THE PREVALENCE OF GASTROINTESTINAL PARASITES IN WILD AND DOMESTIC ANIMALS IN RADOM NATIONAL PARK; SOUTH DARFUR STATE, SUDAN

THE PREVALENCE OF GASTROINTESTINAL PARASITES IN WILD AND DOMESTIC ANIMALS IN RADOM NATIONAL PARK; SOUTH DARFUR STATE, SUDAN

ABUESSAILLA, A.A.^*; ISMAIL, A.A.^** and AGAB, H.^***

^* Ministry of Animals Resources and Fisheries, South Darfur State. Email: atifabuessailla@yahoo.com.

^** Department of Pathology, Parasitology and Microbiology, College of Veterinary Medicine, Sudan University of Sciences and Technology. Email:ahmedaliismail@gmail.com.

^***Department of Fisheries and Wildlife Science, College of Animal Production Science and Technology, Sudan University of Science and Technology. Email:hamidagab1@hotmail.com (Corresponding author). Current address: The Arab Centre for the Studies of Arid Zones and Dry Lands (ACSAD), Cairo Office, P O Box 12619, Giza, Cairo, Egypt. Cell Phone: 00 20 1091971806.

INTRODUCTION

The available information on parasitic infection among wildlife species, particularly in the Sudan, is scanty. There are few scattered published papers in scientific journals. Eisa et al. (1979) published a check-list of helminth parasites of domestic and wild animals in Sudan during the period 1902 – 1975. According to these authors, Cysticercus tenuicollis was reported in the reedbuck, monkey and kob; Cysticercus pisiformis in the rabbit; Trichuris spp. was reported in the monkey and gazelle; Toxocara canis was reported in cheetah and wild cat; Setaria labiatopapillosus in the reedbuck; Trichostrongylus spp. in the giraffe; Ascaris lumbricoides in the wild pig; Strongyloid spp. in the gazelle; Ascaris pythonis in the python and Toxascaris leonina in the lion. All the investigated faecal matters for the above mentioned findings were collected from wildlife species kept in captivity at Khartoum Zoo. Saad and Eisa (1980) surveyed the parasites of seven hussar monkeys in which they reported the presence of three helminthes, namely; Streptophagus pigmentatus, Oesophagostomum biforcum and Trichuris trichura. They noticed that, although some wild mammals are infected by endoparasites, however, they did not show any clinical evidence of disease or health deviation despite the presence of these parasites. Laboratory examination of 184 faecal samples collected from 44 species of wild animals kept at Khartoum Zoo (Sudan) revealed the presence of Trichostrongylus eggs in faeces of dorcas gazelles, cheetah, roan antelope, giraffe, red-fronted gazelles, Nubis baboons, vervet monkeys and cape buffaloes (Saad et al., 1983). Free ranging wild animals in Sudan seemed not had been investigated for the prevalence of helminth parasites before. The present study is intended to investigate the prevalence of helminth parasite in free-ranging domestic and wildlife in Radom National Park, South Darfur State, Sudan.

MATERIALS and METHODS

 Study Areas: Radom National Park is located to the south-west of Lake Kundi on the border with the Central Africa Republic, in the south-western corner of Southern Darfur State. The park consists of an area of broken hilly country lying between two main rivers, the Adda and the Umbelasha. Radom was declared a Biosphere Reserve in 1979 by the International Union for Conservation of Nature (IUCN) (1987). The vegetation is principally heavy savannah woodland dominated by some bush trees such as Terminalia brownii, Combretum spp., Anogeissus leiocarpus and Isoberlinia doka.

Collection and examination of faecal samples: The study was doneduring the period from December, 2010 to December, 2011. A total of 1179 faecal samples were collected from the five sites namely: Radom area, Alhufra, Titrbi, Kafindibei and Kafiakingi. 10% formaldehyde solution was added to the collected faecal samples, then the samples were put in nylon bags, labeled then transported to the Veterinary Laboratory in Nyala for examination. In the laboratory, two qualitative techniques, namely floatation and sedimentation techniques were used for separation, concentration and demonstration of parasite eggs and oocysts in the collected faecal samples. Both techniques were done following the method described by FAO (2006). Results of faecal examination were analyzed using Chi – square analysis methods.

