Trypanosomosis in small ruminants maintained bylow riverine tsetse population in central Nigeria

A.U. Kalua,*, S.I. Oboegbulemb, M. Uzoukwub

aDepartment of Veterinary Public Health and Preventive Medicine, University of Maiduguri, P.M.B. 1069, Maiduguri, Borno State, NigeriabDepartment of Veterinary Pathology, Microbiology and Epidemiology, University of Nigeria, Nsukka, Enugu State, Nigeria

Accepted 23 September 2000

Abstract

The prevalence of trypanosomosis was investigated over a 12-month period, among small ruminants grazing in known

sleeping sickness endemic area of central Nigeria and under light riverine tsetse challenge. Analysis of the data from 304

Yankassa sheep and 239 West African Dwarf � Red Sokoto goats indicated high mean prevalence (27.62%, con®dence limits

Cl: 0.232, 0.312). Interspecies difference between sheep (38.16%; 0.382, Cl: 0.332, 0.432) and goats (14.23%; 0.142, Cl:

0.102, 0.182) was highly signi®cant (P < 0:001). Infections were also signi®cantly higher (P < 0:05) with agro-pastoral

(extensive) management, during the dry season and in adults compared to intensively managed animals, the wet season and

young animals, respectively. Trypanosoma vivax was the predominant parasite encountered and accounted for over 49% of the

infections. T. congolense and mixed populations were diagnosed at approximately 15% each while T. brucei were absent in

caprines. The implications of these ®ndings in the epidemiology of the diseases in both man and domestic animals is

discussed. # 2001 Elsevier Science B.V. All rights reserved.

Keywords: Trypanosomosis; Yankassa sheep; Trypanosoma vivax; Glossina tachinoides

1. Introduction

In Nigeria, small ruminants are the most populous

and equitably distributed livestock (Ikede, 1987).

Current ®gures are 25.5 million goats and 14.5 million

sheep (FAO/OIE/WHO, 1995) and these contribute

26.5% of the total Tropical Livestock Units (TLU)

(Ikede, 1987). These animals may not show overt

clinical signs of trypanosomosis under ®eld conditions

as cattle do (Stephen, 1970; Nawathe et al., 1995) and

this indicates a degree of trypanotolerance and lower

rates of exposure due to tsetse feeding habits. Stephen

(1970) was of the opinion that tsetse seldom feed on

sheep and goats and advanced the reason that these

vectors may ®nd their blood unpalatable or experience

dif®culties in penetrating the hosts' dense coats of

wool or hair. Little importance is therefore attached to

trypanosomosis in small ruminants compared to cattle

(Krammer, 1966; Stephen, 1970; Grif®n, 1978). Most

available information on the disease in these stock are

sourced from abattoir data (Joshua and Ige, 1983;

Kalejaiye et al., 1995; Nawathe et al., 1995; Dadah

et al., 1997).

On the other hand, it has been suggested that great

economic losses occur in small ruminants due to

trypanosome infections (Grif®n, 1978; Grif®n and

Allonby, 1979; Kalu and Edeghere, 1985). Also, these

animals have been incriminated as sources/reservoirs

of infection to other animals and man (Mahmaud and

Elmalik, 1977; Scott et al., 1983). Recent records of

Small Ruminant Research 40 (2001) 109±115

* Corresponding author.

0921-4488/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved.

PII: S 0 9 2 1 - 4 4 8 8 ( 0 0 ) 0 0 2 1 5 - 7

the incidence of trypanosomes even among trypano-

tolerant breeds of cattle and the isolation, from try-

panosusceptible ones (with which sheep and goats

graze together under pastoral management practice)

of potentially human-infective Trypanosoma brucei

subspecies in sleeping sickness endemic foci of cen-

tral Nigeria (Kalu, 1995a, b), dictate studies into other

domestic ruminants. We therefore investigated the

prevalence of trypanosomosis in sheep and goats in

the area as a contribution to the epidemiology of the

disease.

