Veterinary Parasitology: Regional Studies and Reports 12 (2015) 1620

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Veterinary Parasitology: Regional Studies and Reports

journal homepage: www.elsevier.com/locate/vprsr

Bovine eimeriosis in Swedish calves: Epidemiology and insights into

sampling procedures
Anna Forslid a, Dan Christensson b, Jan Dahl c, Giulio Grandi b,, Jrg M.D. Enemark d
a
Sknemejerier, SE 205 03 Malm, Sweden
b
Department of Microbiology, National Veterinary Institute, SE 751 89 Uppsala, Sweden
c
Jan Dahl Consult, strupvej 89, DK-4350 Ugerlse, Denmark
d
Bayer Healthcare, Arne Jacobsens All 13, 6., DK-2300 Copenhagen S, Denmark

a r t i c l e i n f o a b s t r a c t

Article history: Bovine eimeriosis is a common, globally distributed infection in housed calves aged from 3 to 12 weeks. To date,
Received 10 November 2015 no national prevalence study revealing the occurrence and distribution of Eimeria species under Swedish
Received in revised form 9 February 2016 environmental and farming conditions has been performed.
Accepted 16 February 2016
This study revealed the excretion of Eimeria bovis or Eimeria zuernii (alone or together) in 23% of all sampled
Available online 21 February 2016
calves (N = 541) and 61% of all herds (N = 99). The number of tested calves was critical for whether positive
Keywords:
calves were detected or not. Nine other Eimeria species were identied, the most frequently reported being
Eimeria bovis Eimeria ellipsoidalis (9% and 35% of positive calves and herds, respectively) and Eimeria auburnensis (4% and
Topic: 19% of positive calves and herds, respectively). Not all calves shedding oocysts had diarrhoea and not all
Eimeria zuernii diarrhoeic calves shedded oocysts. Based on these present ndings, Swedish cattle practitioners should include
Coccidia bovine eimeriosis as a relevant differential diagnosis to other common gastrointestinal pathogens in 3 to
Topic: 12 weeks old calves with diarrhoea or unthrifty calves without diarrhoea. When testing a herd for bovine
Calves eimeriosis, a sufcient number of faecal samples, i.e. 10 or more samples, should be examined to obtain a reliable
Diarrhoea
picture of the infection status in a given farm.
Sweden
2016 Elsevier B.V. All rights reserved.

1. Introduction
Eimeria spp., commonly known as coccidia, are parasitic protozoa
commonly found in many mammalian and bird species, including cattle
(Andrews et al., 2004). They are obligate, intracellular parasites that
cause the destruction of infected cells. Bovine Eimeria spp. belong to
the intestinal form of coccidia and develop in the epithelial cells of
different regions of the intestinal tract. There are also forms of coccidia
which parasitise other locations (e.g. hepatic and renal forms in rabbits
and geese).
Transmission occurs orofaecally via the intake of resistant sporulated
oocyst stage in the environment (Daugschies and Najdrowski, 2005;
Taylor and Catchpole, 1994). There are 12 different species of Eimeria
described in European cattle. Of these, mostly Eimeria bovis, Eimeria
zuernii and Eimeria alabamensis are considered pathogenic (Daugschies
and Najdrowski, 2005; Taylor and Catchpole, 1994), although recent
ndings suggest that other Eimeria spp. may have a synergistic role in
the development of disease (Enemark et al., 2013). Eimeria spp. are
commonly found in cattle herds (Autzen et al., 2002; Daugschies and
Najdrowski, 2005; Enemark et al., 2013; Kurkela et al., 2000; Svensson,
Corresponding author.
E-mail address: giulio.grandi@sva.se (G. Grandi).
1993; Taylor and Catchpole, 1994). Economic losses due to Eimeria infec-
tions in cattle and buffaloes were estimated to be around USD 700 million
per year in 1980 (Fitzgerald, 1980) and to be (only in cattle) around USD
400 million worldwide in 2002 (Matjila and Penzhorn, 2002). Losses due
to reduced feed efciency were recently calculated to GBP 2560 per calf
with coccidiosis (Andrews, 2008). A recent study by Lassen and
stergaard, using a herd simulation model, predicted an annual loss of
68% due to eimeriosis (Lassen and stergaard, 2012).
Pathogenic Eimeria species are frequently isolated from 3 to
12 weeks old calves with diarrhoea (Autzen et al., 2002) and are thus
an important differential diagnosis in diarrhoeic calves (Andrews
et al., 2004). The infection may be present either as a subclinical or a
clinical form. Both forms affect the well-being of the calf and its weight
gain (Daugschies et al., 2007) and in serious cases may lead to a chronic
deterioration of the calf's general state of health or a long recovery peri-
od (Fitzgerald and Manseld, 1972; Oetjen, 1993).
Diagnosis is based on identication and quantication of faecal
oocysts together with clinical ndings (Henriksen and Korsholm,
1984; Daugschies and Najdrowski, 2005; Thienpoint et al., 1986).
So far no national study has documented the occurrence and distribu-
tion of E. bovis and E. zuernii as well as other Eimeria species in Swedish
cattle herds. The present study aimed at investigating the prevalence of
coccidia in calves after being relocated from individual to group housing

