ORIGINAL PAPER

Epidemiology of Eimeria and associated risk factorsin cattle of district Toba Tek Singh, Pakistan

Tauseef Ur Rehman & Muhammad Nisar Khan &

Muhammad Sohail Sajid & Rao Zahid Abbas &

Muhammad Arshad & Zafar Iqbal & Asif Iqbal

Received: 28 July 2010 /Accepted: 8 November 2010 /Published online: 26 November 2010# Springer-Verlag 2010

Abstract A cross-sectional study was carried out to determinethe prevalence, species characterization, and associated riskfactors with Eimeria of cattle of district Toba Tek Singh fromApril, 2009 to March, 2010. Of the total 584 fecal samplesexamined for Eimeria, 275 (47.09%) were found infected withsix species of Eimeria. Among the identified species ofEimeria, Eimeria bovis was found to be the highest prevalentspecies (52.36%), followed in order by Eimeria zuernii,Eimeria canadensis, Eimeria ellipsoidalis, Eimeria alabamensis,and Eimeria cylindrica with prevalence of 48.27%, 34.83%,29.31%, 24.14%, and 8.62% respectively. Peak prevalence wasobserved in August. Cattle were infected more frequentlyduring rainy (60.32%) and post-rainy seasons (59.25%). Calveshad significantly higher prevalence (P<0.05) of Eimeria thanadults while higher prevalence of Eimeria was observed infemale cattle. Among management and husbandry practices,feeding system, watering system, housing system, floor type,and herd size strongly influenced the prevalence of Eimeria incattle. Coccidiosis was more prevalent in ground feedingsystem, pond-watered animals, closed housing system, andnon-cemented floor type (P<0.05) as compared to troughfeeding system, tap watered animals, open housing system, andpartially cemented floor types, respectively. Breed and bodycondition of animals were not found risk factors (P>0.05)influencing prevalence of Eimeria.

Introduction

Bovine coccidiosis is one of the most common parasiticdiseases of cattle that prevail widely in different parts of theworld. More than twelve different species of Eimeria incattle and buffalo have been documented uptil now.Thirteen are considered prevalent in USA. Prevalent speciesof Eimeria are Eimeria bovis, Eimeria zuernii, Eimeriaauburnensis, Eimeria canadensis, Eimeria ellipsoidalis,Eimeria subspherica, Eimeria cylindrica, Eimeria alabamensis,Eimeria wyomingensis, Eimeria bukidnonensis, Eimeriaillinoisensis, Eimeria pellita, and Eimeria brasilensis(Sanchez et al. 2008 and Abebe et al. 2008). Most commonlyprevalent species are E. bovis, E. zuernii, and E. auburnensis(Afzal 1996; Cicek et al. 2007; Abebe et al. 2008; Priti et al.2008; Sa´nchez et al. 2008 and Lassen et al. 2009). E. bovisand E. zuernii are highly pathogenic causing mortality andmorbidity by disturbing absorption mechanisms (Cicek et al.2007; Klockiewicz et al. 2007). Coccidiosis in cattle commonlyoccurs as subclinical disease causing great economical lossessigns of clinical coccidiosis include reduced appetite, reducedbody weight, unthriftness, diarrhea, dysentery, and anemia(Abebe et al. 2008). It is estimated that coccidiosis causes aneconomic loss in excess of $3,800,000 annually in Canada(Niilo 1970).

Eimeriosis in cattle is observed in all age groups but it ismost common and important in young animals. Inassociations with other enteropathogens, coccidia havebeen indicated as an important cause of diarrhea in calves(Ernst et al. 1987). A negative correlation exists betweenage of cattle and risk of infection. Younger animalsdepicted higher prevalence (27.23%) of coccidial infectionthan older animals (15.65%) as reported by Cicek et al.(2007). Higher oocyst counts have been observed inimmature as compared to adults (Waruiru et al. 2000).