2. Materials and methods

2.1. The study area

The Lower Benue area or old Tiv Province of

central Nigeria is part of the primordial foci of sleep-

ing sickness described by Duggan (1970). The studies

were conducted in the three most important local

government areas (LGAs) in terms of sleeping sick-

ness in Nigeria. The Nigerian Institute for Trypano-

somiasis Research (NITR) and other workers have

consistently found the highest annual prevalence of

the disease among Nigerians in these LGAs since

1983 (NITR, 1983; Kalu, 1996). They are within

the derived savanna vegetational zone between

78150±188140 and 88000±98580 East (Fig. 1). Two dis-

tinct seasons exist per year: rainy season is between

April and September while the dry season prevails

from October to March. Most of the area lies between

50 and 100 m above sea level. Katsina-Ala LGA,

located on the east of the foci is bissected by River

Katsina-Ala which drains into River Benue to the

north-west and is contiguous with the Donga Valley

to the east (Kalu, 1996). The main features of Gboko

LGA are River Mu, a tributary of River Benue to the

north, and three forest reserves at Gboko (98150N,

98000E), Akpagher (78180N, 88470E) and Wannune

(78350N, 88500E). Gwer LGA in the west is trasvered

by rivers Ogori and Gwer which originate from the

Fig. 1. Map of the local government areas of central Nigeria surveyed. Insert shows the central position of the survey sites.

110 A.U. Kalu et al. / Small Ruminant Research 40 (2001) 109±115

south-west and north, respectively. Also along the

banks of these two rivers are found patches of forest

in one of which is the Livestock Investigation and

Breeding Centre (LIBC) described by Godfrey et al.

(1964). Previous reports from the same (Lower Benue

primordial sleeping sickness) area (Fig. 1) document

low levels of riverine tsetse (Godfrey et al., 1964;

Aiyedun and Amodu, 1976) while Kalu et al. (1991)

recorded only G. tachinoides at an apparent density of

0.024 ¯y/trap/day.

2.2. The small ruminants and management practices

Ovine herds were nomadic Yankassa breed which

graze with zebu cattle and owned by agro-pastoralists.

They graze daily for distances of 15 km from owner's

hamlets but usually return at night to be housed in

wire-fenced enclosures (extensive management).

Goats were peri-domestic West African Dwarf

(WAD) cross Red Sokoto (RS) normally tethered at

home during the rainy (cropping) season and fed cut

grass/legume mixture but allowed to browse crop

residues within family premises/lands during the

dry season (semi-intensive). The animals sampled

were aged between 6 months and 5 years.

2.3. Sampling technique and sources of blood

Within each LGA, the districts to be sampled were

selected by simple random technique and in propor-

tion to the total number of districts indicated in the

most current 1:25,000 map of Federal Surveys Depart-

ment. Three to four extensively-reared ovine herds

were chosen by the same randomization from among

herd-owners who had been resident in the area for at

least 5 years. Within the herds, the number of animals

sampled were selected according to population (herd-

size) distribution of age and sex and guided by the

upper limits required to give 95% level of con®dence

assuming a prevalence of 5% (ILCA, 1987). The peri-

domestic (semi-intensively managed) goats sampled

were from the same districts as the sheep but the

sample units were compounds (collection of hamlets)

as the animals were from small-holder farmers.

Two to three millilitres of blood was collected, by

jugular venipuncture, per animal into bijou bottle

containing EDTA (ethylenediamine tetra-acetic acid)

as anticoagulant (Schalm et al., 1975).

2.4. Diagnostic technique and parasite identi®cation

Both the standard trypanosome detection methods

(STDM) and the concentration techniques were used.

Among STDM, wet, thin and thick ®lms were carried

out as described by Kalu et al. (1986). Two concen-

tration methods Ð the microhaematocrit technique

and the buffy coat examination as previously

described by Paris et al. (1982) and Kalu et al.

(1986) were employed. Con®rmation of the species

of trypanosomes in positive samples was by morpho-

logical differentiation on Giemsa-stained thin ®lms

and biological transmission characteristics in labora-

tory-bred mice (Hoare, 1972). Packed cell volume

(PCV) was estimated using haematocrit centrifuge

and reader (Schalm et al., 1975).