http://dx.doi.org/10.1016/j.vprsr.2016.02.004
2405-9390/ 2016 Elsevier B.V. All rights reserved.
 A. Forslid et al. / Veterinary Parasitology: Regional Studies and Reports 12 (2015) 1620
pens. Furthermore, it was hypothesised that highly pathogenic Eimeria
species are present in the majority of Swedish cattle herds.
2. Methods
2.1. Herds
A total of 541 calves were included in the study. The calves were
distributed throughout 99 cattle herds (Fig. 1), of which 95% were
dairy herds and 5% beef herds, which varied in size between 30 and
980 cattle (individual herd size not recorded). At the time of sampling
(2006) the Swedish national herd consisted of 387,500 dairy cows and
177,500 beef cattle distributed on 8000 dairy herds and 12,400 beef
herds, respectively (Statistics Sweden, 2015). Calves were group
housed. Beef and dairy herds, which participated in the study, consisting
of at least 30 cows and had individual routines for weaning and
regrouping of calves. The animals were either loose or tied up, and the
Fig. 1. Distribution by region of Swedish cattle herds enrolled in the prevalence study of
Eimeria bovis and Eimeria zuernii, winter to autumn 2006. Every black dot represents a
herd.
17
stocking rate varied. Treatment or prevention of coccidiosis by means
of coccidiocidals was not performed within four weeks prior to testing.
2.2. Sampling
Sampling was carried out during winter to autumn 2006. Faecal
sampling was performed either as part of acute veterinary advise or a
planned farm visit. Samples were collected randomly in each herd
from 5% of the reared calves between 3 weeks and 9 months of age. In
herds with less than 100 calves in this age-category, samples were
obtained from 10% of the calves. Individual rectal samples (1015 g)
were taken from calves in group housing pens for at least three weeks.
Each sample was marked with date, calf and herd numbers and absence
or presence of diarrhoea (liquid or unformed stool). In addition, age,
history and type of herd (dairy or beef) was recorded. Upon collection,
samples were stored in cool boxes and subsequently shipped to the
Swedish National Veterinary Institute (SVA, Uppsala, Sweden) for
analysis.
2.3. Parasitological analysis
The samples were analysed using a modied otation method for
the detection and identication of Eimeria parasites. For each sample,
3 g of faeces were homogenised, mixed with a sucrosesalt (NaCl)
solution with a density of 1.280 (Thienpoint et al., 1986) and subse-
quently ltered through a single layer of cheese cloth as described by
Henriksen and Aagaard (1975). The strained faecal suspension was
poured into a 10 ml test tube to form a convex meniscus on the
top. A 18 18 mm cover slip was then placed on the top of the test
tube and left to oat for 20 min. The cover slip was then transferred
to a microscope slide and examined for the presence of oocysts. The
species identication was performed by morphological assessment
of unsporulated oocysts using the criteria described by Eckert et al.
(1995), and their size was measured using an ocular micrometer
under an optical microscope at 100400 times magnication. The
total quantity of identied Eimeria oocysts was graded at 100 times
magnication on a 5-point scale, (0 = none under all of the cover
slip, (+) = single (a single oocyst under the cover slip), + = few
(210 oocysts under all of the cover slip), ++ = medium (35
oocysts/view eld) and +++ = high/massive occurrence (N5
oocysts/view eld)).
2.4. Statistical analysis
The association between diarrhoea in a single calf and the range of
explanatory variables was investigated in a generalised linear mixed
model (Glimmix, SAS institute, logit link, binomial distribution) taking
into consideration two of the pathogenic species (E. bovis and E. zuernii).
Explanatory variables included the quantity of E. zuernii and E. bovis in
the calf (none, single, few, medium, high), prevalence (in %) of
E. zuernii in other calves in the herd, the prevalence (in %) of E. bovis
in other calves in the herd, geographical region (North, Mid, Swea,
South, see Fig. 1), the age and the number of calves in the tested groups.
Incidence in other calves was included due to the fact that diarrhoea can
occur before oocyst can be detected in the faeces (Daugschies and
Najdrowski, 2005). The number of sampled calves was included as an
expression of the herd size. The herd and geographical region was
inserted as a random effect. The model was then reduced until there
were only signicant variables remaining. Although the geographical
region in itself was not a signicant variable inside the model, it
was left inside the model since it proved to have an effect on other
parameter estimates. The nal model had the following formula:
Logit (diarrhoea)=+1 E.zuernii (medium/high) +2 E .zuernii
(few)+3 E.zuernii (individual)+4 Midregion+5 Northregion+
6 Swearegion + 7 (E .bovis in other calves)+8 age + 9 number
18 A. Forslid et al. / Veterinary Parasitology: Regional Studies and Reports 12 (2015) 1620

