OF TOXOPLASMA ANTIBODIES IN PASTORAL CAMELS

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(1988)). It is conceivable that the longer an animal lives, the greater the chance of it being exposed to Toxoplasmaoocysts. In conclusion, the widespread prevalence of Toxoplasma antibodies among pastoral camels warrants a closer look into its economic impact, as well as its public health significance, especially among the nomads who consume cameline milk and liver raw. It is worth noting that acute clinical toxoplasmosis has recently been reported in a camel in the USA (Hagemoser et al., 1990). ACKNOWLEDGMENTS

This work was supported by the Hannover/Khartoum-Link between Tier/irztliche Hochschule Hannover, Hannover, Germany, and the Faculty of Veterinary Science, University of Khartoum. The authors thank Mr. Babiker Adlan and Mr. Mohammed E1 Hassan Ahmed for their assistance in bleeding the camels.

REFERENCES Abbas, B., El Zubair, A.E.A. and Yassin, T.T.M., 1987. Survey for certain zoonotic diseases in camels in Sudan. Rev. 121ev. M6d. Vdt. Pays Trop., 40: 231-233. Bornstein, S. and Musa, B.E., 1987. Prevalence of antibodies to some viral pathogens, Brucella abortus and Toxoplasma gondii in serum from camels (Camelus dromedarius) in Sudan. J. Vet. Med. B, 34: 364-370. Dubey, J.P. and Beattie, C.P., 1988. Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, 220 pp. E1 Din, E.A.Z., El Khawad, S.E. and Kheir, H.S.M., 1985. A serological survey for Toxoplasma antibodies in camels (Camelus dromedarius) in the Sudan. Rev. l~lev. M6d. V6t. Pays Trop., 38: 247-249. Fahmy, M.A., Mandour, A.M., Arafa, M.S. and Abdel Rahman, B.M., 1979. Toxoplasmosis of camels in Assiut governorate. J. Egypt. Vet. Med. Assoc., 39:27-31. Fayer, R. and Reid, W.M., 1982. Control of coccidiosis, In: P. Long (Editor), The Biology of the Coccidia. University Press, Baltimore, MD, pp. 453-487. Gill, H.S. and Prakash, O., 1969. Toxoplasmosis in India: Prevalence of antibodies in camels. Trop. Med. Parasitol., 63: 265-267. Hagemoser, W.A., Dubey, J.P. and Thompson, J.R., 1990. Acute toxoplasmosis in a camel. J. Am. Vet. Med. Assoc., 196: 347. Hossain, A., Bolbol, A.S., Bakir, T.M.F. and Bashandi, A.M., 1987. A serologic survey of the prevalence of Toxoplasma gondii in slaughtered animals in Saudi Arabia. Ann. Trop. Med. Parasitol., 81: 69-70. Hussein, M.F., Bakkar, N., Basmaeil, S.M. and Gar El Nabi, A.R., 1988. Prevalence of toxoplasmosis in Saudi Arabian camels ( Camelus dromedarius). Vet. Parasitol., 28: 175-178. Jewell, M.L., Frenkel, J.K., Johnson, K.M., Reed, V. and Ruiz, A., 1972. Development of Toxoplasma oocysts in neotropical Felidae. Am. J. Trop. Med. Hyg., 21 : 512-517. Michael, S.A., El Refaii, A.H. and Morsy, T.A., 1977. Incidence of Toxoplasma antibodies among camels in Egypt. J. Egypt. Soc. Parasitol., 7: 129-132.