T. U. Rehman :M. N. Khan (*) :M. S. Sajid : R. Z. Abbas :Z. Iqbal :A. IqbalDepartment of Parasitology, University of Agriculture,Faisalabad 38040, Pakistane-mail: khanuaf@yahoo.com

M. ArshadDepartment of Microbiology, University of Agriculture,Faisalabad 38040, Pakistan

Parasitol Res (2011) 108:1171–1177DOI 10.1007/s00436-010-2159-5

A number of risk factors like season (moisture, temperature),sex of animal, watering system, feeding system, housing systeminfluence the prevalence of disease. A higher intensity ofinfection is found in wet season as compared to dry season(Waruiru et al. 2000). Cattle directly fed on ground or grazinganimals have more chances of ingestion of coccidial infectionas compared to animals fed in feed troughs as reported byAbebe et al. (2008) from Ethopia. Female animals are moresusceptible to infection (Priti et al. 2008). Eimeriosis in cattleis particularly a problem of confined animals and the disease ismore common in housed animals than in those on pastures(Abebe et al. 2008). Fecal contamination of feed and water areimportant factors for the transmission of the infection (Tayloret al. 2007). Other factors like poor nutrition, poor sanitation,and overcrowding can increase level of infection and incidenceof the disease due to stress-induced immunosuppression (Ernstet al. 1984; Ernst and Benz 1986; Kennedy and Kralka 1987;Radostits et al. 2009; Taylor et al. 2007).

There is scarcity of information on the occurrence anddetermination of risk factors associated with bovine coccidiosisin Pakistan. Prevalence of coccidiosis was only reported byAfzal (1996) in cattle calves in Pakistan. Moreover, noattempt was made to determine the species composition andassociated risk factors of Eimeria infections in cattle inPakistan. Therefore, in preview of significance of the parasiteas one of the most important causes of economic losses andthe dearth of literature in the country, the present study wasdesigned to determine the prevalence, species composition,

and associated risk factors with Eimeria infections of cattle indistrict Toba Tek Singh (T.T. Singh), Pakistan.

Materials and methods

Study area

Study area confined to district T.T. Singh which is locatedin central Punjab between 30°33′ to 31°2′ degree northlatitudes and 72°08′ to 72°48′ degree longitudes. Thisdistrict comprises of three tehsils (Gojra, Kamalia, and T.T.Singh) and 82 union councils (UC). It occupies an area of3,252 km2 most of which is lowland that floods during therainy season. The floods originate from the Ravi River thatruns along the southern and southeastern borders. Accordingto Pakistan Livestock Survey (2006), T.T. Singh has anaverage cattle population of 270 thousands. May, June, andJuly are the hottest months of the year with maximum meantemperature of 40.7°C while December and January are thecoldest months of the year with minimum mean temperatureof 6°C. An average annual rainfall is 254–381 mm.

Sampling units

Based on two-stage cluster random sampling, the numberof primary units (UC) and elementary units (animals) wassampled using formulae as given by Thrusfield (2008).

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Selection of primary units to be sampled was done using mapgrid method. A total of 45 out of 82 union councils weresurveyed throughout the study period. Five hundred andeighty-four animals were examined in the present survey.

Development of questionnaire

A questionnaire was developed for collecting necessaryinformation from farmers regarding associated risk factorsusing closed ended (dichotomous and multiple choice)questions (Thrusfield 2008). Information regarding thefollowing determinants were collected through questionnaire.

1. Age: Animals were divided into two age categories viz;adults and young-stock. The age range of adult andyoung-stock was 5–10 years and 3–5 years respectively.

2. Breed: Sahiwal, Friesian, Jersey, and Crossbred werethe breeds under study.

3. Sex: Both sexes were sampled during study.4. Climate: Season-wise prevalence was noted separately.

The four well-marked seasons in Pakistan are:(a) Cold season (December to March)(b) Hot season (April to June)(c) Rainy season (July to September)(d) Post-rainy season (October and November)5. Husbandry and Management: Type of feeding system

(ground feeding/trough feeding), housing system (open/closed), floor pattern (non-cemented/partially cemented),watering system (tap water/pond), and herd size (larger/smaller) were observed in present study. Herds havingmore than fifty animals were designated as larger herdswhere as herds with less than this were smaller.

