Effect of a Wildlife-Livestock Interface on the Prevalence of Intra-Erythrocytic Hemoparasites in Cattle

doi:10.4236/ojvm.2013.38051

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Open Journal of Veterinary Medicine, 2013, 3, 315-318

Published Online December 2013 (http://www.scirp.org/journal/ojvm)

http://dx.doi.org/10.4236/ojvm.2013.38051

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: *[email protected]

Received October 22, 2013; revised November 22, 2013; accepted November 29, 2013

cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In

ABSTRACT

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

interface.

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.

R. M. KABUUSU ET AL.

316

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-

sion.

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

3.2a.

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

Open Access OJVM

R. M. KABUUSU ET AL. 317

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

support.

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