EFFECTS OF EXPERIMENTAL TRYPANOSOMA EVANSI AND TRYPANOSOMA BRUCEI BRUCEIINFECTIONS ON HAEMATOLOGICAL AND SOME REPRODUCTIVE PARAMETERS OF YANKASA RAMS

ABSTRACT
The effects of experimental T. evansi and T. bruceibruceiinfections on haematology and some reproductive parameters of Yankasa rams were investigated. Sixteen Yankasa rams aged, 24 to 30 months and weighing 22-25kg were acclimatized for a period of two months in a clean fly proof house, adequately fed and given water ad libitum. Of the sixteen rams, twelve that were clinically fit for the experiments at the end of the eight weeks acclimatization period were randomly divided into four groups (I, II, III and IV), of three rams each. Groups I and II were each challenged singly with experimental T. bruceibrucei(Federe strain) andT. evansi (Sokoto strain), respectively, while group III was challenged with mixed T. bruceibruceiand T. evansiparasites (50% of each species in the infective inoculum) and group IV was left as uninfected control. Each infected ram received 2ml containing 2x106 trypomastigotes via the jugular vein. Parasitaemia in groups I and III appeared 5-9days and 6-11 days post infection, respectively, while it appeared 19-21 days post infection (P.I) in group II. There was significant difference (P < 0.01) in the mean parasitaemia levels of groups I and III in comparison to that of group II at the end of the experiment. The pre-infection mean weekly packed cell volume (PCV)of the rams in the experimental groups I, II, III and IV were 33.0 ± 1.2%, 31.0 ± 1.6%, 31.67 ± 1.1% and 32.67 ± 1.5%, respectively.The mean PCV by the end of the experiment in groups I, II, III and IV were18.70 ± 1.4%, 24.75 ± 1.6%, 17.48 ± 1.8%, and 35.01 ± 1.5%respectively. There was a significant difference (P < 0.01) in the mean PCV and haemoglobinconcentrations among the groups at the end of the experiment. The clinical signs observed in the infected groups included intermittent pyrexia, pale ocular mucous membranes indicative of anaemia, dullness, lethargy, roughy hair coat, scrotal oedema, scrotal degeneration, loss of libido, increase in semen collection reaction time, emaciation, and death. There was a drastic and progressive deterioration in semen quality in all infected rams manifested by a decrease in volume or cessation of semen production, a sharp decrease in progressively motile sperm, elevated numbers of dead sperm and significant morphological abnormalities of sperm in most animals. The rams especially in groups I and III were all deemed unfit for breeding by the end of the 98 days post infection. Uninfected rams were healthy and had good semen characteristics throughout the experimental period. There was significant difference (P < 0.01) in the gonadal and epipidymal sperm reserves of groups I and III in comparison to group II, and between infected and control rams.The gross lesions observed in the infected rams in group II were moderate and very severe in groups I and III. These lesions included pale carcasses indicative of anaemia, watery blood, lymphadenopathy, splenomegaly and hepatomegaly.No observable gross lesion was found in the organs from rams of the control groupIV. The microscopic lesions observed in the testes of the infected rams were characterized by degeneration of the seminiferous tubules, mononuclear infiltration of interstitial tissues, infiltrations by lymphocytes with minor cellular damages.The results indicate that trypanosomosis due to experimentalT.b. brucei, T.evansi and mixed infections (of both parasites), may cause marked defects in the haematological parameters, severe degenerative changes in the reproductive organs resulting in the rapid deterioration of semen characteristics and associated infertilityproblems. Therefore, pathogenic trypanosomes may be important cause of various grades of infertility problems in Yankasa rams in tsetse and pathogenic trypanosomes-endemic areas of Nigeria.


CHAPTER ONE
1.1       INTRODUCTION
Livestock production plays important roles in the provision of high-quality protein to consumers and regular income to producers. To fulfill their potential sustainably, they must be managed with care. From time immemorial livestock rearing is given much importance not only in developing countries but also in developed countries (Mohammed, 2007).Currently, livestock is one of the fastest growing agricultural subsectors in developing countries where it contributes about 33 per cent of the Gross Domestic Product (GDP). This growth is driven by the rapidly increasing demand for livestock products; which is equally being driven by population growth, urbanization and increasing incomes in developing countries (Delgado, 2005). Livestock therefore plays a major role in the socio-economic development of any nation. Between 70 – 80% of the Nigeria‘s population of over 140 million are engaged in agriculture and livestock industry as their major occupation(Mohammed, 2007).

