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Journal of Public Health and Epidemiology Vol. 2(5), pp. 100-108, August 2010
Available online at http://www.academicjournals.org/jphe
©2010 Academic Journals
Full Length Research Paper
Factors influencing the sero-prevalence of
Trypanosoma brucei gambiense sleeping sickness in
Juba District, Central Equatoria State, Southern Sudan
Yassir Osman Mohammed1, Khitma Hassan ElMalik2, Mohammed Musa Mohammed-Ahmed3
and Intisar Elrayah4*
1Department of Tsetse and Trypanosomosis Control, Centeral Veterinary Research Laboratries (CVRL),
Federal Ministry of Science and Technology, Sudan.
2Faculty of Veterinary Medicine, University of Khartoum, Sudan.
3Faculty of Veterinary Medicine and Animal Production, Sudan University of Science and Technology, Sudan.
4Tropical Medicine Research Institute (TMRI), Federal Ministry of Science and Technology, Sudan.
Accepted 19 May, 2010
A surveillance of the Gambian type of Human African Trypanosomosis (HAT) conducted in Juba area
using the Card Agglutination Test for Trypanosomosis (CATT) showed that 257 (11.1%) out of 2322
individuals were sero-positive. The sero-positive rate in the pooled adults was higher but not
significanty different from that of the pooled children. The adult females sero-prevalence rate was
significantly higher than those of adult males, male or female children. There were no significant
differences in the sero-prevalence rates between adult men and male or female children. The internally-
displaced group and the military personnel showed statistically higher sero-positive rates than the
resident groups regardless of the presence or absence of the only extant tsetse species, Glossina
fuscipes fuscipes. The proportions of sero-positives differed significantly between locations in the
study area. The respondents examined along the riverine vegetation had a statistically higher encounter
with the disease than those in the derived savanna and the open savanna woodland. There was no
significant correlation between the density of G. fuscipes fuscipes and the incidence of Trypanosoma
brucei gambiense.
Key words: CATT, sero-prevalence, sleeping sickness, HAT, Gambian type.
INTRODUCTION
At the end of the19th century, sleeping sickness
decimated the populations of vast areas in the Equatoria
region of Southern Sudan (Kuzoe, 1991). The devasta-
ting epidemic in Southern Sudan was attributed to the
Gambian form of the disease (Bloss, 1960; Ford, 1971)
although, Sudan lies in the edge of the geographical
distribution of the rhodesiense and gambiense, the two
*Coressponding author. E-mail: intisar62@yahoo.com. Tel:
+249-912234657.
Abbreviations: HAT, Human African trypanosomosis; CATT,
card agglutination test for trypanosomosis.
types of sleeping sickness. Additionally, at that time there
were no effective diagnostic techniques, which might
have lead to the suspicion that the causative agent was
anything other than Trypanosoma brucei gambiense. The
main characteristic feature of the history of Human
African Trypanosomosis (HAT) in the Sudan is a cycling
between periodic devastating epidemics interspersed
with long periods of low-level endemicity.
The epidemics of sleeping sickness flared up mainly as
a sequel to civil unrest in the country or its neighbours,
the Congo and Uganda, most likely due to population
dislocation and the collapse of the health system it
caused (Hunt and Bloss, 1945; Bloss, 1960; Hutchinson,
1975; Snow, 1983; 1984; Kuzoe, 1993; Moore et al.,
1999; Moore and Richer, 2001).
Mohammed et al. 101
Figure 1. Study area showing the various location surveyed for tsetse and Gampian sleeping sickness in Bahr El Jebel State,
Sudan.
Presently, the national efforts are expanding to address
the problems posed by sleeping sickness in Southern
Sudan. Yet, there are serious limiting factors that restrict
and suspend these efforts. These include security and
instability altogether with movement of refugees and the
internally-displaced people which have led to new
epidemiological patterns that are inadequately elucidated.
However, the recent introduction of Card Agglutination
Trypanosomosis Test/ T. brucei gambiense (CATT), a
serodiagnostic screening test for antibodies detection,
during active surveillance has been a major breakthrough
in the control of sleeping sickness (CATT/wb: Magnus et
al.,1978). The present HAT surveillance was conducted
using CATT in the accessible villages around metro-
politan Juba, the Central Equatoria State capital, together
with the accessible camps of the military and internally-
dispalced people.
The main objective was to identify the factors influceing
the sero-prevalence of sleeping sickness in the country in
order to understand the disease epidemiology, and
consequently to formulate a suitable integrated strategy
for control.
