Reprinted from veterinary parasitology An...
Reprinted from
veterinary
parasitology
An International Scientific Journal
Veterinary Parasitology 81 (1999) 235-247
Tsetse challenge, trypanosome and helminth
infection in relation to productivity of
village Ndama cattle in Senegal
A. FallaqbT*, A. Diack”, A. Dis”,
, G.D.M. d’Ieterend
“Institut S&&alais de Recherches Agricoles, CR.U Kolda, BP 52, Kolda, Senegal
hCentre for Tropical Veterinary Medicine, Easter Bush Roslin, Midlothian, EH25 9RG, UK
‘Institut Sénégalais de Recherches Agricoles, LNERI! BP 2057, DakaG Senegal
dIntematioml
Livestock Research Institute, P.0. Box 30 709, Nairobi, Kenya
Received 13 January 1998; accepted 24 July 1998
ELStiIER
veterinary parasitology
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veterinaty
parasitology
ELSEVIER
Veterinary Parasitology 81 (1999) 235-247
Tsetse challenge, trypanosome and helminth
infection in relation to productivity of
village Ndama cattle in Senegal
A. FallapbT*, A. Diack”, A. Diaité”, M. Seye”, G.D.M. d’Ieterend
“institut Sénégalais de Recherches Agricoles, CRz/ Kolda, BP 52, Kolda, Senegal
“Centre,for Tropical Veterinary Medicine, Easter Bush Roslin. Midlothiun. EH25 9RG, UK
‘Institut Sénégalais de Recherches Agricoles. LNERI! BP 2057, Dakar Scnegal
dlnternational Livestock Research Institute, J?O. Box 30 709, Nairobi. Kenya
Received 13 January 1998; accepted 24 July 1998
-..-~.- ~---.
Abstract
Data on tsetse fly, and on village Ndama cattle collected over a 4-year period in southern
Senegal, were analysed. A total of 431 Ndama cattle in four herds of three villages in the Upper
Casamance area of southern Senegal were monitored monthly. Glossina morsituns suhmorsitans
and Glossina palpalis gumbiensis are present in the study area. Mean tsetse apparent density was
5.4 fliesltraplday. Trypanosome (Trypanosoma congonlense and Trypanosoma vivux) infection rate
in flies was 2.4 (s.e. 0.37)%. Tsetse challenge index was 17.3 (s.e. 4.18). Mean monthly
trypanosome prevalence in cattle was 2.5 (s.e. OSl)%. Highest trypanosome prevalence occurred
during the dry season, and animals less than 1-year old were more frequently infected than older
animals. The linear relationship between the loglO+l tsetse challenge and the arcsine of the
trypanosome prevalence was significant only when mean monthly values of these variables over the
4-year period were used with tsetse challenge preceding infection rate by 3 months. Mean monthly
prevalence of strongyle, Strongyloides Spp. , Toxocara spp. and coccidia were 34.4 (s.e. 0.60), 2.1
(s.e. 0.18), 1.2 (s.e. 0.45) and 15.6 (s.e. 0.47)%, respectively. Calf mortality rate at 1, 6 and 12
months of age was 2.1 (s.e. 2.1), 5.2 (s.e. 2.8) and 12.2 (s.e. 3.3)%, respectively. Calving interval
(584 s.e. 58 days) was not influenced by trypanosome status of the cow during lactation. Calving
interval was shorter by 167 days when the calf died before 1 year of age in comparison to calving
intervals for which the calf survived beyond one year. Live weight at birth, 6 and 12 months of age
were 15.8 (s.e. 0.54). 48.1 (s.e. 2.56) and 71.1 (s.e. 5.44) kg, respectively. Mean lactation length,
total and daily milk offtake were 389 (s.e. 16) days, 231 (s.e. 15) litres and 0.69 (s.e. 0.037) litres,
respectively. Trypanosome infection during lactation did not have a significant effect on the amount
* Corresponding author. Tel.: +l-231-3823-678; fax: +1-221-8322-l 18: e-mail: abdoufal@isra.refer.sn
0304.4017/99/$ - see front matter !: 1999 Elsevier Science B.V. Al1 rights reserved.
PII: SO304-4017(98)00213-l
236
A. Fall et ul. /Vetruinary Parusitology 81 (1999) 23.5-247
of milk extracted for human consumption nor did trypanosome status affect calf growth. $7 1999
Elsevier Science B.V. Al1 rights reserved.
Kqvword.~ Tsetse challenge; Trypanosomosis: Helminthiosis; Ndama cattle; Prodnctivity
1. Introduction
Because of their trypanotolerance, Ndama cattle constitute a unique animal genetic
resource which forms the basis of large ruminant agriculture in many parts of West Africa
where the risk of trypanosomosis is high. The Ndama cattle breed are a multipurpose
breed that produce milk. meat, power and manure and therefore contribute a great deal to
the income and welfare of millions of farmers in mixed trop-livestock production
systems in West Africa. However, a complex set of technical factors related to health,
nutrition and management constrain the productivity of Ndama cattle kept under
traditional husbandry systems. The relative importance of these factors needs to be
determined if strategies to make better use of this genetic resource are to be developed to
meet the growing demand for animal products in West Africa. TO this end, an
epidemiological study was carried out from 1988 to 1992 in the Upper Casamance region
of southern Senegal to investigate causes of variation of Ndama cattle productivity and
the stability of the trypanotolerance trait under village management systems. This study
was part of a large epidemiological programme that was conducted by International
Livestock Centre for Africa (ILCA now ILRI) and National ,4gricultural Research
Institutes in many sites in Africa with different degrees of trypanosomosis risk. This
paper reports findings on the tsetse challenge, prevalence of parasitic diseases
(helminthiosis, trypanosomosis) in village Ndama cattle in southern Senegal and how
these factors affect the reproduction performance, calf growth and milk production.
2. Materials and methods
2.1. The study area
The study was carried out in the region of Upper Casamance in Southern Senegal. The
climate in this region is of a sudano-guinean type. Annual rainfall was 1018. 1045, 787.
and 684 mm in 1988, 1989, 1990 and 1991, respectively. The unimodal rainfall in this
area occurs between June and October. Four herds in these villages (Salamata, Yassiriba,
Sare Pathe) were selected for the investigation Ndama cattle health characteristics and
production parameters over a 4-year period (1988-1992). Salamata and Yassiriba are
along the Mahon forest boundaries and close to a stream. Sare Pathe is located in the
forest of Bakor. The criteria used to Select villages were the presence of tsetse flies (but
the infection rates were not taken into account), accessibility (particularly during the
rainy season when roads becomc impractical), and farmcrs willingness to participate to
the monitoring program.
A. Fol1 et ul. /Veterinary Pcrrmitology 81 (1999) 235-247
237
2.2. Herd management
Animals graze natural pastures which form the main source of the food supply.
Animals have access to millet, rice and sorghum residues that are consumed directly in
the fields from November. Shortage of food supply during the hot dry season (March,
April, May and June) is the single most important constraint that faces the herd owners in
this area. Animals are tethered individually overnight in trop fields during the dry season
and are moved lo the forest during the cropping season to avoid damage to crops. Mating
is not controlled and calving occurs a11 year round. However, peak calving is recorded in
July and August. Milking is performed once a day, and begins one week after calving.
The calf is allowed to suckle its dam for a few seconds to trigger milk let-down and
thereafter, is tethered at the foot of the dam during the course of milking. A main feature
of the milking system in the study area is that milking for human consumption is
suspended during part of the dry season and is resumed during the next wet season.
2.3. Experimental
design
2.3.1. Animals
A total of 431 Ndama cattle kept in four herds of three villages were monitored
monthly for 52 months in Salamata and Yassiriba with 163 animais, and for 24 months in
Sare Pathe with 268 animals. Animals were individually tagged on both ears. Animals
were managed under traditional village conditions and therefore were subjected to natural
tsetse challenge. Routine vaccination against rinderpest, anthrax, hemorrhagic septicae-
mia, and contagious bovine pleuropneumonia was given. Animals were also treated with
diminazene aceturate (Berenil ” , 3.5 mg kg- ’ body weight) when trypanosomes were
detected and the packed red ce11 volume (PCV) was below 20%.
2.4. Field recording and lahoratoy determinations
2.4.1. Monitorirzg of tsetse f7ie.F
Twelve biconical traps, as described by Challier and Laveissière ( 1973), were placed at
each site each month for three consecutive days and harvested every 24 h. Traps we’re set
100 m apart from each other, in Savannah and riverine areas. Al1 flics caught were
identified and recorded with reference to biotope, species, sex, teneral/non-teneral status,
and age group by wing-fray method as described by Jackson (1946). Al1 live non-teneral
flies were then dissected in a 0.9% saline solution and the midgut, labrum, hypopharynx
and the salivary glands were examined for the presence of trypanosomes by phase-
contrast microscopy at 320 x magnification using a combination of periplan
10 x eyepieces and a long-distance L32 objective.