As an integral component of agricultural economy of any nation, livestock performs multifarious functions such as provisions of food, nutrition, income, savings, foreign currency earning (by exporting hides and skin, bone and other products), draught power, manure, fuel, transport, social and cultural functions (Bangladesh Agricultural Research Council, 2010). At the household level, livestock plays a critical economic and social role in the lives of pastoralists, agro-pastoralists and smallholder farmers. Livestock fulfills an important function in coping with shocks, accumulating wealth and serving as a store of value in the absence of formal financial institutions and other missing markets (Asfawet
al., 2011). In the case of smallholder mixed farming systems, livestock provides nutritious food, additional emergency and cash income, transportation, farm outputs and inputs and fuels for cooking food. In the case of pastoralists, livestock represents a sole means to support and sustain their livelihoods. Furthermore, available research suggests that with economic growth, consumption patterns tend to change towards high value and high-protein foods, such as those derived from livestock (Delgado et al., 1999).

Sheep and goats constitute the world‘s largest population of livestock with an estimate of 1,078.9 and 861.9 million, respectively. This implies that there is about one goat to approximately 1.25 sheep in the world, but tremendous variations occur among the different parts of the world regarding the number of goats, its ratio to sheep and their percentages (FAOSTAT, 2008). The largest numbers of goats are in Asia, followed by Africa, representing about 59.7% and 33.8% respectively, summing up to 93.5% of the world‘s total. The lowest numbers of goats are in Oceania, accounting for 0.1% of the world‘s total number. The ratio of goat to sheep ranged between one goat to 0.8 sheep in the Caribbean to one goat to 119.2 sheep in Oceania (FAOSTAT, 2008). The total number of goats in the world has increased by 146% of the total number (590.1 million) encountered in 1990. During the same period, cattle number increased by 5%, while that of sheep decreased by 10%, reflecting a fall in the productivity of sheep as a major livestock species.Africa alone contributed a total of 287.6 million sheep and 291.1 million goats, representing approximately 26.7% and 33.8% respectively, of the world‘s total(FAOSTAT, 2008). Within Africa, the distribution of these small ruminants varies widely, with a higher concentration found in dry areas than humid areas (Ademosun,
1988). In West Africa, Nigeria has the largest number of livestock population.In the world, the country is ranked sixth in terms of sheep and goat production with a total production level of 33.9 million sheep and 53.8 million goats (FAOSTAT, 2008). Keeping small ruminants is regarded as an investment as these animals are sold to meet compelling family and financial obligations or slaughtered for consumption. Little capital investment in buildings or other material is required for their upkeep, and space and maintenance requirements are low, with high reproductive efficiency (Ademosun, 1988). This implies that, given the economic growth in Nigeria, the market demand for livestock and livestock products is likely to continue growing in the future (Ademosun, 1988). Paradoxically, the livestock sub-sector tends to be playing a decreasing role in national development in view of its contribution to the country‘s agricultural Gross Domestic Product (Ifeanyi and Olayode, 2008). Livestock as a percentage of agricultural GDP was as high as 19% in 1983 and 1984, but the share has dropped persistently over time to 10% in 1998 and further to 6% in 2004 and 2005 (Ifeanyi and Olayode, 2008).

One of the most important and debilitating constraints to livestock production is livestock diseases (Firew, 1999; Soudre et al., 2013). Diseases are the most significant limiting factors to livestock productivity in sub-Saharan African countries. Diseases such as helminthosis, ectoparasitism, and haemoparasitism as well as bacterial and viral infections constitute impediments to livestock production(Agwuma, 1983).Due to the devastating effect of livestock diseases, animal protein output has not been able to keep up with national demands (Njombe and Msanga, 2009).Prominent among livestock diseases istrypanosomosis, which isone of the most deadly and pathogenic despite the
age-long attempts to control it. Griffin (1978), reported that sheep and goats gave quicker returns and lower per head value than cattle. However, a disease such as animal trypanosomosis poses a great risk to their production. The economic impact of the disease on these animals has been shown to be substantial. It is described as a complex debilitating and often fatal conditions caused by infection with one or more of the pathogenic tsetse-transmitted protozoan hemoflagellate parasites of the genus Trypanosoma (Anene et al., 2001). The incidence and severity of the disease in different regions are dependent upon local conditions (Anene et al., 2001). The impact of trypanosomes on African agriculture is most obviously felt at the herd level leading to reduced milk output, reduced live animal output and reduced efficiency of animals used for cultivation (Swallow, 2000). In susceptible cattle breeds, the disease reduces calving by up to 20% thereby causing death of young stock; meat and milk outputsare reduced by at least 50% (Swallow, 2000). The disease has been a great challenge to the livestock industry where the barrier imposed has been difficult to surmount by any form of chemotherapy, prophylaxis or control (Holmes et al., 2004; Van den Bossche and Doran, 2004).