Collection of samples

A total of 584 fecal samples were collected. Five grams offecal samples were collected directly from rectum orimmediately after defecation in a wide-mouth plastic bottleand preserved in 10% formalin (Zajac and Conboy 2006).Collecting bottles were labeled properly.

Parasitological examination

Fecal samples were analyzed using floatation techniquewith saturated Sodium chloride solution as floatationsolution for the presence of oocyst. The procedure wasadopted as described by Zajac and Conboy (2006).Quantitative fecal examination was performed by McMastertechnique to determine the number of oocysts per gramof feces (OPG) as per the procedures of MAFF (1986).Identification of Eimeria species was based on themorphological features of the oocysts (size, shape, color,and texture of oocyst wall, presence or absence of

micropyle, polar cap, etc.) with the aid of taxonomic keys(Iqbal et al. 2006; Soulsby 2006).

Meteorological data

Data regarding meteorological parameters i.e. monthlyaverage temperature, relative humidity, and rain fall havebeen collected from Meteorological Cell, Department ofCrop Physiology, University of Agriculture, Faisalabad,Pakistan.

Statistical analyses

Logistic analysis was carried out by using logit model includingall variables in the model with backward elimination procedure.Factors with paired characteristics were analyzed using OddsRatio (OR) and Mantel–Haenszel (M. H.) chi-square. Hosmer–Lemeshow goodness-of-fit test indicated that model fits well.All the analyses were carried out using SAS software package(1998) at 95% confidence level (SAS 1998).

The prevalence was calculated for all data by using thefollowing formula:

Prevalence %ð Þ ¼ Number of infected individualsðnÞTotal number of sampled individualsðNÞ � 100

Results

Of the total 584 fecal samples of all animal examined, 275(47.09%) contained oocysts of Eimeria. The taxonomicidentification of Eimeria revealed the presence of sixspecies of Eimeira. E. bovis was found to be the highestprevalent (52.36%) species, followed in order by E. zuernii,E. canadensis, E. ellipsoidalis, E. alabamensis, and E.cylindrica with prevalence of 48.27%, 34.83%, 29.31%,24.14%, and 8.62%, respectively (Fig. 1). Mean OPG wasrecorded highest in August (2007) which lies in rainyseason in study area (Fig. 2). Generally, calves revealedhigher mean OPG than adults (Fig. 3).

E.ellipsoidalis,29.31%

E.canadensis,34.83%

E.zuernii,48.27%

E.bovis,52.36%

E.cylindrica,8.62%E.alabamensis,

24.14%

Fig. 1 Species-wise prevalence of Eimeria

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Associated risk factors

Analysis of all the hypothesized risk factors by stepwisemultivariate logistic regression model and M. H. chi-squareanalysis revealed that season, age, sex, floor, herd size,feeding; housing and watering system were the factorssignificantly associated (P<0.05) with Eimeria infection.Peak prevalence was recorded in August (69.56%) whileleast number of animals (29.54%) harbor Eimeria in March(Fig. 2). Higher prevalence was recorded during rainy(60.32%) and post-rainy seasons (59.25%) as compared tocold (39.02%) and hot seasons (35.77%). Figure 4 shows arelation between rain fall, temperature, relative humidity,and occurrence of Eimeria. Eimeria was observed in all agegroups. Calves had significantly higher prevalence(60.68%; 142/234; χ2=15.396) than adults (133/350;38%; OR=0.390; Tables 1 and 2, Fig. 5).

Eimeria infection was found to be more prevalent infemales (52.08%; 213/409; χ2=15.396) as compared tomales (35.43%; 62/175; OR=0.458; Tables 1 and 2, Fig. 5).Breeds and body condition of host animals were found to

be non-significantly associated (P>0.05) with χ2=2.1974and χ2=0.3442, respectively, although Eimeria infection inanimals having poor body condition was little higher thananimals with good body condition (Table 1).