2.4.2. Cattle herd monitoring
Each month, immediately following the tsetse trapping on the site, blood samples were
collected from the jugular vein of the cattle into evacuated tubes containing EDTA. The
PCV was measured and the level of parasitaemia estimated using phase-contrast
examination of the blood buffy-coat (Murray et cil., 1983). Whenever the PVC declined
238
A. Fall et al./Veterinary Parasitology 81 (1999) 235-247
below 20%, blood smears were made in order to determine if other haemoparasites (eg.,
Bab&a spp, Anuplasma spp.) were present. Faeces samples were collected from the
animal’s rectum for the entire herd every 3 months and monthly for animals aged O-3
years. Faecal samples were immediately examined for the presence of gastro-intestinal
parasites using the McMaster egg-counting technique (Murray et al., 1983). Animals
were weighed each month using an electronic scale (Barlo, Australia) and milk
offtake for human consumption was measured using a graduated tube. Information on
herd dynamics including the date of birth, mortality and animal transactions (e.g.,
purchases, sales, exchanges and transfers) were routinely collected during weekly herd
visits.
2.5. Data analysis
A regression analysis of the arcsine of trypanosome prevalence on log lO+l of the
challenge index (CI), the product of the apparent density and the infection rate of flics,
was performed to investigate the relationship between these two variables. SAS General
Linear Mode1 procedures (SAS Institute, 1989) were used to analyse health parameters
and production traits. Statistical models used for the analysis of variante of these
variables included the fïxed effects of village and herd within village, the month and year
the observation was made, age category (category 1: <1 year, category 2: l-3 years,
category 3: >3 years) and sex of the animal (female, entire male, castrated male).
For each trait analysed, specific additional factors were also included in the statistical
mode1 as necessary. For instance, analysis of PCV also included the trypanosome status of
the animal and the interaction between trypanosome and helminth infections. The data set
used to investigate the effects of these factors on PCV was formed by using data from
animals for which both faecal and blood samples were analysed for the determination of
blood and gastro-intestinal parasites. Also, the data set used to analyse PCV excluded data
from 49 animals which were infected with Babesia spp. or Anaplasma spp. and that had a
mean PCV of 19 (S.D. lO)%. Additional factors for the analysis of calving interval
included parity of the previous parturition and the trypanosome stams of the cow. Calving
number was classified into two groups, with group one formed by parturition number 1
and 2, and group two composed of cows with three or more calvings. Cows were also
grouped into non-infected and infected with trypanosomes after the first parturition of the
interval. Trypanosome status was also included in the analysis of calves LW growth up to
the age of 12 months. Two classes of infection status (non-infected and infected at least
once with trypanosomes), between the age of O-6 months and between 6-12 months,
were formed. For the analysis of lactation length, total and daily milk for human
consumption, the following classes of factors were included: three seasons of calving
(season 1, the wet season: June, July, August, season 2: the cool dry season, October,
November, and season 3, the hot dry season, February, March, April), two levels of
infection status (non-infected and infected at least once during lactation irrespective
.
of the time during lactation when the infection occurred), the interaction between
season and infection status, and two types of milk extraction practices (continuous
milk extraction throughout lactation, and suspension, and later resumption of milk
offtake).
A. Fall et al./Veterinary Parasitology 81 (1999) 235-247
239
Mean calving intervals and cow survival rate, calf mortality rate, calf live weight at 1
year, and milk offtake for human consumption,
were combined to determine productivity
indices as described by Agyemang et al. ( 199 1).
3. Results
3.1. Tsetse challenge
3
Tsetse flies present in the study area were identified as G.m. submorsitans and G.p.
gambiensis. Out of the 10210 flies caught from March 1988 to March 1992, 64% were
G.m. submorsitans and 36% were G.p. gambiensis. The number of flies caught per trap
per day is an estimate of the apparent density of tsetse flies and the average apparent
density found in this study was 5.4 flies/trap/day.
The number of G.p. gambiensis trapped
was highest during the rainy season (June-September) and during the first months of the
dry season (November-January) whereas most of catches of G.m. submorsitans occurred
during the second half of the dry season (February and May). The dissection of 50% of
the caught flies gave a mean monthly infection rate by T congolense or 7: vivax of 2.4
(s.e. 0.37)%. Mean monthly CI, an estimate of the trypanosomosis risk, was 17.3 (s.e.
4.18). Fig. 1 shows the seasonal pattem of changes in CI. Tsetse challenge was more
pronounced from Januar-April, peaked in March and decreased gradually as the dry season
progressed. Lowest CIs were recorded during the rainy season. There was a Sharp decrease in
tsetse apparent density and CI in 1991 and 1992 compared to 1988 and 1990 (Table 1).
3.2. Trypanosome infection rates in Ndama cattle
The overall mean trypanosome prevalence was 2.5 (s.e. 0.51)%. Infection rates due to
T. congolense and 7: vivax were 1.89 (se. 0.43) and 0.64 (s.e. 0.27)%, respectively.
4 5
5
40
4
3 5
0
0
J
F
M
A
M
J
J
A
S
O
N
D
Fig. 1. Monthly tsetse challenge index and cattle infection rates with T congonlensr and Z vivax.
240
A. Fall ut al. /Vetcrinay Parasitology 81 (1999) 235-247
Table 1
Number of flies caught, number of flics dissected, mean yearly number cif Glossr’nu rnov.sit~~~~ suhorsitar~s
and
Ghssina palpalis gmhiensi.s caught per trap per day, flies infection rates by Try~anosma
uqonl~wr and
hpmosor~~a
vivm, and tsetse challenge index (tsetse infectionxnumher of flies caupht per trap per day) at
Solda from March 1988 to March 1992
Number of months
Number of flies
F’TDZ’
FIR”
TCI’
Caught
Dissected-~
Year
1988
10
2528
1546
6.1
2.1
21.1
1989
12
3968
2120
8.4
1.7
18.2
1990
Il
2879
1121
6.4
4.8
33.7
1991
12
835
292
1.9
1 .o
0.9
r-<
1992
3
84
29
0.8
2.8
0.1
” FTD - Fly per trap per day
h FIR - Fly infection rates
’ TCI: tsetse challenge index
Trypanosome infection rates were significantly affected by village @<O.OOl), month of the
year Q~0.01) and age of the animal @<O.OOl). The monthly relative number of animals
infected with trypanosomes was larger in Yassiriba (4.3 s.e. 0.68%) than in Salamata ( 1.5 s.e.
0.54%) or Sare Pathe (1.7 s.e. 0.59%). Trypanosome infection rates increased steadily each
year from January, during the dry season, and peaked in June, the end of the dry season
(Fig. 1). Lowest infection rates were recorded in December and January. There was a time lag
of 3 months between peak of the trypanosome prevalence and that of the tsetse challenge.
When the log+ 1 of the monthly tsetse challenge was regressed on the arcsine of the mean
monthly infection rates aggregated over the 4-year period, significant relationship
(R2 = 0.52, p >O.Ol) was detected between these two factors. However this relationship
was no longer significant when the 48 monthly infection rates and monthly tsetse challenges
were used in the regression analysis. Adult animals aged more than 3 years were more
affected by trypanosomes (3.6 s.e. 0.5%) than younger animals (1.9 s.e. 0.5%). Castrated
males tended also to be less infected with trypanosomes than both entire males and females
(Table 2) but the difference
was not signifïcant (p = 0.16).
3.3. Gastro-intestinal parasites
Out of 6016 animal-month faecal samples analysed, 34.4 (s.e. 0.60), 2.1 (s.e. 0.18). 1.2
(se. 0.45) and 15.6 (se. 0.47)s were infested with strongyle, Strongyloides
spp.
Toxocara spp. and coccidia, respectively. The proportion of animals infested with
strongyle and mean egg output were lowest during the dry months of January-May.