MATERIALS AND METHODS
Locations surveyed
The study was conducted in Juba district (Latitude 4˚ 40'-5˚ N and
Longitude 30˚ 30'-31˚ 45' E). The areas covered represented the
major types of vegetation. In the derived savanna woodland west of
Juba town the locations examined were: Nyamini, Koda, Serimon,
El-Jebalain and Rokon, in the open savanna woodland North west
of Juba, the locations were: Kapu, and Luri, in the riverine vege-
tation South of Juba on the western bank of River Bahr El Jebel,
Lologo, Khor Rommalla, Tokiman, Rejaf West, Nyori and on the
eastern bank of the river: Gumbo, Rejaf East, Khor Kit and Logo
East, were screened (Figure 1).
Screening procedures for human African trypanosomosis
At each location visited, at least 95% of the consenting inhabitants
were screened for T. brucei gambiense sleeping sickness using the
card agglutination test for trypanosomosis (CATT/wb: Magnus et
al., 1978). Blood was collected from the basilic veins of consenting
individuals using heparinized capillary tubes. Confirmed CATT
positives were recorded according to location, vegetation,
residence, gender, age group and tsetse occurrence.
Tsetse survey
The biconical trap is effective for sampling Glossina palpalis group
tsetse (Challier et al., 1977; Odulaja and Mohamed-Ahmed, 1997)
and the Epsilon trap is similarly effective against Glossina morsitans
group tsetse (Hargrove and Langley, 1990). Since the two groups
of tsetse flies are thought to occur in the study area both of the
latter traps were used in order to define the tsetse occurrence, their
diversity and apparent densities. In each vegetation type traps were
placed 200 m apart for 3 days during each of the wet and dry
seasons. Captured flies (pooled males and females) were collected
102 J. Public Health Epidemiol.
Table 1. The percentage of inhabitants seropositive for human African trypanosomosis according to
age groups and gender in Juba area, Central Equatoria State, Sudan.
Classification of individuals % sero-prevalence Chi2 value Probability, P
Pooled adults 11.9 (194/1630)
Pooled children 9.10 (63/692) 3.6df = 1 p = 0.058
Pooled males 9.53 (139/1459)
Pooled females 13.67 (118/863) 9.05df = 1 p<0.0026
Pooled adult males 9.45 (104/1100)
Pooled adult females 16.98 (90/530) 18.61df = 1 p<0.00001
Pooled adult males 9.45 (104/1100)
Pooled male children 9.75 (35/359) 3.80df = 1 p>0.9
Pooled adult females 16.98 (90/530)
Pooled female children 8.41 (28/333) 12.02df = 1 p<0.0005
Pooled male children 9.75 (35/359)
Pooled female children 8.41(28/333) 0.23df = 1 p>0.63
every 24 h, identified, sexed and counted. It is a fact that the
transmission of T. b. gambiense occurs among humans is through
the agency of tsetse flies, the palpalis group. For this reason we
tried to find out the relationship between the density of tsetse (x) in
each location and the seroprevalence rate (y) in the same location
using the simple linear regression equation (y = a + bx) where a is
the intercept or constant and (b) is the regfression coefficient or
slope.
RESULTS
Human African trypanosomosis (HAT) sero-
prevalence
The surveillance of HAT, covered 2322 persons. Regard-
less of age and sex, 257 individuals (11.07%) of the total
scanned were seropositive.
Sero-prevalence of HAT based on pooled gender and
age-groups
The results are presented in Table 1. The sero-pre-
valence rate in the pooled adults, although, are relatively
higher than in the pooled children and the difference was
marginally insignificant (Chi2 = 3.6; p = 0.058). However,
regression analysis showed a significant positive
correlation between the square of age of respondents
regardless of sex or location (x) and their HAT
seroprvalence rate (y) (Y = 1.07 + 0.039x; r = 0.9656; df
=169; t = 2.082; p < 0.04). On the other hand, the adult
females sero-prevalence rate was significantly higher
than that of the adult males, male or female children (Chi2
= 9.05; df = 2, p = 0.0026). In contrast, there was no
significant difference in the sero-prevalence
rate between men and male children.
Sero-prevalence of HAT based on residence
The pooled internally-displaced group showed a
statistically higher HAT seropositive rate (p <0.000),
when compared with the pooled resident groups where
Glossina fuscipes fuscipes had been caught in biconical
traps or the pooled resident groups where tsetse had not
been seen in traps. Conversely, paired comparisons
showed insignificant difference in HAT encounter
between the two resident groups (Chi2 = 0.007:p > 0.93)
(Table 2).