RESULTS

Frequencies and distributions of the test samples by type, species, and area are presented in Table 1. Almost equal numbers of samples were collected from both domestic animals (600 samples) and wildlife (579 samples) (Table 1). Domestic animals were available within the study areas and were easy to catch and sample. Within the wildlife groups, the Dikdik represented the highest sampled animal. Conversely, the bushbuck and the leopard represented the lowest species sampled (Table1).

Generally, eggs of internal parasites were detected in the study area with variations observed in the prevalence between different types, species, and areas as presented in Table 2. The overall prevalence was 9.8% (115/1179) with 95% CI between 8.1 and 11.5.

The prevalence estimated in the two types with domestic animals had the high prevalence of 9.8% (59/600), with 95% CI between 7.42 and 12.18, and wild animals showed the low prevalence of 9.7% (56/579), with 95% CI between 7.29 and 12.11, as presented in Table 2.  

Among the infected animals, the leopard (Panthera pardus) had the highest prevalence (50%) (6/12), with 95% CI between 21.71 and 78.29, and Patas monkey (Erythrocebus patas) showed the lowest prevalence (2.7%) (1/37), with 95% CI between -2.52 and 7.92, as presented in Table 2. Radom area showed the highest prevalence of internal parasites (13.9%) (49/352), with 95% CI between 10.29 and 17.51, followed by Kafiakingi with a prevalence of 9.3% (27/289), with 95% CI between 5.95 and 12.65, whereas Alhufra showed the lowest prevalence (5.4%) (7/129), with 95% CI between 1.5 and 9.3 (Table 2).

Table 1: Frequencies and distributions of examined faecal samples by type, species and area for internal parasites in Radom National Park, South Darfur State.

Out of all internal parasites identified in the present study, Toxocara spp. Recorded the highest prevalence rate (7.4%), followed by Oesophagostomum spp. (3.6%), then Haemonchus spp. (1.4%) and finally Ascaris spp. (1.2%).

The univariate associations with positive status against Ascaris:

The proportions of positive results differed between type, species, and area. In the univariate analysis using chi square, type (p-value = 0.037) and species (p-value = 0.000) were significantly associated with floatation and sedimentation methods of identification for Ascaris infection. However, area (p-value=0.577) was not significantly associated with floatation and sedimentation methods of identification for Ascaris infection. 

Table 2: Prevalence of internal parasites by type, species, and area in Radom National Park South Darfur State (December 2010 - December 2011).

The prevalence of Ascaris infection in the wildlife was low (0.5%) (3/579), with 95% CI ± 0.57, while in the domestic animals was higher (1.8%) (11/600), with 95% CI ± 1.06.

Regarding prevalence of Ascaris per animal species, Bushbuck (Tragelaphus scriptus) had the highest prevalence (18.2%) (2/11), with 95% CI ± 22.8, and Dikdik (Madaqua guentheri) showed the lowest prevalence (1%) (1/101), with 95% CI ±1.94. All domestic animals were free of parasitic infection except sheep which has only eleven positive samples out of 138 samples examined. All wildlife infected by Ascaris eggs were ruminant animals.

As for the prevalence of Ascaris per area or site of sample collection, Radom area showed the highest prevalence (1.7%) (6/352), with 95% CI ± 1.35, whereas Kafiakingi showed the lowest prevalence (1%) (3/289), with 95% CI ± 1.15.

 For Toxocara infection, the proportions of positive results differed between type, species and area. In the univariate analysis using chi square, type (p-value = 0.000) and species (p-value = 0.000) were significantly associated with floatation and sedimentation methods of identification. However, area (p-value=0.778) was not significantly associated with floatation and sedimentation methods of identification for Toxocara infection.