The major pathogenic trypanosome species in livestock are transmitted by the tsetse fly (genus Glossina) and include:Trypanosoma congolense, T.vivax, T.brucei brucei and T.evansi, while the sub species of T.brucei, T.b.rhodesiense and T.b.gambiense cause sleeping sickness in man and were important causes of death in Africa (Losos, 1986; Okubanjo et al., 2014). Nagana and related diseases also caused by T. congolense, T.vivax and T.brucei brucei in cattle are prevalent in much of sub-Saharan
Africa,especially Nigeria. Surra, another disease caused by T. evansi, isa problem wherever camels are or have been. Chagas disease caused by T.cruzi (transmitted mechanically) is a serious public health problem in South and Central America, where about 10 million people are infected(Losos, 1986; Okubanjo et al., 2014). The pathogenicity of trypanosome infection varies considerably and depends on both the species of trypanosome and the host involved. Trypanosomes are either haematic such as T. congolense and T. vivax which are found in the plasma or tissue-invasive such as T.b. brucei, T.b. rhodesiense orT.b. gambiense,T. evansi and T. equipadum which are found intravascularly or extravascularly(Murray et al., 1982; Awobode, 2006). The severity of the infection is influenced by a number of factors such as virulence of the different species of trypanosomes, age, nutritional status, and the breed of livestock (Murray et al., 1982; Awobode, 2006).


Clinically, the effects of trypanosomosis on these animals range from anaemia, immunosuppression, depression with inability to rise, pyrexia directly associated with parasitaemia, paleness of mucous membrane, rapid pulse beat, retarded growth, roughness of haircoats,enlargement of peripheral lymph nodes, low milk production, low meat quality, and weight loss as well as infertility, abortion, stillbirth and depressed reproductive performance and reduced capacity to work leading to morbidity and mortality in the absence of treatment (Sekoni, 1994;Snow et al., 1996; Bezerraet al., 2008; Batista et al., 2007; 2009; 2012; Silva et al., 2013).Trypanosomosis can be a highly debilitating and fatal disease in domestic ruminants, mainly due to the haematological disturbances that induce severe anaemia and inflammatory foci in the central nervous
system (CNS), heart, liver, spleen and lymph nodes (Gardiner et al., 1989; Desquesnes, 2004; Chamond et al., 2010). Further haematological effects include decreased packed cell volume, reduced red blood corpuscles, reduced haemaglobin concentration, decrease in total protein and leucocytes counts (Sekoni et al., 1990a; Audu et al., 1999; Chamond et al., 2010).Histologically, the effects of trypanosomosis on reproductive tissues and organs include testicular lesions and severe degeneration, necrosis and focal calcification of the seminiferous tubules in rams and goats (Edeghere et al., 1985; Rodrigues et al., 2013). Adamu et al. (2007) reported depletion of spermatogonic cells and destruction of interstitial tissues in Zebu bulls experimentally infected with T. vivax. Sporadic cases of congenital transmission of trypanosomes have also been reported in humans, sheep and goats (Ikede and Losos, 1972), calves (Batista et al., 2012) and mice (Ijagbone and Agbede, 2000). Additionally, T. vivax infection has induced abnormal pregnancy, dystocia, abortion, premature and low birth weights, stillbirths, transplacental foetal infection, neonatal death and other pathogenic effects on foetuses and offsprings (Sekoni, 1994; Batista et al., 2012). Other pathological effects include splenomegaly, hepatomegaly, genital lesions, congestion of the lungs, inflammatory lesions of the heart and paleness of carcasses (Dargantes et al., 2005b).

Direct losses due to trypanosomosis are estimated to amount to between US$ 1-1.2 billion each year, while the indirect impact of African animal trypanosomosison agriculture in sub-Saharan Africa exceeds this amount. A pondered evaluation extrapolated for the total tsetse-infested lands values the total losses, in terms of agricultural Gross Domestic Product, at US$ 4.75 billion per year (FAO, 2004). In
Nigeria, these damaging effects and the manpower and material resources committed to the disease result in financial loss of more than $23.8 million annually (Mulligan et al., 1970).