HAT sero-prevalence based on gender and age group
in relation to residence
Table 3 compares the sero-prevalence rates in the
internally-displaced respondents according to gender and
age group. Paired comparisons showed significant
variations between pairs excluding the male
children/female children. Furthermore, comparisons
between residents of tsetse infested areas showed
essentially similar sero-prevalence rates irrespective of
sex or age (Table 4). However, for the inhabitants of
tsetse free areas there were significant discrepancies in
sero-prevalence rates between sexes and age groups
barring adult female/female children and male children/
female children (Table 5). Subsequent regression
Mohammed et al. 103
Table 2. The percentage of male and female inhabitants seropositive for Human African Trypanosomosis
according to residence in Juba area, Central Equatoria State, Sudan.
Classification of individuals % sero-prevalence Chi2 value Probability, P
Total displaced 18.09 (131/724)
Total resident with tsetse 7.93 (23/290)
Total resident with no tsetse 7.87 (103/1308)
52.75
df = 2
P<0.000
Total displaced 18.09 (131/724)
Total resident with tsetse 7.93 (23/290)
15.82
df = 1
P<0.0007
Total displaced 18.09 (131/724)
Total resident with no tsetse 7.87 (103/1308)
46.76
df = 1
P<0.000
Total resident with tsetse 7.939 (23/290)
Total resident with no tsetse 7.87 (103/1308)
0.007
df = 1
P>0.93
Table 3. The percentage of internally-displaced people seropositive for human African trypanosomosis
according to gender and age-groups in Juba area, Central Equatoria State, Sudan.
Classification of individuals % sero-prevalence Chi2 value Probability, P
Pooled adults 26.93 (108/401)
Pooled children 9.16 (23/251) 28.46 df = 1 p<0.000
Pooled adult males 21.97 (49/223)
Pooled adult females 49.58 (59/178) 5.724 df = 1 p<0.0167
Pooled adult males 21.97 (49/223)
Pooled male children 9.09 (11/121) 8.167 df = 1 p<0.0042
Pooled adult females 49.58 (59/178)
Pooled female children 9.23 (12/130) 22.89 df = 1 p<0.000
Pooled male children 9.09 (11/121)
Pooled female children 9.23 (12/130) 0.0325 df = 1 p>0.857
Table 4. The percentage of human African trypanosomosis seropositive residents of tsetse infested
areas according to gender and age-groups in Juba area, Central Equatoria State, Sudan.
Classification of individuals % sero-prevalence Chi2 value Probability, P
Pooled adults 9.05 (20/221)
Pooled children 4.35 (3/69)
1.01 df = 1 p>0.314
Pooled adult males 9.30 (16/172)
Pooled adult females 8.16 (4/49)
1.371 df = 1 p>0.971
Pooled adult males 9.30 (16/172)
Pooled male children 2.94 (1/34)
0.793 df = 1 p>0.373
Pooled adult females 8.16 (4/49)
Pooled female children 5.71 (2/35)
0.0 df = 1 p = 1
Pooled male children 2.49 (1/34)
Pooled female children 5.71 (2/35)
0.0007 df = 1 p>0.979
104 J. Public Health Epidemiol.
Table 5. The percentage of human African trypanosomosis seropositive inhabitants of tsetse free
areas according to gender and age-groups in Juba area, Central Equatoria State, Sudan.
Classification of individuals % sero-prevalence Chi2 value Probability, P
Pooled adults 7.05 (66/936)
Pooled children 15.55 (37/275) 10.39 df = 1 p<0.00126
Pooled adult males 5.53 (39/705)
Pooled adult females 11.69 (27/231) 9.144 df = 1 p<0.00249
Pooled adult males 5.53 (39/705)
Pooled male children 11.27 (23/204) 7.331 df = 1 p<0.0067
Pooled adult females 11.69 (27/231)
Pooled female children 8.33 (14/71) 2.339 df = 1 p>0.126
Pooled male children 11.27 (23/204)
Pooled female children 8.33 (14/71) 2.54 df = 1 p>0.11
analysis showed a significant positive correlation bet-
ween the square of age of the internally-displaced female
respondents (x) and their HAT sero-prevalence (y) (Y =
3.457 + 0.0002x; r + 0.9418; df =28 ; t = 14.077; p <
0.000001). No similar siignificant correlations could be
established between age and HAT seroprvalence in any
other group, irrespective of type of residence (p > 0.2 -
0.9).