The
frequency of faecal samples infested with Strongyloides
spp. increased gradually each
year from April to reach a peak in June and remained high (>40’%) in July, August and
September, the wettest months of the year. Mean strongyle EPG followed the same
pattern, but its peak occurred in September, 3 months later than when the proportion of
faecal sample infested with strongyle is highest. Mean strongyle egg counts were higher
in animals less than l-year-old (BPG - 346 s.e. 47) than in animals I-3 years old
(EPG = 286 s.e. 43), or in animals more than 3 years old (EPG = 220 s.e. 44). It has also
A. Full et al./Veterinary Parusitology 81 (1999) 2.5247
241
Table 2
Mean (+ s.e.m.) infection rate with T~ptrnosomu congonlensr and Trvpunosoma
vivat and mean ((i s.e.mj
packed ce11 volume (PCV %) in Ndama cattle kept under village management conditions at Kolda, Senegal,
between 1988 and 1992
Source of variation
Trypanosome infection rate (07)
Packed ce11 volume (%)
II
Mean f s.e.m
Significance
IZ
Meanfs.e.m
Signitïcance
Overall mean
9905
2.5 rt 0.51
5957
27.8 + 0.28
***
***
Village
Yassiriba
1005
4 . 3 i 0 . 7
749
28.3 0.32
Salamata
4 1 0 1
1.5 * 0 . 5
2787
27.4029
Saré Pathé
4799
1.7 f 0 . 6
2 4 2 1
27.5030
Year
***
***
1 9 8 8
2 5 9
1.4 + 1.2
210
30.6 zt 0.43
1 9 8 9
1 4 5 8
2 . 4 _t 0 . 6
1 0 1 3
29.2 i 0.30
1 9 9 0
1 1 3 7
3 . 2 + 0 . 7
792
26.3 3~ 0.32
1991
3396
3.1 f 0 . 5
2148
26.4 i 0.29
1 9 9 2
3 6 5 5
2 . 4 + 0 . 6
1 7 9 4
26.2 * 0.30
Sex
***
***
Female
6772
2 . 8 f 0 . 3
3582
27.6 zt 0.24
Entire male
2968
3 . 4 + 0 . 4
2279
26.4 IIC 0.25
Castrated male
165
1.3 i 0 . 3
9 6
29.3 + 0.52
AFcl year
1 5 8 6
1.9 * 0.7
***
1 3 1 0
27.9 f 0 . 3 0
* * *
l-3 year
3398
1.9 i 0.5
2745
2 7 . 5 z!c 0 . 2 9
Strongyle infestation
NS
Negative
4074
28.1 f 0 . 3 0
Positive
1 8 8 3
2 7 . 5 f 0.41
Tryp. ~Strongyltinfec-
* * *
tion
Negative negative
5 8 3 1
29.4 f 0 . 1 7
Negative positive
1 2 6
26.1 + 0 . 4 8
Positive negative
1 8 4 5
29.1 f 0 . 1 9
Positive positive
8 8
26.4 f 0.51
Positive positive
3 8
2 5 . 8 -i- 0 . 7 6
***p<o.o01.
NS - not significant.
been noted that Strongyloides spp. egg output was greater in animals infected (4.4 s.e
0.35%) than in animals not infected (1.9 se. 0.35%) with trypanosomes. Age of the
animal had a significant effect on the frequency of samples infested with Toxocaru spp.
and Strongyloides spp. Animals less than 1-year-old were more frequently infested with
Toxacaru spp. than older animals. While adult animals were free of Toxucaru spp. and
Strongyloides spp., the frequency of strongyle-type infestation was almost as high (34 se.
2.5%) as in Young animals (36% se. 2.7).
3.4. Packed ce11 volume
In general there was a trend of a decline of PCV from 1988 to 1992 (Table 2). Each
year, PCV reached its peak in February and the lowest values were recorded from May to
A. Fall et al./Veterinan, Parasitology 81 (1999) 235-247
3 0
ô
a-
2 9 s
P
E
2 8 $>=
0
2 6
J
F M A M J J A S 0 N D
Month
Fig. 2. Monthly packed ce11 volume (PCV, 7%) and trypanosome prevalence in village Ndama cattle between
1988 and 1992.
October, coinciding with the end of the dry season and the rainy season (Fig. 2). Highest
PCVs were recorded each year from November to February, with peak values reached in
February. Thereafter. there was a Sharp decrease of PCV values from February to May.
This period coincided with the time when food supply was critical and when significant
increases in trypanosome infection rates were seen. In general there was a decline in PCV
values of 3.3% in animals infected with trypanosomes. Castrated males had higher PCV
than entire males or females. The effect of strongyle infection was close to signifïcance
levels 0, = 0.08). In general strongyle-free animais had higher PCV than infected
animals. Although, the effect of the interaction between strongyle and trypanosome
infections was not significant, PCV values shown in Table 2 suggest an additive effect of
these infections on the development of anaemia.
3.5. Mortality rates
Out of the 225 calves bom during the course of the monitoring programme, 2.1 (se.
2.1), 5.2 (s.e. 2.8) and 12.2 (s.e. 3.3)% died before the age of 1, 6 and 12 months,
respectively.
3.6. Calving inter-vals
The unadjusted mean calving interval was 634 (s.d. 186) days. The least square mean
calving interval was 584 (s.e. 58) days. Cows whose calf died before the age of 12 months
had calving intervals shorter (by 167 days, ~~0.05) than that of cows whose offspring
survived beyond 12 months of age. The trypanosomosis status of cows did net affect
significantly calving intervals. When the previous calving number was 1 or 2, the calving
A. Fall et al./Veterinury
Parasitolqy 81 (1999) 235-247
243
interval was greater by 98 days than when the previous calving number was greater or
equal to 3. Mean calving intervals were 663 (se. 78) 493 (s.e. 73) and 445 (se. 65) days
for cows that had calved previously in 1988, 1989 and 1990, respectively.
3.7. Live weight changes
Live weight at birth, 6 and 12 months of age were 15.8 (s.e. 0.54), 48.1 (se. 2.56) and
71 .l (s.e. 5.44) kg, respectively. Only the season of calving had a significant effect on calf
weight at 6 months of age. Calves born during the late dry season (February-May) were
lighter at 6 months of age 0, < 0.05, 42.9 se. 3.48 kg) than those bom during the wet
season (50.5 se. 2.95 kg) or in the early dry season (50.7 s.e. 3.09 kg). Trypanosome
infection status did influence significantly calf LW at 6 or 12 months of age. The average
LW of empty cows was 222 (s.e. 1.3) kg. Cows lost LW during the second half of the dry
season, from March to June and they gained LW progressively during the wet season, but
it was until November, the early dry season, that they fully recovered their LW. The
difference
between the highest cow LW in November and the lowest LW in June was an
average of 25 kg.
3.8. Lactation characteristics
Mean lactation length, total milk extracted for human consumption
and daily milk
offtake were 389 (s.e. 16) days, 231 (s.e. 15) litres and 0.69 (se. 0.037) litres,
respectively. Lactation length was longer when calving occurred during the wet season
(season 1: June-September: 446 s.e. 18 days) than when calving took place during the
early dry season (season 2: October-January: 358 se. 23 days) or during the late dry
season (season 3: February-May: 365 s.e. 33 days). Cows for which milk offtake was
suspended had a longer lactation length (452 s.e. 18) days) than cows that were
continuously milked (327 s.e. 20 days. Cows that calved in season 1, the wet season, out-
produced (264 s.e. 17 1) cows that gave birth during the dry seasons 2 and 3 (188 (s.e. 22)
and 240 (s.e. 31)) litres, for seasons 2 and 3, respectively).
The interaction between season of calving and trypanosome infection on lactation
length was significant Q~0.05). Cows that gave birth in late dry season and that were
infected with trypanosomes during lactation had the shortest lactation length of 318 (se.
60) days. Trypanosome infection did not appear to affect lactation length when calving
occurred in the wet season or in the early dry season. Total and daily milk offtake
appeared also to be minimal in cows that calved in late dry season and that were infected
with trypanosomes during lactation, but these differences were not significant. When
calving occurred in early dry season and the cows were detected parasitaemic, total and
daily milk offtake were 166 (s.e. 36) and 0.560 (se. 0.09) litres, respectively. In contrast
cows that calved in the same period but that were not detected parasitaemic produced 210
(s.e. 18) litres during the entire lactation and 0.740 (s.e. 0.044) litres per day.
Trypanosome infections that occurred during the wet season or during the last part of the
dry season did not seem to affect milk offtake. Total milk offtake of non-infected and
infected cows that started lactation between February and June were 242 (se. 23) and 238
(se. 56) litres, respectively.