A strong association (P<0.05) was observed betweenhousing system and risk of Eimeria infection. HigherEimeria prevalence was recorded in animals reared underclosed type of housing system (53.76%; 143/266; χ2=4.882; OR=2.071) as compared to open type (Tables 1 and2, Fig. 5). There was a statistically significant associationbetween floor type and risk of Eimeria infection. Eimeriainfection was more prevalent (P<0.05) in non-cementedfloor type (58.23%; 145/249; χ2=7.470) compared topartially cemented floor type (38.80%; 130/335; OR=0.642;Tables 1 and 2, Fig. 5). Multivariate logistic regressionanalysis and Mantel–Haenszel chi-square analysis of wateringsystem with the intensity of infection revealed that there wasa highly significant association between these two. Animalswatered at pond had significantly higher infection (55.72%;151/271; χ2=10.947; OR=1.562), compared to those giventap water (39.62%; 124/313; Tables 1 and 2, Fig. 5). Theprevalence of Eimeria was found to be highly influenced(P<0.05) by feeding system. Ground-fed animals revealedhigher risk of infection (55.86%; 143/256; χ2=12.301;OR=2.279) instead of cattle fed in troughs (40.24%; 132/328; Tables 1 and 2, Fig. 5). Prevalence of Eimeria wasstrongly predisposed by the herd size (P<0.05). Percent-age prevalence of positive cases in larger herds wasobserved higher (55.97%; 164/293; χ2=17.877; OR=2.507) than smaller ones (38.14%; 111/291; Tables 1 and2, Fig. 5).

Discussion

This is the first time that a full-scale investigation ofepidemiological aspects of Eimeria was carried out in

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Pakistan. These results were justified by reports of variousresearchers in many countries of the world like in Argentinaby Sanchez et al. (2008), in India by Harpreet and Daljit(2008) and in South Africa by Matjila and Penzhorn (2002)who recorded prevalence as 48%, 50%, and 52%, respec-tively. Overall prevalence of Eimeria in present study ishigher than previously reported in Pakistan by Afzal (1996)

who found 19% infection in cattle. This suggests thatepidemiological status of Eimeria infection has beenchanged. The results are lower than the observations ofRodríguez-Vivas et al. (1996), Von Samson-Himmelstjernaet al. (2006), Klockiewicz et al. (2007), and Abebe et al.(2008). This variation is most likely attributed to thedifferences in agroecology, management, and husbandry

Table 1 Mantel–Haenszel chi-square analysis of all hypothesized risk factors with Eimeria infection in cattle of district T.T. Singh

Associated determinants Variables Prevalence (n/N) Mantel–Haenszel chi-square (P value)

Age Young 60.68% (142/234) 28.1782 (<0.0001)Adult 38% (133/350)

Sex Male 35.43% (62/175) 15.3961 (<0.0001)Female 52.08% (213/409)

Breed Crossbred 51.43% (126/245) 2.1974 (0.1382)Sahiwal 43.89% (97/221)

Fresion 48.53% (33/68)

Jersey 33.33% (20/60)

Feeding system Ground 55.86% (143/256) 12.3006 (0.0005)Trough 40.24% (132/328)

Floor Non-cemented 58.23% (145/249) 7.4702 (0.0063)Partially cemented 38.80% (130/335)

Housing system Open 41.51% (132/318) 4.8823 (0.0271)Close 53.76% (143/266)

Watering system Tap water 39.62% (124/313) 10.9472 (0.0009)Pond 55.72% (151/271)

Herd size Larger 55.97% (164/293) 17.8767 (<0.0001)Smaller 38.14% (111/291)

Body condition Poor 48.33% (159/329) 0.3442 (0.5574)Good 45.49% (116/255)

Prevalence (%)=n/N×100

n, number of animals infected; N, total number of animals examined

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practices of the study animals in different countries.Eimeria species identified in present study have beenpreviously reported by Abebe et al. (2008), Klockiewiczet al. (2007), and Lassen et al. (2009). E. bovis and E.zeurnii were recorded as the highest prevalent coccidianspecies which is in accordance with reports of Ernst et al.(1984), Kennedy and Kralka (1987), and Cornelissen et al.(1995). According to Levine (1985), these two species arethe most pathogenic of the bovine coccidia.