Variation of human African trypanosomosis sero-
prevalence with vegetation type
The results shown in Table 6 reveal that the respondents
examined along the riverine vegetation had a statistically
higher encounter with the disease compared with those in
the derived savanna woodland or the open savanna
woodland.
Sero-prevalence of human African trypanosomosis
based on location of respondents
The pooled sero-prevalence of the disease was relatively
high in Lologo, Khor Rommalla, Tokiman, Gumbo and
Kapu locations where the internally-displaced people
were being settled at the time of the survey. Analysis of
sero-prevalence data obtained on the displaced people
showed a significant difference between settlers loca-
tions, probably highlighting their encounter with varing
trypanosomosis challenge either at their abandoned
original homes or enroute to these camps. Similar treat-
ment of data, pertaining to military personnel (all adult
males) who were prepetually (and are) on the move
showed a relatively high sero-prevalence rate. As with
the displaced people, there was also significant variation
between locations. In contrast, Table 7 clearly suggests
that the encounter of the diseases among residents in
established villages and hamlets was relatively low with
insignificant difference in sero-prevalence rates between
these villages.
Relationship between human African
trypanosomosis sero-prevalence and density of G.
fuscipes fuscipes
Regression analysis (Table 8) showed no significant
correlation between the density of G. f. fuscipes and the
sero-prevalence of HAT in Southern Sudan (r + 0.698; p
= 0.191; df = 8).
DISCUSSION
An active surveillance was conducted in reachable
villages and camps around Juba, the Central Equatoria
State capital. Under civil conflict circumstances time and
efficiency are vital factors. For these reasons the card-
agglutination test for trypanosomosis (CATT), is a
serologic technique, highly sensitive and efficient for
diagnosis of T. b. gambiense sleeping sickness (Magnus
et al., 1978) and recommended for active surveillance to
estimate the disease sero-prevelance rate was adopted
(W H O, 1998). Moreover, the test is quick, easy to
perform and permits the examination of hundreds of
people each day (Chappuis et al., 2002, 2004).
In the present study some 2322 consenting individuals
in Juba area were screened for gambiense HAT. Of
these 257 (11.1%) were seropositive. This level of sero-
prevalence is almost identical to those levels regarded as
epidemics in Western Equatoria (Moore et al., 1999;
Mohammed et al. 105
Table 6. Comparisons between human African trypanosomosis seropositive individuals in open savanna
woodland, derived savanna woodland and riverine vegetation, Juba area, Central Equatoria State, Sudan.
Vegetation % sero-prevalence Chi2 value Probability, P
Open savanna inhabitants 4.93 (17/345)
Derived savanna inhabitants 7.04 (78/1108)
Riverine vegetation inhabitants 18.64 (162/869)
82.13 df = 2 p<0.000
Open savanna inhabitants 4.93 (17/345
Derived savanna inhabitants 7.04 (78/1108)
1.59 df = 1 p>0.207
Open savanna inhabitants 4.93 (17/345)
Riverine vegetation inhabitants 18.64 (162/869)
35.87 df = 1 p<0.000
Derived savanna inhabitants 7.04 (78/1108)
Riverine vegetation inhabitants 18.64 (162/869)
60.39 df = 1 p<0.000
Table 7. The perecntage of human African trypanosomosis seropositives according to locations and
residence in Juba area, Central Equatoria State, Sudan.
Residence Village % sero-prevalence Chi2 value Probability, P
Lologo 38.03 (81/213)
Khor Rommalla 21.36 (22/103)
Tokiman 14.81 (4/27)
Gumbo 7.04 (7/94)
Kabu 5.92 (17/287)
Displaced camps
Sub-total 18.09 (131/724)
93.92 df = 4 p <0.000
Rejaf East 12.5 (25/200)
Kit 7.69 (1/13)
Logo East 8.22 (6/73)
Rejaf West 12.5 (11/88)
Nyori 8.62 (5/58)
Luri 0 (0/58)
Permanent resident
Sub-total 9.8 (48/490)
1.698 df =5 p>0.79
Nyamini 15.14 (28/185)
Koda 8.48 (15/177)
Serimon 1.75 (5/285)
El Jebalain 4.76 (8/168)
Rokon 7.51 (22/293)
Mobile military camps
Sub-total 7.04 (78/1108)
32.68 df = 4 p <0.000
Moore and Richer, 2001). It is suggested that the break
down of the health service and the displacement of the
population as a consequence of the civil conflict has
aggravated the situation of sleeping sickness in the area.