For the prevalence of Toxocara by animal type, the wildlife had a prevalence of 7.4% (43/579), with 95% CI ± 2.13, whereas the domestic animals were not infected at all with Toxocara (0%) (0/600), with 95% CI ± 0.

Regarding the prevalence of Toxocara by animal species, the leopards (Panthera pardus) had a prevalence of 50% (6/12), with 95% CI ± 28.29, and the warthog (Phacochoerus aethiopicus) showed a lower prevalence (4%) (3/75), with 95% CI ±4.43.

For the prevalence of Toxocara infection by area (site of sample collection), Kafiakingi showed a prevalence of 4.5% (13/289), with 95% CI ± 2.39, and Alhufra showed a lower prevalence (2.3%) (3/129), with 95% CI ± 2.59.

The proportions of positive results for Haemonchus infection differed between type, species, and area. In the univariate analysis using chi square, species (p-value = 0.000) were significantly associated with floatation and sedimentation methods of identification for Haemonchus infection. However, type (p-value = 0.150) and area (p-value=0.135) were not significantly associated with floatation and sedimentation methods of identification for this parasite.

For the prevalence of Haemonchus infection by animal type, the wild animals had lower prevalence (0.9%) (5/579), with 95% CI ± 0.77 compared to the domestic animals which had a prevalence of 1.8% (11/600), with 95% CI ± 1.06. Concerning the prevalence of Haemonchus by animal species, the reedbuck (Redunca redunca) had a prevalence of 17.6% (3/17), with 95% CI ± 18.1, while goats showed a lower prevalence (1.2 %) (2/161), with 95% CI ± 1.68.

As far as the area of sampling is concerned, Radom area showed the highest prevalence of Haemonchus (2.6%) (9/352), with 95% CI ± 1.66, and Alhufra showed the lowest prevalence (0.8%) (1/129), with 95% CI ± 1.54.

The proportions of positive results for Oesophagostomum infection differed between type, species and area. In the univariate analysis using chi square, type (p-value = 0.000) and species (p-value = 0.000) were significantly associated with floatation and sedimentation methods of identification for Oesophagostomum infection. However, area (p-value=0.010) was not significantly associated with floatation and sedimentation methods of identification for this parasite.

The prevalence of Oesophagostomum by animal type showed that the wild animals had lower prevalence (0.9%) (5/579), with 95% CI ± 0.77, compared to the domestic animals which showed higher prevalence (6.2%) (37/600), with 95% CI  ± 1.93. Cattle had the highest prevalence (16.7%) (22/132), with 95% CI ± 6.36, while Patas monkeys (Erythrocebus patas) showed the lowest prevalence (2.7%) (1/37), with 95% CI ± 5.22.

Considering the prevalence of Oesophagostomum by area of faecal sample collection, Radom area showed the highest prevalence (6.5%) (23/352), with 95% CI ± 2.58, in contrast to Titrbi whichshowed the lowest prevalence (1.6%) (3/184), with 95% CI ± 1.81.

DISCUSSION

In the present study, wild and domestic animal species in Radom National Park, South Darfur State (Sudan), were investigated for gastrointestinal helminths by examination of faecal samples, gastrointestinal tracts and detection of pasture contamination in the study area.The present study confirmed the presence of Ascaris spp. as the most predominant parasite of Bushbuck (Tragelaphus scriptus) in Radom area. Ascaris worms are known to have a wide range of hosts andwere formerly reported in waterbuck in Lake Mburo National Park in Uganda (Ocaido et al., 2004).