Higher prevalence observed in young animals is inaccordance with findings of Waruiru et al. (2000), Ciceket al. (2007), Abebe et al. (2008), Priti et al. (2008), andLassen et al. (2009) who demonstrated that age stronglyinfluences the risk of infection with Eimeria. Calveshave been found to be more susceptible to Eimeriainfections due to immature immunity (Grafner andGraubmann 1979). Calves had significantly higher oocystcounts than adults which is in agreement with Waruiruet al. (2000).

The results of month wise prevalence of Eimeria inpresent study were not different from previous reports likeRodríguez-Vivas et al. (1996) who reported higher preva-lence during month of July (month of rain). Waruiru et al.(2000) recorded that wet season prevalence of coccidialinfections in calves and immatures were significantlyhigher than those in the dry season. However peakprevalence was recorded during late wet season by Wojiet al. (1994). An increase in prevalence in rainy and post-rainy season could be attributed to increase in rain fall andtemperature (Pilarczyk et al. 2000; Taylor et al. 2007). InTanzania, higher median oocyst counts were observedduring the dry short rainy seasons compared to otherseasons (Kusiluka et al. 1998). Prevalence of coccidiosis inspring and summer was rarely observed (Skirnisson 2007).The slight variation in the occurrence of coccidiosis indifferent regions of world may be due to varied seasonalclimate.

Higher prevalence of Eimeria was recorded in femalesin the present study. Similar results were reported by Priti

et al. (2008) from India that female cattle and buffaloeswere more susceptible to infection. Different breeds werefound to have no genetic influence on prevalence ofEimeria. Similar results were also recorded by Jäger et al.(2005) who observed non-significant differences in preva-lence of Eimeria in German Angus and German Simmentalbreeds of cattle.

Findings of ground fed animals being at higher risk toEimeria infection than trough fed cattle are in agreementwith the findings of Abebe et al. (2008) who described asignificant association between different feeding systems ofcalves and the risk of infection with Eimeria species. Thisfinding is in agreement with the recommendation describedby Radostits et al. (2009) and Kennedy (2001) to avoid thefeeding of calves on the ground as this increase the chancesof contamination of the feed with Eimeria oocysts. Priti et al.(2008) reported that prevalence of coccidiosis was higher install-fed in comparison to free range cattle. Ernst et al.(1987) stated that eimeriosis in cattle is particularly aproblem of confined animals and that the disease is morecommon in housed animals than in those on pastures. Theobservation regarding higher prevalence in animals kept atnon-cemented floor may be true because it is easy to cleancemented floor than non-cemented floor. Reason for higherprevalence of Eimeria in pond-watered animals may be morecontamination of water in ponds and overcrowding around alimited water source, which concentrates the hosts andparasites within a restricted area. McKellar (2008) describedthat clinical coccidiosis is more prevalent under conditionsof poor sanitation, poor nutrition, and overcrowding. So,lower number of animals was observed infected withEimeria in smaller herds as compared to larger herds in thecurrent study. These results are in accordance with findingsof Kusiluka et al. (1998) who described that small herdsizes may result in low environmental contamination.Klockiewicz et al. (2007) also reported that the highlypathogenic Eimeria occurred more frequently in big farmsrather than in small farms.

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Fig. 5 Association of various risk factors with prevalence of Eimeriain cattle of district T.T. Singh

Table 2 Multivariate logistic regression analysis of associated factorswith risk of Eimeria infection in cattle of district T.T. Singh

Term Odds ratio C.I. P value

Month 1.156 1.088–1.228 0.000

Age 0.422 0.279–0.637 0.000

Sex 0.512 0.325–0.805 0.004

Floor 0.487 0.315–0.755 0.001

Housing system 2.671 1.759–4.057 0.000

Watering system 2.166 1.436–3.265 0.000

Feeding system 1.741 1.123–2.700 0.013

Body condition 0.482 0.314–0.741 0.001

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