During the last decade there has been a similar strong
resurgence of human African trypanosomosis in several
countries including Angola and the Democratic Republic
of Congo (Van Nieuwenhove et al., 2001; Chappuis et al.,
2002). The major cause of these flare-ups is the collapse
of sleeping sickness control programmes as a result of
strife in these countries (Ekwanzala et al., 1996;
Chappuis et al., 2002).
In the surveillance higher sero-prevalence rates were
recorded in adults rather than in children. Similar results
were obtained during a T. b. gambiense sleeping
sickness surveillance in the Ivory Coast (Stanghellini and
Duvallat, 1981). The high sero-prevalence of the disease
in adults might be attributed to the community social
behaviour and daily activities which take the adult into
close and more frequent contact with the vector G.
106 J. Public Health Epidemiol.
Table 8. The sero-prevalence rate of human African
trypanosomosis in relation to G. fuscipes fuscipes apparet density
in Central Equatoria State, Sudan.
Location Fly apparent density Sero-prevalence rate
Rejaf East 0.0 12.50 (25/200)
Kit 3.5±0.65 07.69 (01/13)
Logo Eat 4.0±1.15 08.22 (06/73)
Rejaf West
1.3±0.88 12.50 (11/88)
Nyori 5.0±1.15 08.22 (05/58)
Luri 0.0±0.30 00.00 (0.0/58)
Y = 2.826 + 1.62x; r + 0.696; df + 4; t + 1.681; P>0.191
Fly apparent density = (male +female tsetse/trap/day)
Sero-prevalence rate =(total number of seropositives divided by total
examined at a location, between parentheses)
fuscipes fuscipes in watering sites. In general terms, the
frequency of human/fly contact decides the disease
incidence rate (Gouteux, 1985).
In the present work, the sero-prevalence rates were
found to be significantly higher in adult females and
children compared with that of adult men (p < 0.0005;
Chi2 = 9). It has been observed that there are substantial
variations between men and women in the type and
duration of their daily activities within the local tsetse
biotopes where the disease might be transmitted,
possibly resulting in profound differences in exposure
between men and women and the children who, usually
pursue their mothers. The adult men are mainly traders,
agropastoralist and junior workers in government offices
thus they have lower intensity of fly-contact compared
with women. Recently, there has been considerable
interest towards the influence of sex or gender on tropical
diseases, sex referring to a biological characteristic while
gender denotes socially constructed behaviour, expecta-
tions and roles that derive from, but may not depend on
sex (Vlassoff and Manderson, 1998). It has been
perceived that women had higher apparent incidence of
Gambian trypanosomosis than men due to their selective
activities which take them into contact with tsetse e.g.
water collection, washing, firewood cutting and bathing.
Children, especially girls, usually follow their mothers
(Pepin et al., 2002). Dissimilarity in incidence of African
trypanosomosis between genders was reported in many
countreies. For instance in Fankana-Kalakitini, Kwamouth
and Nioki foci of the Congo women had higher incidence
of trypanosomosis than men (Henry et al., 1982; Pepin et
al., 2002). Conversely, in other African countries, the inci-
dence was higher in males in some foci. The differences
in population structures of endemic villages as well as the
differences in exposure to infected tsetse between men
and women probably explain most of the gender variation
in the incidence of HAT (Pepin and Meda, 2001).
In the present work the HAT sero-prevalence rate of
the internally-displaced people and military was signi-
ficantly higher than that scored for the resident population.
This might be due to the fact that the internally-displaced
people and the military had probably come from highly
endemic foci of sleeping sickness in Western Equatoria
where they might have harboured the infection before
they migrated or operated as a result of the civil unrest.
The role of the population sectors who are perpetually on
the move in the spread of HAT is well established in the
literature and had already been discussed (Adekolu-
John, 1978). In our study, the high prevalence of the
disease recorded in certain locations and its absence or
low prevalence in others, might be attributed to the
presence of the internally-displaced people –including the
government soldiers, the presence or absence of tsetse
in the location and the daily activity of residents in
endemic areas. Thus, the differences in the sero-
prevalence rates of T. b. gambiense in Juba area is in
tandem with patterns of the disease in Central Africa
including Uganda and the Kenya shores of lake Victoria
(Hide, 1999; Van Nieuwenhove et al., 2001).