Table 1
Prevalence of Eimeria bovis and Eimeria zuernii in Swedish cattle herds and in calves 39 months of age.

Number Findings of pathogenic E. bovis + E. zuernii (%) Findings of Eimeria bovis (%) Findings of Eimeria zuernii (%)

Farms 99 60 (61%) 54 (55%) 35 (35%)

Individual tests (calves) 541 123 (23%) 100 (18%) 47 (9%)

of calves tested . Medium and high counts were combined due to few age and diarrhoea was nearly always noted in this age range. At the
observations. time of sampling, 32% of all herds had either one or more calves with di-
The statistical analysis was repeated using the level of E. zuernii or arrhoea, while 7% of all tested calves had diarrhoea. In non-shedding
E. bovis as a continuous variable, coded 0, 1, 2, 3 and 4 corresponding calves, 5% (27 calves) had diarrhoea. Shedding of E. zuernii was not
to none, single, few, medium, high counts of coccidia, and coding region age dependent, whereas shedding of E. bovis oocysts tended to increase
from north (1) to south (4). with increasing age, thus increasing the probability of nding E. bovis
Herd sensitivity of the sampling frame of 5% of calves in herds with with increasing age by about 12% (OR = 1.12, p = 0.06).
more than 100 calves in the relevant age group and 10% of calves in Table 5 shows the number of samples per herd and the number of
herds with less than 100 calves in the relevant age group was evaluated herds found positive for pathogenic Eimeria spp., in relation to the
using the lowest in-herd prevalence-estimate (= design prevalence) total number of samples. As expected, the chance of nding at least
obtained across all herds with at least one positive sample. one sample positive for E. bovis and/or E. zuernii increases with increasing
Assuming a test-sensitivity and test-specicity of 100%, herd- sample size. The herd sensitivity of 10% of the calves in herds up to 50
sensitivity can be calculated as 1 minus the hypergeometric probability calves was under 50%, even for sample sizes up to 6 samples, when the
of obtaining zero positive samples out of n sampled in a population of N design prevalence was 10%. On the other hand, a sample size of 10
with 10% positive for pathogenic Eimeria in the population. would result in a 67% likelihood of detecting E. bovis or E. zuernii, using
These results were then compared to the observed number of the same design prevalence.
positive herds given the sample size. Furthermore, it could be shown (Table 4) that increasing occurrence
The correlation between the occurrence of E. bovis and E. zuernii and of diarrhoea was signicantly correlated to increasing quantities of
age was investigated using a logistic regression model with age in E. zuernii (OR = 9.0, p = 0.05). E. zuernii was a signicant predictor of
months as the explanatory variable and the prevalence of E. zuernii or diarrhoea, both as a continuous variable (p-value = 0.02) and as a
E. bovis as the dependent variables. Age as a variable was investigated class variable (p = 0.05). Similarly, calves from herds in which E. bovis
both as a linear explanatory variable and as a second degree polynomial. was present showed a signicantly increased risk (OR = 2.25, p =
As calves from the same herd cannot be regarded as independent obser- 0.04) of having diarrhoea (Table 4).
vations, the herd effect was modelled by using proc genmod (SAS Inst.) The overall geographical region effect was not signicant (p = 0.09)