24‘l
A. Full et al./Veterinaty Parasitology RI (1999) 235-24Î
3.9. Productivity indices
Mean calving interval (584 days), cow survival rate (98.5% per year), calf survival rate
(88% per year), calf LW at one year of age (71.1 kg), and milk offtake during the first 12
months of lactation (216 kg) found in this study were combined to produce productivity
indices. Index 1 which is the amount of 1-year-old calf LW plus the LW equivalent of
milk extracted for human consumption
produced per cow per year was 62.8 kg. Index 2,
the LW of 1 -year-old calf produced plus LW equivalent of milk offtake per 100 kg of cow
maintained per year was 28.8 kg. Index 3, the LW of a I-year-old calf produced plus LW
equivalent of milk offtake per 100 kg of cow metabolic LW was 120.8 kg.
4. Discussion
In the present study, the population of tsetse flies decreased lover the experimental
period. The apparent density of tsetse flics was particularly low in 1991 and 1992 as
compared to the previous years. These changes in the population of flies may be
attributed to the effect of continuous trapping for 4 years in the same site. Another
contributing
factor to the decline of the tsetse population could have been the reduced
rainfall recorded during 199 1 and 1992 and also the occurrence of bush-fires which may
have destroyed their habitat or caused migration of a great deal of them. However. the
decline in the challenge index in 1991 and 1992 did not translate into reduced
trypanosome infection rates in cattle during these years. The regression of the monthly
trypanosome infection rates on the monthly challenge index after a log transformation of
tsetse challenge and arcsine transformation of trypanosome infection rates showed a
significant correlation between these two parameters. However, correlation was only
apparent when data was aggregated over the 4-year period and that challenge preceded
the prevalence data by three months. The correlation of these two parameters on a
monthly basis year by year failed to detect any signifïcant relationship between these two
factors. The absence of significant relationship was apparent even when the moving
average of the tsetse challenge was used in the regression analysis. There were many
months when the number of flics caught was zero in 199 I and 1992, but trypanosomes
were detected in the blood of the animals. This suggests that although the challenge index
is a simple field estimate of the seriousness of trypanosomosis in an area, it may fail to
give valid assessment of the problem if data is collected for a short period of time or if
there are many months when the challenge index is zero. Even when the index is zero it
does not mean that îlies are totally absent. Vectors other than Cm. suhmorsitans
and G.p.
gambiensis (e.g. mechanical transmitters) and reservoirs may also have played a role in
the transmission of trypanosomes to cattle.
The overall trypanosome prevalence (2.5%) found in the present study is relatively low.
Animals in Yassiriba were more frequently infected with trypanosomes than those in
Salamata and Sare Pathe. The herd size in Yassiriba was smaller than in other villages.
This, coupled with the fact that Yassiriba was located deeper in the forest and at the
vicinity of a stream may have created conditions for animals in Yassiriba to be more
exposed to tsetse flies than in other villages where these conditions did not occur. In the
present study there was an increase in the trypanosome prevalence as the animals aged.
The higher capacity of Young animals to resist trypanosomosis relative to adult animals
has already been reported (Stephen, 1986; Rowlands et al., 1993) and is suggested to be
related to the superior erythropoeitic response of younger animals (Murray, 1988).
However, as suggested by Rowlands et al. (1993), differences in exposure may contribute
to these variation in trypanosome prevalence in animals of different age classes. In this
study castrated males tended to be less subjected to trypanosome infection than entire
males and females. It would have been thought that being used for work, the physical
stress castrated males undergo during work would increase their susceptibility
to
infection. It is likely that both Young animals and castrated males are less infected than
other categories
of animals because of differences in their respective management. Not
only are draught animals better fed during the dry season but also both the Young and
draught animals graze in the vicinity of the homesteads and are not watered in gallery
forest where contact with flies is more likely. The time lag between peaks of tsetse
challenge and trypanosome prevalence in cattle found in this study is similar to that
reported in studies in Ethiopia (Rowlands et al., 1993) and Gambia (Claxton et al., 1992).
This is supposedly due to the time interval between the infective bite and the detection of
trypanosomes in the animals (Leak et al., 1993).
Although, this study showed a significant relationship between trypanosome
prevalence and tsetse challenge, the seasonal variations of trypanosome infection rates
suggests also that nutrition could be a confounding factor. Indeed, increases in
trypanosome prevalence during the dry season, from January to June. coincided with poor
nutrition during that period and the consequent reduction in animal LW and PCV%. Work
done in Gambia showed that nutritional stress depresses the capacity of the animals to
tope with trypanosome infection (Little et al., 1994).
The present study has also provided information on the epidemiology of gastro-
intestinal parasites in Ndama cattle in southern Senegal. Infestations with strongyle-type
parasites were more frequent and EPG values greater in the wet season than in the dry
season. In general, adult animals appeared as frequently infested with strongyle-type
parasites as younger animals and could therefore constitute a source of contamination of
pastures. Studies in Gambia revealed the same epidemiological characteristics of
gastrointestinal
nematodes in Ndama cattle (Kaufmann and Pfister, 1990).
This study has also shown that when calving occurred during the late dry season calves
had a slow growth rate up to 6 months of age. Growth of calves bom during this period
was impaired by low milk output of the dam due to poor nutrition.
Although, previous studies (Agyemang et al., 1993) have indicated the depressing
effect of trypanosome infection on reproductive performance, in the present study calving
interval was not affected by the trypanosome status of Ndama cows during lactation. This
finding is in agreement with that of Thorpe et al. (1988). The most important factor that
influenced
the reproductive performance in the work described here was whether the calf
survived or not up to 12 months of age. The calving interval of cows whose calves died
before the age of 12 months was lower by 167 days than that of cows that suckled their
offspring over 12 months. Indeed, the depressing effect of suckling on post-partum
cyclicity of Ndama cows is reported by Sanyang et al. (1995). As pointed out by Thorpe
et al. (1988), use of calving interval as an estimate of reproductive performance fail to
246
A. Fall et al./Vetrrina~ Purasitology 81 (1999) 235-247
take into account non-fertile cows in the herd and this may mask the effect of
trypanosome infection on reproductive performance.
The mean lactation length (389 se. 16 days) and total milk for human consumption
(23 1 s.e. 15 litres) found in this study carried out in southern Senegal where milking is
done once a day agrees with the level of lactation performance by Ndama cows milked
once daily in Gambia. Lactation length and milk offtake were 437 (s.e. 16.6) days and
239 (s.e. 19.3) litres in the once-daily milking system in Gambia (Agyemang et al., 1991).
Trypanosome infection did not affect lactation length or total milk offtake. This again
agrees with the results obtained in Gambia where non-infected cows out-produced
infected cows during lactation by only 24 kg during a l4-month location period and this
difference was not significant (Agyemang et al., 1991). However, trypanosome infection
caused a reduction in milk production during the 6 months following infection in Ndama
cows in Gambia (Agyemang et al., 1990). Larger lactation length and greater milk offtake
seen in cows starting lactation during the wet season when food was plentiful and of good
quality as compared to the dry season, suggest that nutrition is the driving factor that
determines milk production of the village Ndama CO~S. Cows calving during the last part
of the dry season performed better than those calving during the early part of the dry
season. For the latter, most of the lactation length occurred during dry months whereas
the former Will benefit from the pastures improvement in the next lwet season. In terms of
milk production, cows that gave birth between November and January were more
severely affected by food shortage than cows calving in other seasons. Feed restriction
was compounded in these cows by trypanosome infections and led to the shortest
lactation length. The trends observed regarding the interaction of season of calving and
trypanosome infection on milk offtake suggest that well fed Ndama cows could produce
milk with a no major negative influence of trypanosome infection. Similarly, Agyemang
et al. (1990) suggested that the depressive effect of trypanosome infections on milk
production could be reduced through the provision of additional food to cattle showing
signs of the disease.
Finally, the productivity
indices found in this study (Index 1 = 62.8 kg per cow, Index
2 = 28.3 kg per 100 kg cow LW and index 3 = 120.8 kg per 100 kg metabolic LW) are in
agreement with productivity
indices found in Ndama cattle under once-daily milking
system in Gambia where index 1,2 and 3 averaged 60.4,28.3 and 120.2 kg (Agyemang et
a]., 1991). Village Ndama cow productivity
seems relatively lower than that found in
Ndama cows reared on station with no milk extraction. Productivity indices 1, 2 and 3
were 70.1,29.1 and 127.0, respectively for Ndama cows reared on station in Senegal (Fall
et al., 1983).
Acknowledgements
This work was jointly carried out by ISRA, ILCA and ILRAD and was supported by
the European Development Fund. Additional fund provided by the British Overseas
Development Administration (ODA) allowed the main author to spend time at the Centre
for Tropical Veterinary Medicine, University of Edinburgh to analyse and publish the
data. Comments from A.S. Peregrine, S. Diaw and G. Vassiliades are greatly appreciated.