Significantly, higher prevalence of HAT was detected in
residents who dwell close to or visit rivers and water-
courses where G .f. fuscipes exists: in riverine galleries,
thickets and farm hedges. Thus, people living or visiting
these fly haunts are exposed to higher frequency of
tsetse bites and hence, are at a higher risk of contracting
sleeping sickness (Mulligan, 1970; Gouteux, 1985).
Moreover, the war has forced the residents to flee their
villages to hide in the riverine vegetation where G. f.
fuscipes occurs.
It is well known that the palpalis group tsetse are more
dependent on riverside vegetation (De La Rocque et al.,
2001) and much less affected by human settlement. They
are also better able to adapt to transformed environments
as long as the vegetation cover provides them with
appropriate habitats. Indeed G. f. fuscipes , a riverine
tsetse, was reported to adjust itself in changing habitats
(Okoth,1982). Due to their opportunistic feeding habits,
the palpalis tsetse are also able to adapt from a pre-
ference for feeding on wild animals to feeding mainly on
reptiles, humans and domestic animals (Cuisance et al.,
1973; Jordan, 1989; Mohamed-Ahmed and Odulaja,
1997; Clausen et al.,1998). They are also more capable
of adapting to peri-domestic habitats (Toure, 1974; Kuzoe
et al., 1985). Adaptation to peri-domestic habitats
together with the opportunistic feeding habits enable G. f.
fuscipes to survive and to tolerate the adverse effect of
game animals rarity (Weitz, 1963, 1970; Boyt et al., 1978;
Okoth, 1986). Thus, creation of peri-domestic
environments suitable for the fly might result in new HAT
epidemiological systems closly linked to humans (De La
Rocque et al., 1998). Indeed, due to the civil strife in
southern Sudan people were settling in hamlets along the
watercourses concealed in the riverine vegetation for
security reasons. This may explain why the sero-
prevalence rate was higher in riverine vegetations rather
than savanna areas or inside villages.
Correlation analysis showed no significant association
between HAT sero-prevalence rate in a location and the
density of G. f. fuscipes in that location (Table 8). This
finding agrees with most reports from sleeping sickness
foci elsewhere in Africa where no significant relationship
was demonstrated between the incidence of Gambian
sleeping sickness in inhabitants and the density of
species of riverine tsetse (Gouteux et al., 1993). Con-
versely, in the Central African Republic the rate of T. b.
gambiense transmission was found to be significantly
correlated with the density of the vector fly (Leak, 1999).
The above results confirm the presence of T. b.
gambiense sleeping sickness in Juba area but do not
eliminate the possibility of infection with Trypanosoma
brucei rohdesiense , as CATT appears to be sensitive for
the former only. The Sudan lies in the interface of the
geographical location of the two types of sleeping
sickness (Baker et al., 1970). Considering the instability
of people and their livestock due to the war there is surely
a high likelihood of the spread and overlap of the two
types of sleeping sicknesses. Furthermore, some strain
of T. b gambiense lack the specific gene coding for
CATT-antigen (Penchenier et al., 2003), consequently,
the level of the seropositive obtained here almost cer-
tainly underestimated the true prevalence of infection. For
these reasons the use of other diagnostic devices and
procedures that might help to detect the true infection
with both T. b. gambiense and T. b. rohdesiense are
demanded.
ACKNOWLEDGEMENTS
The TDR/WHO Project No. ID 990917, T16/181/530 and
Eastern African Network of Trypanosomosis (EANETT)
financial and technical support throughout this study are
appreciated. Our gratitude goes to the Tropical Medicine
Research Institute (TMRI) and the Central Veterinary
Research Laboratories (CVRL) staff for their efforts and
assistance.
REFERENCES
Adekolu-John EO (1978). The significance of migrant Fulani for human
trypanosomiasis in Kainji lake areas of Nigeria. Trop. Geogr. Med.,
30: 285-293.
Baker JR, Mc Connel E, Kent DC, Hady J (1970). Human
Trypanosomiasis in Ethiopia. Trans. Royal Society Trop. Med.
Hygiene, 64: 523-530.
Bloss JFE (1960). The history of sleeping sickness in the Sudan.
Proceedings Royal Society Med., 53: 421-426.
Boyt WP, Mackenzie PK, Pilson RD (1978).The relative attractiveness
of donkeys, cattle, sheep and goat to Glossina morsitans morsitans
Westwood and G. pallidipes Austen (Diptera: Glossinidae) in a
middleveld area of Rhodesia. Bull. Entomol. Res., 68: 497-500.