1.2       Statement of the Research Problem

In Nigeria, demand for ramsduring festivity is on the increase but parasites especially trypanosomes, have become a major threat to sustainable livestock production resulting in a decline in production (Soudre et al., 2013). Apart from haematological and pathogenic aberrations that do occur in animals infected with the parasites, recent studies show that they cause awide range of reproductive disorders in animals, including degeneration of the hypothalamus, pituitary glands and gonads with consequent disruptions in the secretions and plasma concentrations of the hormones necessary for normal reproductive processes in both sexes (Sekoni,1994). In female animals, the effects include severe genital lesions, temporary or permanent anoestrus, and abnormal oestrous cycles. Additionally, trypanosomal-induced death during pregnancy, abnormal pregnancy, dystocia, abortion, premature birth, low birth weight, stillbirth, transplacental foetal infection, neonatal death and other pathogenic effects on foetuses and offsprings have been reported (Sekoni, 1994; Silva et al., 2013).


In the males, the effects include delayed puberty, loss of libido, severe degenerative changes of the genitalia, manifested by the production of very poor quality semen and loss of epididymal and gonadal sperm reserves (Sekoni, 1994; Mbaya et al., 2011; Okubanjo et al., 2014). Testicular atrophy has also been reported with the presence of
dead spermatozoa in the seminiferous tubules of bulls, gazelles and rams (Sekoni, 1994; Sekoni et al., 2004; Bezerra et al., 2008; Mbaya et al., 2011). Infection of rabbits with T. brucei brucei causes scrotal oedema, scrotal inflammation, severe testicular degeneration, abnormal spermatogenesis and incomplete resolution of the genital organs following berenil chemotherapy (Ikede and Akpavie, 1982). Omeke and Igboeli (2000) reported the presence of Trypanosoma brucei brucei in the genital tract, soft organs and brain of infected boars with resultant degeneration of testes. There was also loss of libido in infected boars. It has also been reported that animals that survived infection often remained infertile (Sekoni et al, 2004).Information on the effect of T. brucei brucei, T. evansi and mixed infections on the haematology and reproductive physiology of Yankasarams is scanty and basically unavailable.Sheep are often grazed alongside cattle or camels from Northern Nigeria towards the Southern vegetation belts by cattle herdsmen in search of greener pastures thereby exposing them to the risk of trypanosomes.


1.3       Justification

Although T. brucei brucei and T.evansi are primarily parasites of cattle and camels respectively, there is the likelihood that animals herded together with cattle or camels, especially Yankasa rams, may become infected with these parasites. Consequently, there is an urgent need to investigate factors that may negatively affect the success of sheep breeding especially in line with reproductive problems such as lowered fertility, infertility and or sterility. Therefore, a thorough understanding of the pathogenic trypanosomes which could alter normal reproductive physiology of animals with associated
haematological changes (Biryomumaisho et al., 2003), is a pre-requisite for this study in Yankasa rams.This will provide vital information on the progression and degree of degenerative changes that occur in the host‘s tissues as well as the severity of the infection. Hence the need for this study on the effect of T.brucei brucei and T. evansi on the haematological and reproductive parameters of Yankasa rams.The study will provide information on the effects of T. brucei brucei, T. evansi and mixed infections on the haematological indices and reproductive parameters (semen quality and gonadal and epididymal sperm reserves) of Yankasarams in Nigeria. Yankasa rams were selected for this study considering the fact that Yankasa sheep are the most numerous breed of sheep in the Guinea Savanna region. They are also inhigh demand amongst the Muslim populace of Nigeria due to their ceremonial values (naming ceremony), religious importance (used as sacrificial animals during the Eid-El kabir festive periods), social and economic values (e.g. mutton, barbecue, suya and pepper soup).


1.4       Aim and Objectives of the Research

The aim of the research was to evaluate the effects of single and mixed experimental Trypanosoma evansi and Trypanosoma brucei brucei infectionson thehaematological and some reproductive parameters of Yankasa rams.

The specific objectives of the research were to determine the effects of single and mixed experimental T. evansi andT. brucei brucei infections ofYankasa rams on:

i. Haematological indices.

ii. Semen characteristics.

iii. Epididymal and gonadal sperm/spermatid reserves.

iv. Anatomy of reproductive organs and tissues.


Single and mixed experimental infections of T. evansi and T.b. brucei ofYankasa rams have no significant effects on:


i. Haematological indices.

ii. Semen characteristics.

iii. Epididymal and gonadal sperm/spermatid reserves.

iv.Anatomy of reproductive organs and tissues.

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