A. Fall et al. / Vetcrinu- Pauusitolo,yy
81 (1999) 235-247
247
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An International Scientific Journal
Veterinary Parasitology 81 (1999) 235-247
Tsetse challenge, trypanosome and helminth
infection in relation to productivity of
village Ndama cattle in Senegal
A. FallaqbT*, A. Diack”, A. Dis”,
, G.D.M. d’Ieterend
“Institut S&&alais de Recherches Agricoles, CR.U Kolda, BP 52, Kolda, Senegal
hCentre for Tropical Veterinary Medicine, Easter Bush Roslin, Midlothian, EH25 9RG, UK
‘Institut Sénégalais de Recherches Agricoles, LNERI! BP 2057, DakaG Senegal
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Received 13 January 1998; accepted 24 July 1998
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veterinaty
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ELSEVIER
Veterinary Parasitology 81 (1999) 235-247
Tsetse challenge, trypanosome and helminth
infection in relation to productivity of
village Ndama cattle in Senegal
A. FallapbT*, A. Diack”, A. Diaité”, M. Seye”, G.D.M. d’Ieterend
“institut Sénégalais de Recherches Agricoles, CRz/ Kolda, BP 52, Kolda, Senegal
“Centre,for Tropical Veterinary Medicine, Easter Bush Roslin. Midlothiun. EH25 9RG, UK
‘Institut Sénégalais de Recherches Agricoles. LNERI! BP 2057, Dakar Scnegal
dlnternational Livestock Research Institute, J?O. Box 30 709, Nairobi. Kenya
Received 13 January 1998; accepted 24 July 1998
-..-~.- ~---.
Abstract
Data on tsetse fly, and on village Ndama cattle collected over a 4-year period in southern
Senegal, were analysed. A total of 431 Ndama cattle in four herds of three villages in the Upper
Casamance area of southern Senegal were monitored monthly. Glossina morsituns suhmorsitans
and Glossina palpalis gumbiensis are present in the study area. Mean tsetse apparent density was
5.4 fliesltraplday. Trypanosome (Trypanosoma congonlense and Trypanosoma vivux) infection rate
in flies was 2.4 (s.e. 0.37)%. Tsetse challenge index was 17.3 (s.e. 4.18). Mean monthly
trypanosome prevalence in cattle was 2.5 (s.e. OSl)%. Highest trypanosome prevalence occurred
during the dry season, and animals less than 1-year old were more frequently infected than older
animals. The linear relationship between the loglO+l tsetse challenge and the arcsine of the
trypanosome prevalence was significant only when mean monthly values of these variables over the
4-year period were used with tsetse challenge preceding infection rate by 3 months. Mean monthly
prevalence of strongyle, Strongyloides Spp. , Toxocara spp. and coccidia were 34.4 (s.e. 0.60), 2.1
(s.e. 0.18), 1.2 (s.e. 0.45) and 15.6 (s.e. 0.47)%, respectively. Calf mortality rate at 1, 6 and 12
months of age was 2.1 (s.e. 2.1), 5.2 (s.e. 2.8) and 12.2 (s.e. 3.3)%, respectively. Calving interval
(584 s.e. 58 days) was not influenced by trypanosome status of the cow during lactation. Calving
interval was shorter by 167 days when the calf died before 1 year of age in comparison to calving
intervals for which the calf survived beyond one year. Live weight at birth, 6 and 12 months of age
were 15.8 (s.e. 0.54). 48.1 (s.e. 2.56) and 71.1 (s.e. 5.44) kg, respectively. Mean lactation length,
total and daily milk offtake were 389 (s.e. 16) days, 231 (s.e. 15) litres and 0.69 (s.e. 0.037) litres,
respectively. Trypanosome infection during lactation did not have a significant effect on the amount
* Corresponding author. Tel.: +l-231-3823-678; fax: +1-221-8322-l 18: e-mail: abdoufal@isra.refer.sn
0304.4017/99/$ - see front matter !: 1999 Elsevier Science B.V. Al1 rights reserved.
PII: SO304-4017(98)00213-l
236
A. Fall et ul. /Vetruinary Parusitology 81 (1999) 23.5-247
of milk extracted for human consumption nor did trypanosome status affect calf growth. $7 1999
Elsevier Science B.V. Al1 rights reserved.
Kqvword.~ Tsetse challenge; Trypanosomosis: Helminthiosis; Ndama cattle; Prodnctivity
1. Introduction
Because of their trypanotolerance, Ndama cattle constitute a unique animal genetic
resource which forms the basis of large ruminant agriculture in many parts of West Africa
where the risk of trypanosomosis is high. The Ndama cattle breed are a multipurpose
breed that produce milk. meat, power and manure and therefore contribute a great deal to
the income and welfare of millions of farmers in mixed trop-livestock production
systems in West Africa. However, a complex set of technical factors related to health,
nutrition and management constrain the productivity of Ndama cattle kept under
traditional husbandry systems. The relative importance of these factors needs to be
determined if strategies to make better use of this genetic resource are to be developed to
meet the growing demand for animal products in West Africa. TO this end, an
epidemiological study was carried out from 1988 to 1992 in the Upper Casamance region
of southern Senegal to investigate causes of variation of Ndama cattle productivity and
the stability of the trypanotolerance trait under village management systems. This study
was part of a large epidemiological programme that was conducted by International
Livestock Centre for Africa (ILCA now ILRI) and National ,4gricultural Research
Institutes in many sites in Africa with different degrees of trypanosomosis risk. This
paper reports findings on the tsetse challenge, prevalence of parasitic diseases
(helminthiosis, trypanosomosis) in village Ndama cattle in southern Senegal and how
these factors affect the reproduction performance, calf growth and milk production.
2. Materials and methods
2.1. The study area
The study was carried out in the region of Upper Casamance in Southern Senegal. The
climate in this region is of a sudano-guinean type. Annual rainfall was 1018. 1045, 787.
and 684 mm in 1988, 1989, 1990 and 1991, respectively. The unimodal rainfall in this
area occurs between June and October. Four herds in these villages (Salamata, Yassiriba,
Sare Pathe) were selected for the investigation Ndama cattle health characteristics and
production parameters over a 4-year period (1988-1992). Salamata and Yassiriba are
along the Mahon forest boundaries and close to a stream. Sare Pathe is located in the
forest of Bakor. The criteria used to Select villages were the presence of tsetse flies (but
the infection rates were not taken into account), accessibility (particularly during the
rainy season when roads becomc impractical), and farmcrs willingness to participate to
the monitoring program.
A. Fol1 et ul. /Veterinary Pcrrmitology 81 (1999) 235-247
237
2.2. Herd management
Animals graze natural pastures which form the main source of the food supply.
Animals have access to millet, rice and sorghum residues that are consumed directly in
the fields from November. Shortage of food supply during the hot dry season (March,
April, May and June) is the single most important constraint that faces the herd owners in
this area. Animals are tethered individually overnight in trop fields during the dry season
and are moved lo the forest during the cropping season to avoid damage to crops. Mating
is not controlled and calving occurs a11 year round. However, peak calving is recorded in
July and August. Milking is performed once a day, and begins one week after calving.
The calf is allowed to suckle its dam for a few seconds to trigger milk let-down and
thereafter, is tethered at the foot of the dam during the course of milking. A main feature
of the milking system in the study area is that milking for human consumption is
suspended during part of the dry season and is resumed during the next wet season.
2.3. Experimental
design
2.3.1. Animals
A total of 431 Ndama cattle kept in four herds of three villages were monitored
monthly for 52 months in Salamata and Yassiriba with 163 animais, and for 24 months in
Sare Pathe with 268 animals. Animals were individually tagged on both ears. Animals
were managed under traditional village conditions and therefore were subjected to natural
tsetse challenge. Routine vaccination against rinderpest, anthrax, hemorrhagic septicae-
mia, and contagious bovine pleuropneumonia was given. Animals were also treated with
diminazene aceturate (Berenil ” , 3.5 mg kg- ’ body weight) when trypanosomes were
detected and the packed red ce11 volume (PCV) was below 20%.
2.4. Field recording and lahoratoy determinations
2.4.1. Monitorirzg of tsetse f7ie.F
Twelve biconical traps, as described by Challier and Laveissière ( 1973), were placed at
each site each month for three consecutive days and harvested every 24 h. Traps we’re set
100 m apart from each other, in Savannah and riverine areas. Al1 flics caught were
identified and recorded with reference to biotope, species, sex, teneral/non-teneral status,
and age group by wing-fray method as described by Jackson (1946). Al1 live non-teneral
flies were then dissected in a 0.9% saline solution and the midgut, labrum, hypopharynx
and the salivary glands were examined for the presence of trypanosomes by phase-
contrast microscopy at 320 x magnification using a combination of periplan
10 x eyepieces and a long-distance L32 objective.
