Detection of Trypanosoma Brucei Gambiense Specific Li Tat 1.3 Antibodies in Humans and Cattle in Taraba State, North- Eastern Nigeria

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1 Journal of Veterinary Advances Detection of Trypanosoma Brucei Gambiense Specific Li Tat 1.3 Antibodies in Humans and Cattle in Taraba State, North- Eastern Nigeria Karshima N. S., Ajogi I., Lawal A. I., Mohammed G. and Okubanjo O. O. J Vet Adv 2012, 2(12): Online version is available on:

2 ISSN: KARSHIMA ET AL. Original Article Detection of Trypanosoma Brucei Gambiense Specific Li Tat 1.3 Antibodies in Humans and Cattle in Taraba State, North-Eastern Nigeria 1 Karshima N. S., 2 Ajogi I., 3 Lawal A. I., 4 Mohammed G. and 3 Okubanjo O. O. 1 Department of Animal Health, Federal College of Animal Health and Production Technology, PMB 001, Vom, Plateau State, Nigeria. 2 Department of Veterinary Public Health and Preventive Medicine,Ahmadu Bello University, Zaria, Nigeria. 3 Department of Veterinary Parasitology and Entomology, Ahmadu Bello University, Zaria, Nigeria. 4 Department of Veterinary Surgery and Medicine, Ahmadu Bello University, Zaria, Nigeria. Abstract In a prevalence study of Trypanosoma brucei gambiense in humans and cattle in Taraba State, blood samples from 400 each of humans and cattle were examined for the presence of T. b. gambiense Li Tat 1.3 surface antibodies using the Card agglutination test for T. b. gambiense (CATT). The overall prevalence rates were 1.8% (7/400) and 9.25% (37/400) for humans and cattle respectively. In humans, the highest prevalence of 5.7% (4/70) was observed in Gashaka Local Government Area (LGA). This was followed by Karim Lamido and Ibi LGAs with 3.03% (2/66), and 1.5% (1/66) respectively. There was zero prevalence in Bali, Jalingo, and Wukari. The Prevalence in male 3.5% (6/172) was higher than that in female 0.44% (1/228). In cattle, Gashaka LGA recorded the highest prevalence of 25.7% (18/70) while the least prevalence of 3.0% (2/66) was in Ibi. There was zero prevalence in Jalingo and Wukari. The White Fulani cattle had the highest prevalence of 10.5% (35/332) while 3.2% (2/63) and 0% (0/5) were observed in Bokoloji and Muturu cattle respectively. Prevalence rates were higher in female 9.9% (28/284) and adult cattle 10.1% (35/347) than males 7.8% (9/116) and young 3.8% (2/53). About 21.62% of the sero-positive cattle were also parasitologically positive for trypanosomes of the brucei group, while none of the human samples was parasitologically positive for trypanosomes. This study showed serological evidence of T. b. gambiense infection in humans and cattle population of Taraba State. Key words: Detection, Trypanosoma brucei gambiense, Antibodies, Taraba State, Nigeria. Corresponding author: Department of Animal Health, Federal College of Animal Health and Production Technology, PMB 001, Vom, Plateau State, Nigeria. Received on: 03 Dec 2012 Revised on: 19 Dec 2012 Accepted on: 29 Dec 2012 Online Published on: 31 Dec J. Vet. Adv., 2012, 2(12):