and inserting herds as a repeated statement. if correction was made for occurrence of the pathogenic Eimeria spp.
Logit (prevalence of pathogenic Eimeria)=+(age in months)+ (Table 1). However, if the tested herds were split geographically into
(age in months)2 the Northern, Mid, Swea and Southern regions, occurrence of diarrhoea
was most prominent in the Mid region, where as the lowest prevalence
3. Results was found in the Northern region. This difference was statistically
signicant after correction for the herd effect (p = 0.02).
In total, 78% (condential levels (CL):6985) of the herds and 37% Some differences in incidence of diarrhoea between regions may
(CL: 3341) of the calves were tested positive for Eimeria spp. The prev- therefore be explained by the difference in incidence of pathogenic
alence of E. bovis and E. zuernii on farms and individuals, respectively, Eimeria species between the regions.
are shown in Table 1. At least one of them (E. bovis or E. zuernii) were
found in 61% (CL: 5170) of the herds and in 23% (CL: 1926) of 4. Discussion
sampled calves. Eimeria bovis was found in 55% (CL: 4665) of the
herds and 18.5% (CL: 1522) of sampled calves, whereas E. zuernii was Eimeriosis in housed calf populations is an infection that can result in
found in 35% (CL: 2745) of the herds and 8.7% (CL: 6.611.4) of sam- clinical or sub-clinical disease in calves older than three weeks. The
pled calves. Prevalence gures of other Eimeria species are presented present prevalence study is the rst of its kind in Sweden and results
in Table 2. Single infections as well as coinfection by E. bovis and are in agreement with previous studies performed throughout Europe.
E. zuernii, as well as other types of coinfection are presented in Table 3. Since such studies always differ in design it is difcult to compare
The overall results showed a statistically signicant decrease of them directly. Based on available reports, prevalence of Eimeria spp.
diarrhoeic cases with increasing age (Table 4, OR = 0.63, p b 0.0001). recorded in Swedish farms is midway between those lower prevalences
Shedding of oocysts was most common during the rst four months of recorded in southern Europe, England and Hungary and the highest
prevalences in many cases as high as 100% recorded in central-
northern Europe, i.e. in France, Austria, Germany, Denmark and
Table 2 Poland. Even when looking at the single prevalence gures of E. bovis
Prevalence of other Eimeria species in Swedish cattle herds and in calves 39 months of
age.
Table 3
Eimeria spp. Positive farms Positive individual tests Co-infection status in Swedish cattle herds and in calves 39 months of age.
(n = 99) (calves, n = 541)
Status Positive farms Positive individual tests
E. pellita 4 (4%) 5 (0.9%)
(n = 99) (calves, n = 541)
E. subspherica 12 (12%) 13 (2.4%)
E. ellipsoidalis 35 (35%) 47 (8.7%) E. bovis alone 31 (31%) 44 (8.1%)
E. auburnensis 19 (19%) 24 (4.4%) E. zuernii alone 15 (15%) 17 (3.1%)
E. wyomingensis 13 (13%) 20 (3.7%) E. bovis and E. zuernii alone 11 (11%) 11 (2.0%)
E. canadensis 9 (9%) 15 (2.8%) E. bovis + other Eimeria spp. 24 (24%) 32 (6.0%)
E. alabamensis 8 (8%) 13 (2.4%) E. zuernii + other Eimeria spp. 6 (6%) 6 (1.1%)
E. cylindrica 9 (9%) 14 (2.6%) E. bovis + E. zuernii + other Eimeria spp. 11 (11%) 12 (2.2%)
E. braziliensis 1 (1%) 1 (0.2%) Other Eimeria spp. alone 46 (46%) 74 (13.7%)
 A. Forslid et al. / Veterinary Parasitology: Regional Studies and Reports 12 (2015) 1620 19