2.4.2. Cattle herd monitoring
Each month, immediately following the tsetse trapping on the site, blood samples were
collected from the jugular vein of the cattle into evacuated tubes containing EDTA. The
PCV was measured and the level of parasitaemia estimated using phase-contrast
examination of the blood buffy-coat (Murray et cil., 1983). Whenever the PVC declined
238
A. Fall et al./Veterinary Parasitology 81 (1999) 235-247
below 20%, blood smears were made in order to determine if other haemoparasites (eg.,
Bab&a spp, Anuplasma spp.) were present. Faeces samples were collected from the
animal’s rectum for the entire herd every 3 months and monthly for animals aged O-3
years. Faecal samples were immediately examined for the presence of gastro-intestinal
parasites using the McMaster egg-counting technique (Murray et al., 1983). Animals
were weighed each month using an electronic scale (Barlo, Australia) and milk
offtake for human consumption was measured using a graduated tube. Information on
herd dynamics including the date of birth, mortality and animal transactions (e.g.,
purchases, sales, exchanges and transfers) were routinely collected during weekly herd
visits.
2.5. Data analysis
A regression analysis of the arcsine of trypanosome prevalence on log lO+l of the
challenge index (CI), the product of the apparent density and the infection rate of flics,
was performed to investigate the relationship between these two variables. SAS General
Linear Mode1 procedures (SAS Institute, 1989) were used to analyse health parameters
and production traits. Statistical models used for the analysis of variante of these
variables included the fïxed effects of village and herd within village, the month and year
the observation was made, age category (category 1: <1 year, category 2: l-3 years,
category 3: >3 years) and sex of the animal (female, entire male, castrated male).
For each trait analysed, specific additional factors were also included in the statistical
mode1 as necessary. For instance, analysis of PCV also included the trypanosome status of
the animal and the interaction between trypanosome and helminth infections. The data set
used to investigate the effects of these factors on PCV was formed by using data from
animals for which both faecal and blood samples were analysed for the determination of
blood and gastro-intestinal parasites. Also, the data set used to analyse PCV excluded data
from 49 animals which were infected with Babesia spp. or Anaplasma spp. and that had a
mean PCV of 19 (S.D. lO)%. Additional factors for the analysis of calving interval
included parity of the previous parturition and the trypanosome stams of the cow. Calving
number was classified into two groups, with group one formed by parturition number 1
and 2, and group two composed of cows with three or more calvings. Cows were also
grouped into non-infected and infected with trypanosomes after the first parturition of the
interval. Trypanosome status was also included in the analysis of calves LW growth up to
the age of 12 months. Two classes of infection status (non-infected and infected at least
once with trypanosomes), between the age of O-6 months and between 6-12 months,
were formed. For the analysis of lactation length, total and daily milk for human
consumption, the following classes of factors were included: three seasons of calving
(season 1, the wet season: June, July, August, season 2: the cool dry season, October,
November, and season 3, the hot dry season, February, March, April), two levels of
infection status (non-infected and infected at least once during lactation irrespective
.
of the time during lactation when the infection occurred), the interaction between
season and infection status, and two types of milk extraction practices (continuous
milk extraction throughout lactation, and suspension, and later resumption of milk
offtake).
A. Fall et al./Veterinary Parasitology 81 (1999) 235-247
239
Mean calving intervals and cow survival rate, calf mortality rate, calf live weight at 1
year, and milk offtake for human consumption,
were combined to determine productivity
indices as described by Agyemang et al. ( 199 1).
3. Results
3.1. Tsetse challenge
3
Tsetse flies present in the study area were identified as G.m. submorsitans and G.p.
gambiensis. Out of the 10210 flies caught from March 1988 to March 1992, 64% were
G.m. submorsitans and 36% were G.p. gambiensis. The number of flies caught per trap
per day is an estimate of the apparent density of tsetse flies and the average apparent
density found in this study was 5.4 flies/trap/day.
The number of G.p. gambiensis trapped
was highest during the rainy season (June-September) and during the first months of the
dry season (November-January) whereas most of catches of G.m. submorsitans occurred
during the second half of the dry season (February and May). The dissection of 50% of
the caught flies gave a mean monthly infection rate by T congolense or 7: vivax of 2.4
(s.e. 0.37)%. Mean monthly CI, an estimate of the trypanosomosis risk, was 17.3 (s.e.
4.18). Fig. 1 shows the seasonal pattem of changes in CI. Tsetse challenge was more
pronounced from Januar-April, peaked in March and decreased gradually as the dry season
progressed. Lowest CIs were recorded during the rainy season. There was a Sharp decrease in
tsetse apparent density and CI in 1991 and 1992 compared to 1988 and 1990 (Table 1).
3.2. Trypanosome infection rates in Ndama cattle
The overall mean trypanosome prevalence was 2.5 (s.e. 0.51)%. Infection rates due to
T. congolense and 7: vivax were 1.89 (se. 0.43) and 0.64 (s.e. 0.27)%, respectively.
4 5
5
40
4
3 5
0
0
J
F
M
A
M
J
J
A
S
O
N
D
Fig. 1. Monthly tsetse challenge index and cattle infection rates with T congonlensr and Z vivax.
240
A. Fall ut al. /Vetcrinay Parasitology 81 (1999) 235-247
Table 1
Number of flies caught, number of flics dissected, mean yearly number cif Glossr’nu rnov.sit~~~~ suhorsitar~s
and
Ghssina palpalis gmhiensi.s caught per trap per day, flies infection rates by Try~anosma
uqonl~wr and
hpmosor~~a
vivm, and tsetse challenge index (tsetse infectionxnumher of flies caupht per trap per day) at
Solda from March 1988 to March 1992
Number of months
Number of flies
F’TDZ’
FIR”
TCI’
Caught
Dissected-~
Year
1988
10
2528
1546
6.1
2.1
21.1
1989
12
3968
2120
8.4
1.7
18.2
1990
Il
2879
1121
6.4
4.8
33.7
1991
12
835
292
1.9
1 .o
0.9
r-<
1992
3
84
29
0.8
2.8
0.1
” FTD - Fly per trap per day
h FIR - Fly infection rates
’ TCI: tsetse challenge index
Trypanosome infection rates were significantly affected by village @<O.OOl), month of the
year Q~0.01) and age of the animal @<O.OOl). The monthly relative number of animals
infected with trypanosomes was larger in Yassiriba (4.3 s.e. 0.68%) than in Salamata ( 1.5 s.e.
0.54%) or Sare Pathe (1.7 s.e. 0.59%). Trypanosome infection rates increased steadily each
year from January, during the dry season, and peaked in June, the end of the dry season
(Fig. 1). Lowest infection rates were recorded in December and January. There was a time lag
of 3 months between peak of the trypanosome prevalence and that of the tsetse challenge.
When the log+ 1 of the monthly tsetse challenge was regressed on the arcsine of the mean
monthly infection rates aggregated over the 4-year period, significant relationship
(R2 = 0.52, p >O.Ol) was detected between these two factors. However this relationship
was no longer significant when the 48 monthly infection rates and monthly tsetse challenges
were used in the regression analysis. Adult animals aged more than 3 years were more
affected by trypanosomes (3.6 s.e. 0.5%) than younger animals (1.9 s.e. 0.5%). Castrated
males tended also to be less infected with trypanosomes than both entire males and females
(Table 2) but the difference
was not signifïcant (p = 0.16).
3.3. Gastro-intestinal parasites
Out of 6016 animal-month faecal samples analysed, 34.4 (s.e. 0.60), 2.1 (s.e. 0.18). 1.2
(se. 0.45) and 15.6 (se. 0.47)s were infested with strongyle, Strongyloides
spp.
Toxocara spp. and coccidia, respectively. The proportion of animals infested with
strongyle and mean egg output were lowest during the dry months of January-May.