3 DETECTION OF TRYPANOSOMA BRUCEI GAMBIENSE SPECIFIC LI TAT 1.3 ANTIBODIES IN Introduction Human African Trypanosomosis (HAT) is a debilitating and complex vector-borne parasitic zoonosis transmitted by tsetse flies. The disease has re-emerged in the 1990s to be a serious public health problem in the sub-saharan Africa including Nigeria (Airauhi et al., 2006). The disease causes high mortality of up to 100% in untreated cases (Odiit et al., 1997), and poses a major health risk to tourists visiting tropical Africa (Conway-Klaassen et al., 2002). The socio-economic impact of HAT ranks third after malaria and schistosomiasis in affected parts of sub-saharan Africa (Cattand et al., 2001). The disease affects economically active adults with about 25% of cases occurring in the age groups, and just over 60% in those aged from years (Swallow, 2000). The involvement of the central nervous system (CNS) in HAT is manifested by sleep disturbances making the economically active population inactive (Atouguia and Kennedy, 2000). Although man is the natural mammalian host for T. b. gambiense, studies on animals revealed the involvement of numerous wild animals such as nonhuman primates, reptiles, antelopes, and wild bovids in its transmission and sustenance (Mbaya et al., 2009). Domesticated animals such as pigs, goats, sheep and cattle (Welburn et al., 2001; Simo et al., 2006) have also been reported to serve as suitable reservoirs for the parasite and consequently their role in the transmission of the disease. In Nigeria, the disease was first reported in Gboko, Benue State (Aiyedun and Amodu, 1974). Thirty two years later in Abraka, Delta State (Airauhi et al., 2006, Osue et al., 2008), indicating the existence of the risk to the human population in different parts of Nigeria. There is paucity of information on HAT in Taraba State, Nigeria despite the availability of factors that can influence its occurrence, sustenance, and transmission in the State. These factors include: the presence of the Gashaka-Gumti and Yankari game reserves in the State and the neighbouring Bauchi State respectively, as well as the relationship of the State with the endemic areas of Benue State (Aiyedun and Amodu, 1974) and the Fontem Sleeeping 581 J. Vet. Adv., 2012, 2(12): Sickness focus of the Republic of Cameroon (Simo et al., 2006). This study was undertaken to provide information on the status of HAT in Taraba State which will be useful in the designing and institution of awareness campaigns as well as prevention and control programmes against the disease in the State. Materials and Methods Study area This study was carried out in Taraba State, located in the North-eastern Nigeria between longitude N and Latitude E and shares borders with the States of Gombe (North), Adamawa (North-east), Plateau (West), Bauchi (North-west), and Benue (South-west), and with the Republic of Cameroon (South). The State covers an area of 54,473 km 2 representing 5.9% of the total land area of Nigeria. It comprises of 16 LGAs and three Senatorial districts (Northern with 6 LGAs, Central and Southern Senatorial districts with 5 LGAs each). Sampling procedure Two LGAs selected at random using simple balloting were sampled from each Senatorial district. A total of 6 LGAs (Bali, Gashaka, Ibi, Jalingo, Karim Lamido, and Wukari) were sampled. Nomadic and Sedentary cattle herds were identified and herds were randomly selected within the LGAs. A stratified sampling method was employed based on breed, age (young < 1year; Adult >1yr), and sex. About 10% of cattle from each herd were randomly selected to represent each of the stratum (Kuzma and Bohnenblust, 2001). A total of 70 cattle were sampled from Gashaka LGA, while 66 cattle were sampled from the other five LGAs. A total of 66 volunteered humans were sampled from rural parts of the LGAs except for Gashaka where 70 individuals were sampled. Blood sample collection In humans, a total of 2 ml of whole blood was aseptically collected via the median cubital vein using 5 ml syringe and 21 G needle and transferred immediately into clean labeled sample bottles containing ethylene diamine tetra-acetic acid (EDTA) and gently shaken until the blood was properly mixed with the anticoagulant. The samples

4 KARSHIMA ET AL. were kept in cold ice block flask and used within three hours after collection. From well restrained cattle, a total of 3 mls of whole blood was aseptically collected via the jugular vein using 5 ml syringe and 18 G needles and transferred immediately into sample bottles as described previously. Sample Analysis The card agglutination test for T. b. gambiense Blood samples from humans and cattle were analyzed using the CATT for T. b. gambiense as described by Magnus et al. (1978). Data collated at the end of the study were subjected to statistical analysis. Prevalence rates were calculated by dividing the number of infected individuals by the total number of individuals examined and expressed as percentages. This was done for sex, age groups, breed, and LGAs. Chi square test (Kuzma and Bohnenblust, 2001) was used to test for differences in prevalence rates of the disease based on sex, age groups, breeds and LGAs. Values of p<0.05 were considered significant. Results and Discussion Prevalence of HAT in humans The prevalence of HAT in humans is presented in Tables 1 and 2. The overall prevalence in humans was found to be 1.8% (7/400). The highest 5.7% (4/70) was in Gashaka LGA (Table 1). This was followed by that observed in Karim Lamido 3.03% (2/66), and then 1.5% (1/66) in Ibi LGA (Table 1). There was zero prevalence in Bali, Jalingo, and Wukari for HAT (Table 1). The Prevalence in male 3.5% (6/172) was statistically higher (p<0.05) than that in female 0.44% (1/228) as shown in Table 2. None of the human samples was parasitologically positive for trypanosomes. Table 1: Prevalence of T. b. gambiense Li Tat 1.3 surface antibodies in humans in relation to sex and LGAs Variable No. of individuals examined No. positive (%) LGAs Bali 66 0 (0.00) Gashaka 70 4 (5.70) Ibi 66 1 (1.50) Jalingo 66 0 (0.00) Karim Lamido 66 2 (3.03) Wukari 66 0 (0.00) Total (1.80) Sex Male (3.50) Female (0.44) Total (1.80) Prevalence of HAT in cattle The overall prevalence of T. b. gambiense Li Tat 1.3 surface antibodies in cattle was found to be 9.25% (37/400) as shown in Table 3. Cattle examined in Gashaka LGA showed the highest prevalence of 25.7% (18/70) while the least prevalence 3.0% (2/66) was in Ibi (Table 3). There was zero prevalence in Jalingo and Wukari (Table 3). The White Fulani had the highest prevalence of 10.5% (35/332) while 3.2% (2/63) was observed in Bokoloji. This was statistically insignificant (p>0.05). Of the 5 Muturu cattle examined, none was positive (Table 6). Prevalence rates were higher in female 9.9% (28/284) and adult cattle 10.1% 582 J. Vet. Adv., 2012, 2(12):