2.5. Statistical analysis

Differences in infection rates and due to the various

parameters studied (species, gender, age, season)

were analysed using Chi square (X2) method. PCV

values were compared using Student's t-test (ILCA,

1987).

3. Results

3.1. General and interspecies prevalence

Five hundred and forty-three samples were col-

lected from sheep (304) and goats (239) over a 12-

month study period. The data indicated a mean pre-

valence of 27.62% (0.276; con®dence limits, Cl:

0.236, 0.316). The differences in interspecies infection

rates of 38.16% (0.382; Cl: 0.322, 0.432) and 14.23%

(0.142; Cl: 0.102, 0.182) for the sheep and goats,

respectively was highly signi®cant (X2 � 38:33,

df � 1, P < 0:001; Table 1).

3.2. Effects of variables/attributes on prevalence

The effects of variables/attributes on prevalence of

trypanosome infections are in Tables 2 and 3 for sheep

and goats, respectively. Among ruminant herds

sampled, infections were higher (usually over 40%)

in the dry season than in the rainy season (9±29%); the

differences were signi®cant in both sheep (X2 � 6:39,

A.U. Kalu et al. / Small Ruminant Research 40 (2001) 109±115 111

Table 1

Prevalence of trypanosome infection among small ruminantsa in the Lower Benue sleeping sickness endemic area of central Nigeria

Parameter Sample size Positive cases Trypanosome speciesb

No. % CI T. vivax T. congolense T. brucei Mixedc Unidentifiedd

Ruminant species: X2 � 38.331, df � 1, P < 0.001

Sheep 304 116 38.16 �0.05 59 (50.9) 16 (13.7) 11 (9.5) 14 (12.0) 16 (13.8)

Goat 239 34 14.23 �0.04 15 (44.1) 7 (20.6) 0 (0.0) 8 (23.5) 4 (11.8)

Total 543 150 27.6 �0.04 74 (49.3) 23 (15.3) 11 (7.3) 22 (14.7) 20 (13.4)

a Sheep under extensive management and WAD � RS goats raised semi-intensively.b Bracketed values indicate contributions (%) of trypanosome species.c Mixed: mixed Trypanosome populations.d Unidenti®ed: parasite diagnosed only by concentration methods (HCT, BCM) and not positive on stained thin and thick ®lms.

Table 2

Effect of various factors on the prevalence of trypanosomosis among semi-nomadic (extensively-reared) Yankassa sheep in central Nigeria

Parameter Sample size Positive cases Trypanosome speciesa

No. % CI T. vivax T. congolense T. brucei Mixed Unidentifiedb

Season of year: X2 � 6.3913, df � 1, P < 0.05

Dry 177 78 44.63 �0.07 41 (53)a 8 (10) 8 (10) 11 (14) 10 (13)

Wet 127 38 29.63 �0.08 18 (47) 8 (21) 4 (11) 3 (8) 5 (13)

Gender: X2 � 0.1952, df � 1, P > 0.05

Male 70 29 41.43 �0.11 6 (21) 6 (21) 2 (7) 2 (7) 12 (43)

Female 234 87 37.18 �0.06 53 (61) 10 (12) 9 (10) 12 (14) 3 (3)

Age: X2 � 19.3296, df � 1, P < 0.01

Youngc 58 7 12.07 �0.08 3 (43) 1 (14) 0 (0) 2 (29) 1 (14)

Adult 246 109 44.31 �0.06 56 (51) 15 (14) 11 (10) 12 (11) 14 (13)

a Numbers in bracket indicate percentage (approximate) of Trypanosome species.b Unidenti®ed (as in Table 1).c Young: 1 year or less: no permanent teeth.