The
frequency of faecal samples infested with Strongyloides
spp. increased gradually each
year from April to reach a peak in June and remained high (>40’%) in July, August and
September, the wettest months of the year. Mean strongyle EPG followed the same
pattern, but its peak occurred in September, 3 months later than when the proportion of
faecal sample infested with strongyle is highest. Mean strongyle egg counts were higher
in animals less than l-year-old (BPG - 346 s.e. 47) than in animals I-3 years old
(EPG = 286 s.e. 43), or in animals more than 3 years old (EPG = 220 s.e. 44). It has also
A. Full et al./Veterinary Parusitology 81 (1999) 2.5247
241
Table 2
Mean (+ s.e.m.) infection rate with T~ptrnosomu congonlensr and Trvpunosoma
vivat and mean ((i s.e.mj
packed ce11 volume (PCV %) in Ndama cattle kept under village management conditions at Kolda, Senegal,
between 1988 and 1992
Source of variation
Trypanosome infection rate (07)
Packed ce11 volume (%)
II
Mean f s.e.m
Significance
IZ
Meanfs.e.m
Signitïcance
Overall mean
9905
2.5 rt 0.51
5957
27.8 + 0.28
***
***
Village
Yassiriba
1005
4 . 3 i 0 . 7
749
28.3 0.32
Salamata
4 1 0 1
1.5 * 0 . 5
2787
27.4029
Saré Pathé
4799
1.7 f 0 . 6
2 4 2 1
27.5030
Year
***
***
1 9 8 8
2 5 9
1.4 + 1.2
210
30.6 zt 0.43
1 9 8 9
1 4 5 8
2 . 4 _t 0 . 6
1 0 1 3
29.2 i 0.30
1 9 9 0
1 1 3 7
3 . 2 + 0 . 7
792
26.3 3~ 0.32
1991
3396
3.1 f 0 . 5
2148
26.4 i 0.29
1 9 9 2
3 6 5 5
2 . 4 + 0 . 6
1 7 9 4
26.2 * 0.30
Sex
***
***
Female
6772
2 . 8 f 0 . 3
3582
27.6 zt 0.24
Entire male
2968
3 . 4 + 0 . 4
2279
26.4 IIC 0.25
Castrated male
165
1.3 i 0 . 3
9 6
29.3 + 0.52
AFcl year
1 5 8 6
1.9 * 0.7
***
1 3 1 0
27.9 f 0 . 3 0
* * *
l-3 year
3398
1.9 i 0.5
2745
2 7 . 5 z!c 0 . 2 9
Strongyle infestation
NS
Negative
4074
28.1 f 0 . 3 0
Positive
1 8 8 3
2 7 . 5 f 0.41
Tryp. ~Strongyltinfec-
* * *
tion
Negative negative
5 8 3 1
29.4 f 0 . 1 7
Negative positive
1 2 6
26.1 + 0 . 4 8
Positive negative
1 8 4 5
29.1 f 0 . 1 9
Positive positive
8 8
26.4 f 0.51
Positive positive
3 8
2 5 . 8 -i- 0 . 7 6
***p<o.o01.
NS - not significant.
been noted that Strongyloides spp. egg output was greater in animals infected (4.4 s.e
0.35%) than in animals not infected (1.9 se. 0.35%) with trypanosomes. Age of the
animal had a significant effect on the frequency of samples infested with Toxocaru spp.
and Strongyloides spp. Animals less than 1-year-old were more frequently infested with
Toxacaru spp. than older animals. While adult animals were free of Toxucaru spp. and
Strongyloides spp., the frequency of strongyle-type infestation was almost as high (34 se.
2.5%) as in Young animals (36% se. 2.7).
3.4. Packed ce11 volume
In general there was a trend of a decline of PCV from 1988 to 1992 (Table 2). Each
year, PCV reached its peak in February and the lowest values were recorded from May to
A. Fall et al./Veterinan, Parasitology 81 (1999) 235-247
3 0
ô
a-
2 9 s
P
E
2 8 $>=
0
2 6
J
F M A M J J A S 0 N D
Month
Fig. 2. Monthly packed ce11 volume (PCV, 7%) and trypanosome prevalence in village Ndama cattle between
1988 and 1992.
October, coinciding with the end of the dry season and the rainy season (Fig. 2). Highest
PCVs were recorded each year from November to February, with peak values reached in
February. Thereafter. there was a Sharp decrease of PCV values from February to May.
This period coincided with the time when food supply was critical and when significant
increases in trypanosome infection rates were seen. In general there was a decline in PCV
values of 3.3% in animals infected with trypanosomes. Castrated males had higher PCV
than entire males or females. The effect of strongyle infection was close to signifïcance
levels 0, = 0.08). In general strongyle-free animais had higher PCV than infected
animals. Although, the effect of the interaction between strongyle and trypanosome
infections was not significant, PCV values shown in Table 2 suggest an additive effect of
these infections on the development of anaemia.
3.5. Mortality rates
Out of the 225 calves bom during the course of the monitoring programme, 2.1 (se.
2.1), 5.2 (s.e. 2.8) and 12.2 (s.e. 3.3)% died before the age of 1, 6 and 12 months,
respectively.
3.6. Calving inter-vals
The unadjusted mean calving interval was 634 (s.d. 186) days. The least square mean
calving interval was 584 (s.e. 58) days. Cows whose calf died before the age of 12 months
had calving intervals shorter (by 167 days, ~~0.05) than that of cows whose offspring
survived beyond 12 months of age. The trypanosomosis status of cows did net affect
significantly calving intervals. When the previous calving number was 1 or 2, the calving
A. Fall et al./Veterinury
Parasitolqy 81 (1999) 235-247
243
interval was greater by 98 days than when the previous calving number was greater or
equal to 3. Mean calving intervals were 663 (se. 78) 493 (s.e. 73) and 445 (se. 65) days
for cows that had calved previously in 1988, 1989 and 1990, respectively.
3.7. Live weight changes
Live weight at birth, 6 and 12 months of age were 15.8 (s.e. 0.54), 48.1 (se. 2.56) and
71 .l (s.e. 5.44) kg, respectively. Only the season of calving had a significant effect on calf
weight at 6 months of age. Calves born during the late dry season (February-May) were
lighter at 6 months of age 0, < 0.05, 42.9 se. 3.48 kg) than those bom during the wet
season (50.5 se. 2.95 kg) or in the early dry season (50.7 s.e. 3.09 kg). Trypanosome
infection status did influence significantly calf LW at 6 or 12 months of age. The average
LW of empty cows was 222 (s.e. 1.3) kg. Cows lost LW during the second half of the dry
season, from March to June and they gained LW progressively during the wet season, but
it was until November, the early dry season, that they fully recovered their LW. The
difference
between the highest cow LW in November and the lowest LW in June was an
average of 25 kg.
3.8. Lactation characteristics
Mean lactation length, total milk extracted for human consumption
and daily milk
offtake were 389 (s.e. 16) days, 231 (s.e. 15) litres and 0.69 (se. 0.037) litres,
respectively. Lactation length was longer when calving occurred during the wet season
(season 1: June-September: 446 s.e. 18 days) than when calving took place during the
early dry season (season 2: October-January: 358 se. 23 days) or during the late dry
season (season 3: February-May: 365 s.e. 33 days). Cows for which milk offtake was
suspended had a longer lactation length (452 s.e. 18) days) than cows that were
continuously milked (327 s.e. 20 days. Cows that calved in season 1, the wet season, out-
produced (264 s.e. 17 1) cows that gave birth during the dry seasons 2 and 3 (188 (s.e. 22)
and 240 (s.e. 31)) litres, for seasons 2 and 3, respectively).
The interaction between season of calving and trypanosome infection on lactation
length was significant Q~0.05). Cows that gave birth in late dry season and that were
infected with trypanosomes during lactation had the shortest lactation length of 318 (se.
60) days. Trypanosome infection did not appear to affect lactation length when calving
occurred in the wet season or in the early dry season. Total and daily milk offtake
appeared also to be minimal in cows that calved in late dry season and that were infected
with trypanosomes during lactation, but these differences were not significant. When
calving occurred in early dry season and the cows were detected parasitaemic, total and
daily milk offtake were 166 (s.e. 36) and 0.560 (se. 0.09) litres, respectively. In contrast
cows that calved in the same period but that were not detected parasitaemic produced 210
(s.e. 18) litres during the entire lactation and 0.740 (s.e. 0.044) litres per day.
Trypanosome infections that occurred during the wet season or during the last part of the
dry season did not seem to affect milk offtake. Total milk offtake of non-infected and
infected cows that started lactation between February and June were 242 (se. 23) and 238
(se. 56) litres, respectively.
24‘l
A. Full et al./Veterinaty Parasitology RI (1999) 235-24Î
3.9. Productivity indices
Mean calving interval (584 days), cow survival rate (98.5% per year), calf survival rate
(88% per year), calf LW at one year of age (71.1 kg), and milk offtake during the first 12
months of lactation (216 kg) found in this study were combined to produce productivity
indices. Index 1 which is the amount of 1-year-old calf LW plus the LW equivalent of
milk extracted for human consumption
produced per cow per year was 62.8 kg. Index 2,
the LW of 1 -year-old calf produced plus LW equivalent of milk offtake per 100 kg of cow
maintained per year was 28.8 kg. Index 3, the LW of a I-year-old calf produced plus LW
equivalent of milk offtake per 100 kg of cow metabolic LW was 120.8 kg.