5 DETECTION OF TRYPANOSOMA BRUCEI GAMBIENSE SPECIFIC LI TAT 1.3 ANTIBODIES IN (35/347) than males 7.8% (9/116) and young 3.8% (2/53) as shown in Tables 4 and 5 respectively. These were statistically insignificant (p>0.05). About 21.62% of the sero-positive cattle were also parasitologically positive for trypanosomes of the brucei group. Table 2: Prevalence of T. b. gambiense Li Tat 1.3 surface antibodies in cattle in six LGAs of Taraba State LGAs No. of cattle examined No. positive (%) Bali Gashaka Ibi Jalingo Karim Lamido Wukari Total Table 3: Prevalence of T. b. gambiense Li Tat 1.3 surface antibodies in cattle in relation to sex, age group, and breed Variable No. of cattle examined No. positive (%) Sex Male (7.80) Female (9.90) Total (9.25) Age group Young ( 1 year) 53 2 (3.80) Adult (> 1 year) (10.10) Total (9.25) Cattle breed White Fulani (10.50) Bokoloji 63 2 (3.20) Muturu 5 0 (0.00) Total (9.25) The results of this study have shown the serological evidence of HAT in the study area. The existence of HAT in the study area may be attributed to the close proximity of the State with the established endemic HAT areas of Benue State, Nigeria (Aiyedun and Amodu, 1974) and the Fontem Sleeping Sickness focus of the Republic of Cameroon (Simo et al., 2006). Other reasons may be the availability of numerous wildlife species present in the Gashaka-Gumti game reserve in the State and Yankari game reserve in the neighbouring Bauchi State, Nigeria. Moreso, lack of sustained vector control measures, the high cost and inability of the available animal trypanocides to adequately be used as curatives for T. b. gambiense infection, and the increasing incidence of parasites resistance to the available trypanocides (Omotainse et al., 2004) might have contributed to the existence of HAT in the State. The overall prevalence observed in humans is lower than that observed by Airauhi et al. (2006) and Osue et al. (2008) from Abraka, Delta State and that reported by Welburn et al. (2001) in cattle from Seroti, Uganda. This may probably be due to the higher sensitivity of the PCR techniques used by these researchers as compared to the CATT used in this study. The higher prevalence rate in men as compared to women may be due to the selective activities of men such as farming, hunting, fishing, and bathing in rivers/streams which put them at higher risk of exposure to infection through contact with the tsetse vector (Pepin et al., 2002). Lack of invasion of the tsetse habitat by women in search of water in the 583 J. Vet. Adv., 2012, 2(12):