and E. zuernii, the situation looks quite similar, with prevalences of these Table 5
two parasites being highest in Denmark, Germany, Austria and Poland Number of samples per herd, number of herds divided per sample size, positive herds for
pathogenic Eimeria spp. and calculated herd sensitivity (using design-prevalence of 10%
(Autzen et al., 2002; Bangoura et al., 2012; Bhushan et al., 2006; and assuming 100% test-sensitivity and specicity).
Enemark et al., 2013; Koutny et al., 2012; Maddox-Hyttel and
Vestergaard, 2002; Stewart et al., 2008). Regarding reports of bovine Sample sizea Number of herds Number of positive Herd sensitivity
herds (%) (designprevalence 10%)
coccidiosis in Sweden, in one study of 22 peripartal cows and 27 calves
(neonatal to 15 weeks old), Svensson (1993) found that 50% of the 1 1 0 10%
2 10 4 (40%) 19%
calves excreted oocysts (among others E. bovis, E. alabamensis and
3 21 6 (29%) 28%
E. auburnensis) before they were transferred to group housing pens. 4 10 6 (60%) 36%
Another study demonstrated the overwintering of E. alabamenesis 5 23 16 (70%) 42%
oocyst in all regions of Sweden (Svensson, 1995). 6 4 2 (50%) 48%
The present study revealed that E. zuernii was more often observed 7 5 5 (100%) 54%
8 4 4 (100%) 59%
in connection with diarrhoea than E. bovis, which is in agreement with 9 3 3 (100%) 63%
the general perception that E. zuernii is the most pathogenic of the 10 15 12 (80%) 67%
Eimeria species in calves (Taylor and Catchpole, 1994). On several 11 2 1 (50%) 42%
occasions (5%), especially in 4 week old diarrhoeic calves, no oocyst 12 1 1 (100%) 48%
shedding was found. The identication of other probable causative a
10% in herds with less than 100 calves in the age group and 5% in larger herds.
agents of diarrhoea (Andrews et al., 2004) was out of the scope of this
study.
On the other hand, Eimeria spp. oocysts could be demonstrated in a representative amount of faecal samples (Daugschies et al., 2007). A
faeces from calves without diarrhoea, conrming the subclinical nature representative sampling regime should consist of a sufcient number
of Eimeria spp. infection, even in the present scenario (Daugschies and (Table 5) of faecal samples from the calves in each herd in order to be
Najdrowski, 2005; Daugschies et al., 2007; Taylor and Catchpole, able to reliably exclude clinical or subclinical eimeriosis. Under practical
1994; Grandi et al., 2016). The explanation for this observation could conditions and when the disease is present, an even higher in-herd
also be a result of low oocyst uptake (i.e. good hygiene), partial prevalence can be expected (Daugschies and Najdrowski, 2005), thus
immunity in the calf, the age of the calf or incorrect sampling time increasing the likelihood of detecting E. bovis and/or E. zuernii when
(Daugschies and Najdrowski, 2005; Taylor and Catchpole, 1994). collecting 10 or more faecal samples.
According to the most recent classication (KppenGeiger, see Peel
et al., 2007), the climate of Sweden can be divided into warm summer 5. Conclusion
temperate climate (Dfb in the KppenGeiger climate classication) in
the central and southern sectors of the country and into cold summer Based on the present ndings, E. bovis and E. zuernii are commonly
temperate climate (Dfc in the KppenGeiger climate classication) in occurring in Swedish cattle herds, and cattle practitioners examining
the northern sector. For this reason, faecal sampling occurred in herds unthrifty young calves without diarrhoea or calves aged 3 to 12 weeks
from different regions of the country, but no differences were observed with diarrhoea should therefore include bovine eimeriosis as a relevant
regarding occurrence of E. bovis and/or E. zuernii. differential diagnosis to other gastrointestinal pathogens. Also, the
Whether E. bovis and E. zuernii are likely to be detected in individual presence of 9 other Eimeria spp. was found, including those character-
herds depends, as shown, on the number of collected samples, age ized by low pathogenicity in indoor housing systems (E. ellipsoidalis,
groups of the sampled calves and sensitivity of the applied analytical E. alabamensis, E. auburnensis), with mixed infections being rather com-
method. Calf diarrhoea by nature has a multi-factorial aetiology, necessi- mon. A sufcient number of faecal samples should be collected to give a
tating identication of Eimeria pathogenic species and identication of reliable picture of Eimeria infection and circulation within a given farm.
other potentially involved agents. In addition, laboratory ndings should Improvements in calf management, such as adequate colostrum alloca-
always be compared with the clinical ndings made by the practitioner tion, improved pen hygiene, all in-all out procedures for group housing
(Taylor and Catchpole, 1994), bearing in mind that both clinical and sub- pens, decreased stocking rates and strategic metaphylactic treatment
clinical eimeriosis result in negative effect on weight gain (Daugschies with available anticoccidal drugs could be sufcient to control a potential
and Najdrowski, 2005; Daugschies et al., 2007; Maddox-Hyttel and Eimeria problem. Further studies are needed to assess the role of
Vestergaard, 2002). In order to make a realistic assessment of the infec- subclinical coccidiosis in Swedish cattle farms, since indoor calf rearing
tion pressure in the calf pens, it is recommended to collect and analyse will always represent a consistent part of cattle breeding in Sweden,
particularly in dairy herds, as a consequence of the Nordic climate.

