Open Journal of Veterinary Medicine, 2013, 3, 315-318
Published Online December 2013 (
Open Access OJVM
Effect of a Wildlife-Livestock Interface on the Prevalence
of Intra-Erythrocytic Hemoparasites in Cattle
Richard M. Kabuusu1,2*, Ruth Ale xa n de r1, Annet M. Kabuusu2, Sylvia N. Muwanga3,
Patrick Atimnedi4, Calum Macpherson2,5
1Pathobiology Academic Program St. George’s Grenada, School of Veterinary Medicine,
St. George’s University, St. George’s, Grenada
2Graduate Studies Program, St. George’s University, St. George’s, Grenada
3Department of Wildlife and Animal Resources Management, Faculty of Veterinary Medicine,
Makerere University, Kampala, Uganda
4Uganda Wildlife Authority (UWA), Kampala, Uganda
5School of Medicine, St. George’s University, St. George’s, Grenada
Email: *
Received October 22, 2013; revised November 22, 2013; accepted November 29, 2013
Copyright © 2013 Richard M. Kabuusu et al. This is an open access article distributed under the Creative Commons Attribution Li-
cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In
accordance of the Creative Commons Attribution License all Copyrights © 2013 are reserved for SCIRP and the owner of the intel-
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We conducted a cross-sectional study to establish the effect of proximity of livestock to a wildlife-livestock interface on
the relative abundance of intra-erythrocytic hemoparasites in cattle. Blood samples were obtained from 131 randomly-
selected cattle raised around Queen Elizabeth National Park. Cattle-farm location was determined by using Global Posi-
tioning System device from an arbitrarily reference point. Giemsa-stained blood smears were examined microscopically
for intra-erythrocytic hemoparasites. Correlational analysis was used to examine the relationship between farm location
and prevalence, wh ereas risk ratios were u sed to determine the strength of mixed hemoparasitic infections among cattle,
using a significant level of α = 0.05. The location of a cattle farm significantly predicted the prevalence of Anaplasma
(rs = 0.33, p < 0.05) and Theileria ( rs = 0.57, p < 0.01) but, far m’s proximity to QEN P did not explain the var iation in
the prevalen ce of Bab esia (rs = 0.14, p < 0.2). Althou gh mix ed infections occurred in 15% of sampled cattle, concurren t
infection of cattle with A. marginale and B. bigemina [RR = 36; 95% CI (7.191); p < 0.001] was the only statistically
significant mixed infection which was record ed. This study demonstrated that unlike the pr evalence of B. bigemina, the
prevalence of T. parva and A. marginale in livestock sign ificantly increased with close proximity to a wildlife-liv estock
Keywords: Wildlife- L i v estock I n t erface; Geographical Information System; Proximity; Ankole Long-Horned Cattle;
Intra-Erythrocytic Hemoparasites
1. Introduction
Wildlife-livestock interfaces are characterized by conflict
between livestock keepers and wildlife conservation au-
thorities especially as it relates to the transmission and
prevention of diseases common to both wildlife and do-
mesticated animals [1].
Livestock keepers living within the wildlife-livestock
interface mostly practice pastoral farming as a sustain-
able management system [2]. This management system is
characterized by bidirectional movement of domesticated
cattle and wild herbivores in search of water and pasture
with little regard to defined boundaries, limited access to
veterinary services, use of local plant species for pro-
phylaxis and chemotherapy, and if inadequate at all any
record keeping [2,3]. Such characteristics of the wildlife-
livestock interface are fundamentally responsible for
patterns of distribution of ticks and tick borne diseases
(TTBDs) between livestock and wildlife [2,4]. Cattle
keepers raising animals around wildlife national parks
have identified Theileriosis (East coast fever) caused by
Theileria parva and vectored by Rhepicephalus appen-
diculatus; Anaplasmosis caused by Anaplasma margi-
*Corresponding author.
nale and vectored by R. evertsi evertsi and Babesiosis
(Red water) caused by Babesia bigemina and vectored by
Boophilus decoloratus as priority diseases [3,5-7].