Challier A, Eyraud M, Lafaye A, Laveissiére C (1977). Amélioration du
rendement du piége biconique pour glossines (Diptera, Glossinidae)
par emploi un cône inférieur bleu. Cahiers ORSTOM, série
Entomologie médicate et parasitologie, 15: 283-286.
Chappuis F, Pitter A, Bovier PA, Adams K, Godinequ V, Hwang SY,
Magnus E, Buscher P (2002). Field evaluation of the
CATT/Trypanosoma brucei gambiense on blood-impregnated filter
Mohammed et al. 107
papers for diagnosis of human African trypanosomiasis in southern
Sudan. Trop. Med. Int. Health, 7(11): 942-948.
Clausen PH, Adeyemi I, Bauer B, Breloeer M, Salchow F, Staak
C(1998). Host preferences of tsetse (Diptera: Glossinidae) based on
blood meal identification. Med. Vet. Entomol., 12: 169-180.
Cuisance D, Itard J, Boreham PFL (1973). Comportement des mâles
steriles de Glossina tachinoides West., laches dans les conditions
naturelles. Environs de Fort Lamy (Tchad)., 111. Lieux et hauteurs de
repos; comportements alimentaries. Revue Elevage et de Médecine
Vétérinarire des Pays Tropicaux, 26: 323-338.
De La Rocque S, Augusseau X, Guillobez S, Michel V , De Wispelaere
G, Bauer B, Cuisancw D (2001). The changing distribution of two
riverine tsetse flies over 15 years in an increasingly cultivated area of
Burkina Faso. B. Entomol. Res., 91: 157-166.
De La Rocque S, Lefrancois T, Rrifenberg JM, Solano P, Kabore I,
Bengaly Z, Augusseau X, Cuisance D (1998). PCR analysis and
spatial repartition of trypanosomes infecting tsetse flies in
Sideradougou area (Burkina Faso). Annal. New York Acad. Sci., 849:
32-38.
Ekwanzala M, Pepin J, Khonde N, Molisho S, Bruneel H, De Wals P
(1996). In the heart of darkness: sleeping sickness in Zaire. Lancet,
348: 1427-1430.
Ford J (1971). The Role of Trypanosomiasis in African Ecology,
Oxford, Clarendon Press.
Gouteux JP (1985). Ecologie des Glossines en secteur pré-forestiére de
Côte Ivoire Relation avec la trypanosomiases humaine et
possibilités de lutte. Annales de Parasitoloie Humaine et Comparée,
60: 329-347.
Gouteux JP, Kounda JC, Gboumi L, Noutoua D, Amico F, Bailly C,
Roungou JB (1993). Man-fly contact in the Gambian trypanosomiasis
focus of Nola-Bilolo (Cenral Africa Republic). Trop. Med. Parasitol.,
44: 213-218.
Hargrove JW, Langley PA (1990). Sterilising tsetse (Diptera:
Glossinidae) in the field: a successful trial., Bull. Entomol. Res., 80:
397-403.
Henry MC, Ruppo JFl, Bruneel H (1982). Distribution de infection Par
T. b. gambiense dans une population du Bandundu en République du
Zaire. Annales de la Société Belge de Médecine Tropicale, 62: 301-
313.
Hide G (1999). History of sleeping sickness in East Africa. Clin.
Microbiol. Rev., 12(1): 112-125.
Hunt AR, Bloss JFE (1945). Tsetse fly control and sleeping sickness in
the Sudan. Trans. Royal Society Trop. Med. Hygiene, 39: 43-58.
Hutchinson MP (1975). Assignment report: trypanosomiasis in southern
Sudan. 29 April1974 - 31 March 1975. WHO, EM/PD/5 (or
EM/SUD/MPD/005/FR (UNHCR) (2301)) May 1975.
Jordan AM (1989). Importance of land use on the incidence of
Trypanosoma brucei gambiense sleeping sickness. Annales de la
Société Belge de Médecine Tropicale, 69(1): 254.
Kuzoe FAS (1991). Perspectives in research on and control of African
trypanosomiasis. Ann. Trop. Med. Parasitol., 85(1): 33-41.
Kuzoe FAS (1993). Current situation of African trypanosomiasis. Acta
Tropica, 54: 153-162.
Kuzoe FAS, Baldry DAT, Van Der Vloedt A, Cullens JR (1985).