The prevalence of Toxocara spp.parasites in the study areawas higher (63.51%) in the rainy season as compared to the winter season (50%).Thefirst report of Toxocara cati in wildlife was in the leopard (Panthera pardussaxicolor)in Iran and was documented byEsfandiari et al. (2010). It was also reported in tiger, lion, leopard and jungle cat in India (Mahali et al., 2010). Toxocara worms were recovered in the faeces of Nubis baboons, Hussar monkeys, Asmara gazelle and lion by Saad et al. (1983). It was also reported in a tiger and a lion in Khartoum Zoo, Sudan (Saad et al., 1983). Similar results were also recorded in the present study where Toxocara spp. eggswere reported in leopards (Panthera pardus) in Kafiakingi where these worms had the highest prevalence in leopards (50%) than in other animals in the study area. It worths mentioning that Kafiakingi was more populated with feline and canine animals compared to the other remaining four study sites. These results indicated that all domestic animals were free of infection since they are not the right hosts for this parasite.

The results of this study confirmed that Haemonchus spp. was the most predominant parasite of Reedbuck (Redunca redunca) in Radom area. Furthermore, Haemonchus spp. was found to be more prevalent in small ruminants (sheep and goats). The samples collected from reedbuck were few (only 17) compared to these collected from sheep (138) or goats (161). This could be the reason that the reedbuck represented the highest percentage of infection. Haemonchus spp. wasreported as the most predominant parasite in South Africa in mountain Reedbuck (Redunca fulvorufula) (Boomker et al., 1989). It was also reported in the Loskop Dam Nature Reserve and the Mountain Zebra National Park (Boomker et al., 1983). Haemonchus contortus is a cosmopolitan helminth parasite of sheep and goats (Chaudary et al., 2007). It was also reported in blue wildebeest and Kudu in South Africa (Ilana et al., 2011). Haemonchus species diagnosed in sheep and goats were not identified to species level, however, most probably they were Haemonchus contortus. The different species of genus Haemonchus had a wide range of domestic animal hosts as it is a known and widely spread ruminant parasite (Soulsby, 1982).

Oesophagostomum spp. wasreported as the most predominant parasite in cattle in the neighboring Abyei area (Idriss et al., 2012). Oesophagostomum eggs were found in the faeces of Warthog (Phacochoerus aethiopicus) in Dinder National Park (Sudan) by Dunn (1978). Also Oesophagostomum dentatum wasreported as a helminth of swine. Oesophagostomum macombiquei was described from 9 females of Warthog (Phacochoerus aethiopicus)by Boomker (1990) in northern Mozambique. Also Oesophagostomum spp. was reported in water buffaloes in Bangladesh (Islam et al., 1992). A high prevalence of Oesophagostomum infection in cattle (44.7%) was reported in Pakistan by Farooq et al. (2012). The present study confirmed that Oesophagostomum spp. was the most predominant parasite of cattle in Radom area. However, Oesophagostomum spp. had the highest prevalence in cattle (16.7%) than in other animals in the study area which might be due to differences in feeding behaviour as domestic animals are found grazing as a herd and often mixed up with other herds on communal type of pastures. Oesophagostomum is a mainly ruminant parasite.

Therefore, depending on the results of this study, it is recommended to conduct more research and surveys for internal parasites in the Radom National Park to confirm the findings of this study. It is also recommended that the government should provide adequate veterinary and animal health extension services in Radom National Park in order to improve the health condition of both domestic and wildlife and to create the necessary awareness among animal owners in the study area.

ACKNOWLEDGEMENTS

The technical assistance of Mr. S. A. Noja is acknowledged. Due thanks are extended to the staff of Nyala Veterinary Research Laboratory for their help and encouragement. Special acknowledgement and great appreciation to General Administration of Wildlife Protection Department, Nyala Sector, for help and assistance during the field work.

REFERENCES

Boomker, J.; Du Plessis, W.H. and Boomker, E.A. (1983): Some helminth and arthropod parasites of the grey  duiker (Sylvicapragrimmia). Journal of Veterinary Research. Vol. 50(4): 233-41.