In an effort to find solutions to conflicts which occur
as a result of these diseases, as well as to better under-
stand the effect of the wildlife-livestock interface on the
transmission dynamics of intra-erythrocytic hemopara-
sites, Ankole-long horned cattle raised around Queen
Elizabeth National Park (QENP) were sampled and
tested with the aim of investigating whether pro ximity of
livestock to a wildlife-livestock influenced the relative
abundance of intra-erythrocytic hemoparasites. Non-
intra-erythrocytic hemoparasites are beyond the scope of
this study.
2. Materials and Methods
2.1. Study Area and Design
With permission from the Uganda Wildlife Authority
(UWA) and Uganda National Council for Science and
Technology, a cross sectional survey was performed
around QENP between June, 2005 and March, 2006.
QENP covers an area of over 2000 sq km and lies in the
Western region of Uganda (0˚23'S Latitude 29˚58'E Lon-
gitude). Katunguru Bridge was arbitrarily selected a ref-
erence point and farms located east to this point were
included in the study. Geographical information system
(GIS) coordinates of the kraal were taken for each farm
using a global positioning system (GPS) device (Garmin
eTrex® Legend C). Inclusion criteria considered farms
with 10 - 30 indigenous Ankole long-horned cows aged
between 1 month and 7 years. Cattle with evidence of
clinical disease were excluded from the study but, ap-
propriate treatment protocols with anti-protozoa agents
were instituted. Because of confidentiality concerns, as
well as the purpose of the study, all farms were coded
with unique identification numbers.
2.2. Sampling and Sample Size Determination
An established prevalence (10%) of mixed hemoparasite
infection in adult cattle [8] and a 20% tolerable error
were assumed when determining the number of cows to
be randomly selected into the study [9]. About 3 mls of
blood were obtained by venipuncture of the jugular or
tail veins of each cow sampled and placed in EDTA
(Becton-Dickinson, vacutainer system, USA), labeled
and stored at 6˚C until further processing. Thin blood
smear were prepared and stained with May-Grunwald-
Giemsa and microscopically examined under oil immer-
2.3. Data Analysis
Cattle were classified as positive or negative for intra-
erythrocytic hemoparasites based on microscopic evalua-
tion of the blood smear. Data were coded and statistical
analyses were performed using EPIINFO (version 7,
CDC, Georgia, Atlanta USA) at a significant level of α =
0.05. We used a Spearman’s rank correlation co-efficient
to test for the effect of livestock proximity to a wildlife-
livestock interface and risk ratio (RR) to determine the
strengths of associations of mixed infection. Distances
from the reference point, Katunguru Bridge, determined
by GIS coordinates was calculated using GIS Arc View
Prevalence 100
Total number of animals sampled
No ofanimals withparasite
RDP 100
Total number of parasite s id entifie d
Number ofspecific parasite
RDP: Relative diagnostic percentage.
3. Results
The target population was 139 cows but, blood samples
were randomly obtained from only 131 cows located on
13 farms giving a response rate of 94.2% (131/139).
Failure to collect blood samples from 8 cows was due to
a lack of adequate handling facilities. The nearest farm
was 2.7 miles whereas farthest farm included in the study
was 20.8 miles away the reference point. The prevalence
of all intra-erythrocytic hemoparasite infections com-
bined was 55.7% (73/131) with varying between-farm
prevalence (Table 1).
The prevalence of T. parva and A. marginale increased
significantly with close proximity of livestock to the
wildlife-livestock interface (rs = 0.57, p < 0.01) and (rs =
0.33, p < 0.05) respectively but, the prevalence of Babe-
sia did not vary significantly with closeness to the wild-
life-livestock interface (rs = 0.14, p = 0.2). Mixed intra-
erythrocytic hemoprotozoan infections were detected in
15% (11/73) of cows and the number of hemoparasites
identified ranged from 0 - 3 per cow but, the only statis-
tically significant mixed infection was recorded between
A. marginale and B. bigemina [RR = 36 ; 95% CI (7.191);
p < 0.001] (Table 2).
4. Discussion
This study is unique that it utilized proximity of the in-
digenous Ankole lon g-horned breed of cattle to Q ENP as
a model for investigating the consequences of increasing
interaction of domestic cattle with wildlife on the distri-
bution of intra-erythrocytic hemoparasites in cattle.
In spite of the fact that intra-erythrocytic hemopara-
sites routinely cause fatal disease in cows [10] and that
their prevalence was high, the cows used in this present
study did not have evidence of clinical disease. This
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Table 1. Prevalence (%) of intra-erythrocytic hemopara-
sites in cattle stratified by farm proximity.