Table 3

Effect of season of the year, gender and age on trypanosome infections among peri-domestic (semi-intensively-reared) WAD � RS goats in

central Nigeria

Parameter Sample size Positive cases Trypanosome speciesa

No. % CI T. vivax T. congolense T. brucei Mixed Unidentifiedb

Season of year: X2 � 6.0933, df � 1, P < 0.05

Dry 98 21 21.43 �0.08 9 (43) 4 (19) 0 (0) 4 (19) 4 (19)

Wet 141 13 9.21 �0.05 6 (46) 3 (23) 0 (0) 3 (31) 0 (0)

Gender: X2 � 22.3467, df � 1, P < 0.01

Male 82 16 19.51 �0.08 6 (38) 1 (6) 0 (0) 6 (38) 3 (18)

Female 157 18 11.46 �0.05 9 (50) 6 (33) 0 (0) 2 (11) 1 (6)

Age: X2 � 5.7154, df � 1, P < 0.05

Youngc 65 3 4.62 �0.05 1 (33) 0 (0) 0 (0) 0 (0) 2 (67)

Adult 174 31 17.82 �0.06 14 (45) 7 (23) 0 (0) 8 (26) 2 (6)

a Numbers in bracket indicate percentage (approximate) of Trypanosome species.b Unidenti®ed (as in Table 1).c Young: 1 year or less: no permanent teeth.

112 A.U. Kalu et al. / Small Ruminant Research 40 (2001) 109±115

df � 1, P < 0:05) and goats (X2 � 6:093, df � 1,

P < 0:05).

Infections were highest between September and

February. Rarely did infections for other months

of the year attain the annual average. Generally,

infection rates were also higher in males than females

and in adults than young stock. Differences in

infection rates among age groups were signi®cant

in all species studied (Tables 1and 2) and between

the gender in peri-domestic goats (X2 � 22:346,

df � 1, P < 0:01) but not in extensively-grazed

sheep (X2 � 0:195, df � 1, P > 0:05). Kids had

low infection rate (4.62%; 0.046, Cl: 0.016, 0.096).

Besides, 67% of all trypanosome positive cases were

infected by parasites whose concentration was so

low as to be diagnosed only by the concentration

method(s).

3.3. Prevalence of trypanosome species

Trypanosoma vivax was the predominant species

diagnosed; it accounted for 44±57% (mean 49.3%) of

all infections. It was most common among ewes

under nomadic management and responsible for

the only diagnosable trypanosomaemia in kids

(Table 3). T. congolense and mixed trypanosome

populations were diagnosed at a mean of 15% in all

herds; their highest species-speci®c attack rate was,

however, recorded in goats (38%). Infections with T.

brucei were not encountered in lambs (Table 2) nor in

goats (Table 3). The packed cell volume (PCV) of

infected and parasite-free goats (23:8� 2:8 and

24:5� 2:1%, respectively), did not differ signi®cantly

(P > 0:05). Corresponding ®gures for ovine herds

(21:3� 1:8 and 25:6� 2:2%) were signi®cantly dif-

ferent (P < 0:05).

4. Discussion

This study showed high prevalence of trypanosome

infection in small ruminants under extensive manage-

ment (sheep) compared to semi-intensive manage-

ment (peri-domestic) goats in an area under light

riverine tsetse (G. tachinoides) challenge. The results

are similar to those documented for dwarf sheep and

goats owned by small indigenous farmers at Nsukka

by Krammer (1966), and among trypanotolerant

(taurine) cattle (Godfrey et al., 1964) and their crosses

(Kalu, 1995a) in central Nigeria. The site of the

present study and those of these previous workers

are within the same vegetational zone and under

similar tsetse challenge: Kalu et al. (1991) and Kalu

(1996) had recorded G. tachinoides at an apparent

density of 0.07 and 0.14 ¯ies/trap/day, respectively.

Also, on the western part of the same zone, Ikede

(1987) documented high infection rate (28.0%) among

trypanotolerant cattle at Government ranches.