Ethical standards
Table 4
Incidences of diarrhoea as a function of age, occurrence of Eimeria bovis and Eimeria zuernii,
region and number of sampled calves (proxy for herd size). All of the studies reported herein were performed in compliance
with current applicable local laws and regulations.
Effect Number of Parameter OR p-Value
obs. estimate
Conict of interest
Intercept 0.80
High/medium Eimeria zuernii 3 2.20 9.0 0.05
Few Eimeria zuernii 25 1.08 2.9
JMD Enemark received funding for her study from Bayer HealthCare,
Individual Eimeria zuernii 19 0.48 1.6 Nordic of which he is an employee.
No Eimeria zuernii 494 0 1
Mid region 70 0.65 1.9 0.09 Acknowledgements
Northern region 79 1.26 0.3
Swea region 152 0.66 1.9
Southern region 240 1 1 Special thanks must be given to Bayer A/S, who made this prevalence
Eimeria bovis in other calves 208 0.81 2.25 0.04 study possible, to Bjrn Sandgren, Bent Nielsen and Heidi Enemark as well
Eimeria bovis in the herd 233 1 1 as The Danish National Veterinary Institute, DTU, for their valuable opin-
Age in month 0.46 0.63 b0.0001 ions. Thanks to James Mount at Karolinska Institute (Stockholm, Sweden)
No. of tested calves 0.21 0.81 0.01
for the linguistical revision of the manuscript.
20 A. Forslid et al. / Veterinary Parasitology: Regional Studies and Reports 12 (2015) 1620
Many thanks to all of the veterinary practitioners who carried out
the sampling and clinical examination on the farms.
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