4. Discussion
In the present study, the population of tsetse flies decreased lover the experimental
period. The apparent density of tsetse flics was particularly low in 1991 and 1992 as
compared to the previous years. These changes in the population of flies may be
attributed to the effect of continuous trapping for 4 years in the same site. Another
contributing
factor to the decline of the tsetse population could have been the reduced
rainfall recorded during 199 1 and 1992 and also the occurrence of bush-fires which may
have destroyed their habitat or caused migration of a great deal of them. However. the
decline in the challenge index in 1991 and 1992 did not translate into reduced
trypanosome infection rates in cattle during these years. The regression of the monthly
trypanosome infection rates on the monthly challenge index after a log transformation of
tsetse challenge and arcsine transformation of trypanosome infection rates showed a
significant correlation between these two parameters. However, correlation was only
apparent when data was aggregated over the 4-year period and that challenge preceded
the prevalence data by three months. The correlation of these two parameters on a
monthly basis year by year failed to detect any signifïcant relationship between these two
factors. The absence of significant relationship was apparent even when the moving
average of the tsetse challenge was used in the regression analysis. There were many
months when the number of flics caught was zero in 199 I and 1992, but trypanosomes
were detected in the blood of the animals. This suggests that although the challenge index
is a simple field estimate of the seriousness of trypanosomosis in an area, it may fail to
give valid assessment of the problem if data is collected for a short period of time or if
there are many months when the challenge index is zero. Even when the index is zero it
does not mean that îlies are totally absent. Vectors other than Cm. suhmorsitans
and G.p.
gambiensis (e.g. mechanical transmitters) and reservoirs may also have played a role in
the transmission of trypanosomes to cattle.
The overall trypanosome prevalence (2.5%) found in the present study is relatively low.
Animals in Yassiriba were more frequently infected with trypanosomes than those in
Salamata and Sare Pathe. The herd size in Yassiriba was smaller than in other villages.
This, coupled with the fact that Yassiriba was located deeper in the forest and at the
vicinity of a stream may have created conditions for animals in Yassiriba to be more
exposed to tsetse flies than in other villages where these conditions did not occur. In the
present study there was an increase in the trypanosome prevalence as the animals aged.
The higher capacity of Young animals to resist trypanosomosis relative to adult animals
has already been reported (Stephen, 1986; Rowlands et al., 1993) and is suggested to be
related to the superior erythropoeitic response of younger animals (Murray, 1988).
However, as suggested by Rowlands et al. (1993), differences in exposure may contribute
to these variation in trypanosome prevalence in animals of different age classes. In this
study castrated males tended to be less subjected to trypanosome infection than entire
males and females. It would have been thought that being used for work, the physical
stress castrated males undergo during work would increase their susceptibility
to
infection. It is likely that both Young animals and castrated males are less infected than
other categories
of animals because of differences in their respective management. Not
only are draught animals better fed during the dry season but also both the Young and
draught animals graze in the vicinity of the homesteads and are not watered in gallery
forest where contact with flies is more likely. The time lag between peaks of tsetse
challenge and trypanosome prevalence in cattle found in this study is similar to that
reported in studies in Ethiopia (Rowlands et al., 1993) and Gambia (Claxton et al., 1992).
This is supposedly due to the time interval between the infective bite and the detection of
trypanosomes in the animals (Leak et al., 1993).
Although, this study showed a significant relationship between trypanosome
prevalence and tsetse challenge, the seasonal variations of trypanosome infection rates
suggests also that nutrition could be a confounding factor. Indeed, increases in
trypanosome prevalence during the dry season, from January to June. coincided with poor
nutrition during that period and the consequent reduction in animal LW and PCV%. Work
done in Gambia showed that nutritional stress depresses the capacity of the animals to
tope with trypanosome infection (Little et al., 1994).
The present study has also provided information on the epidemiology of gastro-
intestinal parasites in Ndama cattle in southern Senegal. Infestations with strongyle-type
parasites were more frequent and EPG values greater in the wet season than in the dry
season. In general, adult animals appeared as frequently infested with strongyle-type
parasites as younger animals and could therefore constitute a source of contamination of
pastures. Studies in Gambia revealed the same epidemiological characteristics of
gastrointestinal
nematodes in Ndama cattle (Kaufmann and Pfister, 1990).
This study has also shown that when calving occurred during the late dry season calves
had a slow growth rate up to 6 months of age. Growth of calves bom during this period
was impaired by low milk output of the dam due to poor nutrition.
Although, previous studies (Agyemang et al., 1993) have indicated the depressing
effect of trypanosome infection on reproductive performance, in the present study calving
interval was not affected by the trypanosome status of Ndama cows during lactation. This
finding is in agreement with that of Thorpe et al. (1988). The most important factor that
influenced
the reproductive performance in the work described here was whether the calf
survived or not up to 12 months of age. The calving interval of cows whose calves died
before the age of 12 months was lower by 167 days than that of cows that suckled their
offspring over 12 months. Indeed, the depressing effect of suckling on post-partum
cyclicity of Ndama cows is reported by Sanyang et al. (1995). As pointed out by Thorpe
et al. (1988), use of calving interval as an estimate of reproductive performance fail to
246
A. Fall et al./Vetrrina~ Purasitology 81 (1999) 235-247
take into account non-fertile cows in the herd and this may mask the effect of
trypanosome infection on reproductive performance.
The mean lactation length (389 se. 16 days) and total milk for human consumption
(23 1 s.e. 15 litres) found in this study carried out in southern Senegal where milking is
done once a day agrees with the level of lactation performance by Ndama cows milked
once daily in Gambia. Lactation length and milk offtake were 437 (s.e. 16.6) days and
239 (s.e. 19.3) litres in the once-daily milking system in Gambia (Agyemang et al., 1991).
Trypanosome infection did not affect lactation length or total milk offtake. This again
agrees with the results obtained in Gambia where non-infected cows out-produced
infected cows during lactation by only 24 kg during a l4-month location period and this
difference was not significant (Agyemang et al., 1991). However, trypanosome infection
caused a reduction in milk production during the 6 months following infection in Ndama
cows in Gambia (Agyemang et al., 1990). Larger lactation length and greater milk offtake
seen in cows starting lactation during the wet season when food was plentiful and of good
quality as compared to the dry season, suggest that nutrition is the driving factor that
determines milk production of the village Ndama CO~S. Cows calving during the last part
of the dry season performed better than those calving during the early part of the dry
season. For the latter, most of the lactation length occurred during dry months whereas
the former Will benefit from the pastures improvement in the next lwet season. In terms of
milk production, cows that gave birth between November and January were more
severely affected by food shortage than cows calving in other seasons. Feed restriction
was compounded in these cows by trypanosome infections and led to the shortest
lactation length. The trends observed regarding the interaction of season of calving and
trypanosome infection on milk offtake suggest that well fed Ndama cows could produce
milk with a no major negative influence of trypanosome infection. Similarly, Agyemang
et al. (1990) suggested that the depressive effect of trypanosome infections on milk
production could be reduced through the provision of additional food to cattle showing
signs of the disease.
Finally, the productivity
indices found in this study (Index 1 = 62.8 kg per cow, Index
2 = 28.3 kg per 100 kg cow LW and index 3 = 120.8 kg per 100 kg metabolic LW) are in
agreement with productivity
indices found in Ndama cattle under once-daily milking
system in Gambia where index 1,2 and 3 averaged 60.4,28.3 and 120.2 kg (Agyemang et
a]., 1991). Village Ndama cow productivity
seems relatively lower than that found in
Ndama cows reared on station with no milk extraction. Productivity indices 1, 2 and 3
were 70.1,29.1 and 127.0, respectively for Ndama cows reared on station in Senegal (Fall
et al., 1983).
Acknowledgements
This work was jointly carried out by ISRA, ILCA and ILRAD and was supported by
the European Development Fund. Additional fund provided by the British Overseas
Development Administration (ODA) allowed the main author to spend time at the Centre
for Tropical Veterinary Medicine, University of Edinburgh to analyse and publish the
data. Comments from A.S. Peregrine, S. Diaw and G. Vassiliades are greatly appreciated.
A. Fall et al. / Vetcrinu- Pauusitolo,yy
81 (1999) 235-247
247
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