Observation of an apparent population extension of Glossina
tachinoides Westwood in southern Ivory Coast. Insect Sci. its Appl.,
6: 55-58.
Leak SGA (1999). Tsetse Biology and Ecology: Their role in the
epidemiology and control of trypanosomosis. ILRI, Nairobi, Kenya.
CAB Publishing.
Magnus E, Vervoort T, Van meirvenne N (1978). A card- agglutination
test with stained trypanosomes (CATT) for serological diagnosis of T.
b. gambiense trypanosomiasis. Annales de la societe belge de
Medecine Tropical., 58: 169-196.
Mohamed-Ahmed MM, Odulaja A (1997). Diel activity patterns and host
preferences of Glossina fuscipes fuscipes along the shores of Lake
Victoria, Kenya. Bull. Entomol. Res., 87: 179-186.
Moore A, Richer M (2001). Re-emergence of epidemic sleeping
sickness in southern Sudan. Trop. Med. Int. Health, 6(5): 342-348.
Moore A, Richer M, Enrile M, Losio E, Roberts J, Levy D (1999).
Resurgence of sleeping sickness in Tambura county, Sudan. Am. J.
Trop. Med. Hygiene, 61: 315-318.
108 J. Public Health Epidemiol.
Mulligan HW (1970). The African Trypanosomiasis, London, George
Allen and Unwin. Odulaja A, Mohamed-Ahmed MM (1997),
Estimation of the efficiency of the Biconical trap for Glossina fuscipes
fuscipes along the Lake Victoria shore, Kenya., Entomologia
Experimentalis et Applicata, 82: 19-24.
Okoth JO (1982). Further observations on the composition of Glossina
population at Lugala, South Busoga District, Uganda. East Afr. Med.
J., 59: 582-584.
Okoth JO (1986). Peridomestic breeding sites of Glossina fuscipes
fuscipes Newst. In Busoga,Uganda, and epidemiological implications
for trypanosomiasis. Acta Tropica, 43: 283-286.
Penchenier L, Grébaut P, Njokou F, Eboo Eyenga V, Büscher P (2003).
Evaluation of LATEX /T.b. gambiense for mass screening of
Trypanosoma brucie gambiense sleeping sickness in Central Africa.
Acta Tropica, 85(1): 31-37.
Pepin J, Meda H (2001). The epidemiology and control of African
trypanosomiasis. Adv. Parasitol., 40: 71-132.
Pepin J, Mpia B, Iloasebe M (2002).Trypanosoma brucie gambiense
African trypanosomiasis: differences between men and women in
severity of disease and response to treatment. Trans. Royal society
Trop. Med. Hygiene, 96: 421-426.
Snow WF (1983). Assignment Report: Tsetse distribution and ecology
in relation to sleeping sickness in Southern Sudan. May- June 1982,
WHO, EM/PD/5: EM/SUD/MPD/005/ FR (UNHCR) (2301).
Snow WF (1984). Assignment Report: Further observation on tsetse
distribution, ecology and control in relation to sleeping sickness in
southern Sudan., 12 February- 13 June 1983, WHO.
Stanghellini A, Duvallat G (1981). The epidemiology of human
trypanosomiasis due to Trypanosoma gambiense in a focus of the
Ivory Coast. 1. The distribution of the disease in the population. Z.
Tropenmed. Parasit., 32(3): 141-144.
Toure SM (1974). Note sure quelques particultarites dans habital de
Glossina palpalis gambiensis (Diptera : Glossinidae) observées au
Sénégal. Revue Elevage et de Médecine Vétérinarire des Pays
Tropicaux, 27: 81-94.
Van Nieuwenhove S, Betu-Ku-Mesu VK, Diabakana PM, Declercq J,
Bilenge C MM (2001). Sleeping sickness resurgence in the DRC: the
past decade. Trop. Med. Int. Health, 6(5): 335-341.
Vlassoff C, Manderson L. (1998). Incorporating gender in the
anthropology of infectious diseases. Trop. Med. Int. Health, 3: 1011-
1019.
Weitz B (1963). The feeding habits of Glossina. Bull. World Health
Organ., 28: 711-729.
Weitz B (1970). Hosts of Glossina.: The African Trypanosomiases,
London, George Allen and Unwin Ltd., pp: 416-423
World Health Organization (1998). Cnotrol and Surveillance of African
Trypanosomiasis. WHO Technical Report Series 881, WHO, Geneva.