Boomker, J.; Horak, I.G.; Flamand, J. and Keep, M.E. (1989): Parasites of South African wildlife. Helminths of common reedbuck (Redunca arundinum) in Natal. Journal of Veterinary Research. Vol. 56(1): 51-7.

Boomker, J. (1990): Parasites of South African Wildlife. V.A.  Description of the males of Oesophagostomum mocambiquei (Ortlepp, 1964) from warthogs (Phacochoerus aethiopicus) (Pallas, 1766).  J. Vet. Res., 57(3): 169–173.

Chaudary, F.R.; Khani, M.F.U. and Qayyum, M. (2007): Prevalence of Haemonchus contortus in naturally infected small ruminants grazing in the Potohar Area of Pakistan. Pakistan Vet. J., 27(2): 73-79. 73.

Dunn, A.M. (1978): Textbook of Veterinary Helminthology, 2^nd. edn. William Heinemann Medical Books Ltd., London.

Eisa, A.M.; El Bedawi, E.S.; Saad, M.B.; Ibrahim, A.M. and El Gezuli, A.Y. (1979): Check list and first records of helminth parasites of domestic and wild animals reported in Sudan during 1902 – 1975. Sud. J. Vet. Res. (1):    55–63.

Esfandiari, I.B.; Youssefi, M.R. and Tabari, M.A. (2010): First Report of Toxocara cati in Persian Leopard (Pantherpardussaxicolor) in Iran Global Veterinaria. Vol. 4 (4): 394-395.

FAO (2006): Techniques for parasite assays and identification in faecal samples. Management of vertisols in Sub-Saharan Africa. Proceedings of Conference. Available at:  http://www.fao.org/Wairdocs/ILRI/x5492E/x5492e05.htm

Farooq, Z.; Mushtaq, S.; Iqbal, Z. and Akhtar, S. (2012): Parasitic helminths of domesticated and wild ruminants in Cholistan Desert of Pakistan. Int. J. Agric. Biol., 14: 63–68.

Idriss, B.G.; Atif, E.A. andKhitma,H.E. (2012): Study on prevalence of parasitic diseases in cattle in Abyei Area, Sudan. Journal of Cell and Animal Biology. Vol. 6(6): 88-98.

Ilana, C.; Van, W. and Boomker, J. (2011): Parasites of South African wildlife. The prevalence of helminths in some common antelopes, warthogs and a bush pig in the Limpopo Province, South Africa. J. Vet. Res., Vol.78 (1), Cape Town.

 Islam, F.M.S.; Rahman, M.H. and Chowdhury, S.M.Z.H. (1992): Prevalence of parasites of water buffaloes in Bangladesh. Animal Health Research Division, Vol.5 (4): 601-604.

IUCN (1987): (International Union for Conservation of Nature) Radom Bird Life Datazone,  P.p. 6811. 

Mahali, A.K.; Panda, D.N.; Panda, M.R.; Mohanty, B.N. andSahoo, N.(2010): Incidence and seasonal variation of gastro-intestinal parasitic infections in captive carnivores in Nandankanan Zoological Park, Orissa. Journal of Veterinary Parasitology. Vol. 24 (2):      111-115.

Ocaido, M.; Serifert, L. and Baranga, J. (2004): Helminth risks associated with mixed game and livestock interactions in and around Lake Mburo National Park, Uganda. Afr. J. Ecol., 42: 42–48.

Saad, M.B. and Eisa, A.M. (1980): Helminth parasites of the Hussar monkeys (Erythrocebus patas) from Khartoum Zoo. Sud. J. Vet. Sci. Anim. Husb., 2: 101.

Saad, M.B.; El Mubarak, K.A. and El Badawi, K.S. (1983): Endoparasites in wild animals in Khartoum Zoo. Bull. Anim. Hlth. Prod. Afr.  (31): 9 – 15.

Soulsby, E.J.L. (1982): Helminths, Arthropods and Protozoa of Domesticated Animals. 7^th ed. Lea and Febiger, Philadelphia, Pennsylvania,      809 pp.