In other parts of the country, infection rates reported

for small ruminants have been below 10% (Joshua and

Ige, 1983; Kalejaiye et al., 1995; Nawathe et al., 1996;

Kalu and Lawani, 1996; Dadah et al., 1997). These

reports come from northern Nigeria where the tsetse

eradication programme had successfully reduced the

population of the vector. Besides lack of vector control

in the derived guinea zone, many other factors con-

tributed to the high prevalence recorded. First, G.

tachinoides can exist in isolated pockets of forests,

small thickets, clumps of trees, etc. (Nash, 1970)

under conditions unsuitable for other tsetse species

and is a vector of animal trypanosomosis throughout

its range while still transmitting sleeping sickness (the

human disease) locally. Baldry (1964) estimated that

1% of G. tachinoides feed on sheep and goats and that

4% of these are infected with T. vivax Ð a species

which was frequently encountered during the study.

Secondly, herd owners in Nigeria (Kalu et al., 1991)

and other parts of Africa (Mahmaud and Elmalik,

1977) do not incorporate small ruminants into che-

moprophylactic and chemotherapeutic programmes

(as they do for their cattle) because of the trypanoto-

lerant status ascribed to these small stock and eco-

nomic considerations. In effect, once these animals

receive infective bites they may remain infected for

long periods if not self-cured. Thirdly, the relationship

between riverine tsetse and their hosts are usually

prolonged and personal (Nash, 1970). Such associa-

tion between G. gambiensis and sentinel cattle have

been responsible for all trypanosome infections in

west Africa (Goodwin et al., 1986).

The literature on the prevalence of infections in

small ruminants are few and give no clear indication

on their degrees of tolerance under ®eld conditions.

More infections have been reported in goats than

sheep by Krammer (1966), Nawathe et al. (1995)

and Dadah et al. (1997) while the reverse has been

A.U. Kalu et al. / Small Ruminant Research 40 (2001) 109±115 113

documented by Kalu et al. (1991). The species-

speci®c prevalence recorded here was not intended

for comparison: the results are more relevant as a

measure of the effect of management on the disease in

small ruminants. Extensive management and pastor-

alism have been shown to enhance trypanosomosis

(Kalu et al., 1991; Kalu, 1995a) as found here between

extensively-reared sheep, and goats under semi-inten-

sive (peri-domestic) management.

The ®nding of T. vivax as the predominant species in

the area studied agrees with many published reports in

Nigeria (Krammer, 1966; Folkers and Jones-Davies,

1966; Joshua and Ige, 1983; Kalu et al., 1991; Kale-

jaiye et al., 1995; Nawathe et al., 1995; Dadah et al.,

1997). This situation is typical of the West African

sub-region unless when drug treatment suppress the

vivax population (Kalu, 1996). The ubiquitous nature

of T. vivax has been attributed to its short-life cycle in

the tsetse ¯y, large size and motility (and thereby ease

of diagnosis), restriction and equitable distribution of

the parasite in the general circulation and its potential

to be transmitted by other biting ¯ies (Kalu, 1996). In

addition, a combination of many diagnostic techni-

ques as used in the study would ensure a low propor-

tion of missed diagnosis. The high prevalence in

Yankassa sheep with all three pathogenic trypano-

somes, the presence of sub-clinical infections, and

mixed population of these parasites in an area endemic

for sleeping sickness increases the possibility of these

animals acting as reservoirs of infections to man and

his domestic animals.

5. Conclusions

A high prevalence of trypanosome infections

among extensively-reared Yankassa sheep (38.2%)

and peri-domestic (semi-intensively managed) West

African Dwarf � Red Sokoto goats (14.2%) was

diagnosed in the old Tiv sleeping sickness endemic

foci of central Nigeria. The infections maintained by

low density of Glossina tachinoides, which can trans-

mit the parasites which cause sleeping sickness and

animal trypanosomosis, have serious epidemiological

implications for both man and domestic animals. It is

recommended that small ruminants be incorporated

into therapeutic and preventive programmes against

trypanosomosis in this region.

Acknowledgements

The authors are grateful to the Nigerian Institute for

Trypanosomiasis Research (NITR), Kaduna for grant

to AUK. The technical assistance of Messrs Enoch

Haruna, Francis Doro and Yusuf Abdullahi is also

acknowledged.

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