6 rainy season which is a common practice during the dry season may also explain the lower prevalence in women. The higher prevalence rate observed in female as compared to male cattle may be attributed to stress associated with pregnancy and lactation which could decrease resistance in cows and render them more susceptible to the infection. This agrees with the finding of Shah et al. (2004) who reported a higher prevalence of trypanosomosis in females as compared to male camels from the Republic of Cameroon. Another reason for the higher prevalence rate in females may be because they are kept in herds for longer periods than the males which increase their exposure to tsetse bites and the infection. Based on age groups, the prevalence of Li Tat 1.3 surface antibodies was higher in adult cattle than in calves. This may be attributed to the protective effect of maternal immunity which are not detectable using the CATT (Bhutto et al., 2002), and may partly be due to low levels of challenge arising from low attractiveness of the calves to tsetse flies. The release of higher concentrations of insect attractants such as phenols in the urine (Kremar et al., 2006) as well as acetone and octenol in the breath (Torr et al., 2006; Kremar et al., 2007) of adult cattle as compared to young ones may also explain why the prevalence of HAT was higher in adult than young cattle. The identification of trypanosomes of the brucei group in T. b. gambiense sero-positive cattle is a source of concern. Though these parasites were not characterized, their presence in T. b. gambiense sero-positive cattle suggests that they might probably be of human origin. References Airauhi LU, Idogun ES, Omuemu VO, Airauhi ES (2006). Confirmation of Trypanosoma parasitaemia in previously serologically positive individuals in the Abraka area of Delta State, Nigeria. J Med. Biomed. Res., 5(2): Aiyedun BA, Amodu AA (1974). Human sleeping sickness in the Gboko endemic areas in Nigeria. Acta Trop., 33(1): Atouguia JLM, Kennedy PGE (2000). Neurological aspects of human African trypanosomiasis. In: Davis, L. E. and Kennedy, P. G. E. (eds). Infectious Diseases of the Nervous System. Butterworth-Heinemann, Oxford, UK, KARSHIMA ET AL. pp Bhutto B, Gadahi JA, Shah G, Dewan P, Arijo AG (2002). Field investigation on the prevalence of trypanosomosis in camels in relation to sex, age, breed, and herd size. Pakistan Vet. J., 30(3): Cattand P, Jannin J, Lucas P (2001). Sleeping sickness surveillance: an essential step towards elimination. Tropical Medicine and International Health, 6: Conway-Klaassen JM, Wyrick-Glatzel JM, Neyrinck N, Belair PA (2002). Sleeping sickness in young American tourist. Lab. Med., 33: Kremar S, Mikuska A, Merdic C (2006). Response of Tabanidae (Diptera) to different natural attractants. J Vect. Ecol., 31: Kremar S (2007). Responses of Tabanidae (Diptera) to canopy traps baited with 4-methylphenol, 3-isopropylphenol, and naphthalene. Journal of Vector Ecology, 32: Kuzma JW, Bohnenblust SE (2001). Basic Statistics for the Health Sciences, fourth edition, published by McGraw- Hill, pp Magnus E, Vervoot T, Van-Meirvenne N (1978). A cardagglutination test with stained trypanosomes (CATT) for the serological diagnosis of T. b. gambiense trypanosomiasis. Ann. Soc. Belg. Med. Trop., 58: Mbaya AW, Aliyu MM, Nwosu CO, Ibrahim U (2009). Effect of D, L-α-difluoromethylornithine on biochemical changes in Baboons (Papio anubis) experimentally infected with Trypanosoma brucei gambiense. NVJ., 31(1): Odiit M, Kansiime F, Enyaru JC (1997). Duration of symptoms and case fatality of sleeping sickness caused by Trypanosoma brucei rhodesiense in Tororo, Uganda. East Afri. Med. J., 74: Omotainse SO, Kalejaiye JO, Dede P, Dadah AJ (2004). The current status of tsetse and animal trypanosomosis in Nigeria. Vom J Vet. Sci., 1(1): 1-7. Osue HO, Lawani FAG, Saddiq L, Aderemi A, Diara A, Lejon V, Simmaro P (2008). Active transmission of Trypanosoma brucei gambiense sleeping sickness in Abraka, Delta State, Nigeria. Sci. World J., 3(2): Pepin J, Mpia B, Iloasebe M (2002). Trypanosoma brucei gambiense African trypanosomosis: differences between men and women in the severity of disease and response to treatment. Trans. Royal Soc. Trop. Med. Hyg., 96: Shah SR, Phulan MS, Memon MA, Rind R, Bhatti A (2004). Trypanosomes infection in camels. Pakistan Vet. J., 24(4): Simo G, Asonganyi T, Nkinnin SW, Njiokou F, Herder S (2006). High prevalence of Trypanosoma brucei gambiense group 1 in pigs from the Fontem sleeping sickness focus in Cameroon. Vet. Parasitol., 139(3): Swallow BM (2000). Impacts of Trypanosomosis on African Agriculture. PAAT Technical and Scientific Series 2, 584 J. Vet. Adv., 2012, 2(12):

7 DETECTION OF TRYPANOSOMA BRUCEI GAMBIENSE SPECIFIC LI TAT 1.3 ANTIBODIES IN Food and Agriculture Organization (FAO), Rome, pp. 52. Torr SJ, Mangwiro TNC, Hall DR (2006). The effects of host physiology on the attraction of tsetse (Diptera: Glossinidae) and Stomoxys (Diptera: Muscidae) to cattle. Bull. Entomol. Res., 96: Welburn SC, Picozzi K, Fevre EM, Coleman PG, Odiit M, Carrington M, Maudlin I (2001). Identification of human infective trypanosomes in animal reservoir of Sleeping Sickness In Uganda by means of serum resistance-associated (SRA) gene. Lancet, 358: J. Vet. Adv., 2012, 2(12):

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