Prevalence % (95% CI)
Farm i.d n Distance
(miles) T. parva A. marginale B. bigemina
1 11 2.7 55 (23, 83)36 (11, 69) 9 (0, 41)
2 9 3.9 89 (52, 99)0 (0, 36) 0 (0, 34)
3 10 4.8 60 (26, 88)60 (26, 88) 10 (0, 45)
4 9 6.0 78 (40, 97)22 (3, 60) 11(0, 49)
5 11 7.1 73 (39, 94)9 (0, 41) 22 (3, 52)
6 9 7.8 78 (40, 97)22 (3, 60) 22 (3, 60)
7 9 9.0 11 (0, 11) 11 (0, 48) 0 (0, 37)
8 10 10.6 50 (19, 81)0 (0, 31) 0 (0, 31)
9 10 11.5 40 (26, 87)20 (3, 57) 10 (0, 44)
10 11 12.4 64 (31, 89)18 (2, 51) 18 (0, 31)
11 10 14.6 0 (0, 31) 0 (0, 31) 0 (0, 29)
12 11 18.3 18 (3, 52 ) 0 (0, 29) 0 (0, 29)
13 11 20.8 0 (0, 29) 0 (0, 29) 0 (0, 29)
i.d = identification; n = number of cows sam pled.
Table 2. Overall prevalence and relative diagnostic percent
of intra-erythrocytic hemoparasites.
Prevalence 95% CI
Relative diagnostic
percent %
Theileria parva 51% (95% CI 49, 62); 68% (66/97)
Anaplasma marginale 15% (95% CI 9, 21) 21% (20/97)
Babesia bigemina 8% (95% CI 4, 15) 11% (11/97)
finding indicates that this indigenous cattle breed has
adapted mechanisms to regulate the growth and devel-
opment of hemoprotozoa in their blood which has led to
endemic stability [11]. Th is desirable characteristic ma kes
the Ankole long-horned breed apt for mixed livestock-
wildlife production systems; henc e it lessens some of the
conflicts in this wildlife-livestock interface.
With the highest prevalence and highest relative fre-
quency of detection (RDP), T. parva appears to be of
primary importance within the QENP wildlife-livestock
interface. This suggests that wildlife, especially the Cap e
buffalo, which is a keystone species in QENP, is a natu-
ral reservoir, and therefore a fundamental source of vec-
tors and hemoparasites for cattle [12].
T. parva and A. marginale infections were signifi-
cantly higher in cattle raised closer to QENP wildlife-
livestock interface. The zonal differences in prevalence
may be directly correlated with the distribution of the
specific vectors involved. Babesia bigemina had the low-
est prevalence and proximity of cows to QENP was not
significantly associated with the prevalence of B. bige-
mina in farmed cows. This finding is in accordance with
previous research findings, whi ch demonstrated that trends
of B. bigemina across different ecological zones were
similar [13]. Mixed A. marginale and B. bigemina infec-
tions were common and statistically significant, and
likewise a high farm prevalence of A. marginale was
matched by a high farm prevalence of B. bigemina. Simi-
lar mechanisms of transmission or cross-transmission
may be possible explanations for the coexistence of A.
marginale, and B. bigemina in cows [8,14].
The effects of confounding factors such as use of
acaricides (concentration and frequency of application)
or the method of acaricide application (spraying versus
dipping) was not assessed in this study. Future studies
using serological and molecular diagnostic tools are en-
couraged and may be performed concurrently with he-
moparasites in wildlife herbivores.
5. Conclusion
In conclusion, this study finds evidence that proximity of
livestock to a wildlife-livestock interface explains a sig-
nificant proportion of the variation in the prevalence of T.
parva and A. marginale infection in cattle but, it does not
explain the variation in the prevalence of B. bigemina
infection in cattle.
6. Acknowledgements
The authors wish to thank Texas A&M University, Mi-
nority Initiative for Research and Training (MIRT), St.
George’s University School of Veterinary Medicine,
Windward Research and Education Foundation (WIN-
DREF) for funding the research. We wish to thank Dr.
Raymond Sis and Dr. Ludwig Siefert their assistance and
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