Veterinary Parasitology 175 (2011) 293–299

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Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Infections with gastrointestinal nematodes, Fasciola and

Paramphistomum in cattle in Cambodia and their association with
morbidity parameters
Pierre Dorny a,b,∗ , Valérie Stoliaroff a,c , Johannes Charlier a , Sothy Meas c , San Sorn d ,
Bunthon Chea c , Davun Holl d , Dirk Van Aken e , Jozef Vercruysse a
a
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
b
Department of Animal Health, Institute of Tropical Medicine, Antwerp, Belgium
c
Division of Research and Extension, Royal University of Agriculture, Phnom Penh, Cambodia
d
National Veterinary Research Institute, Department of Animal Production and Health, Phnom Penh, Cambodia
e
European Union Livestock Programme in Cambodia on Smallholder Livestock Production, Phnom Penh, Cambodia

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

Article history: Prevalence and seasonal variations of helminth infections and their association with mor-
Received 19 March 2010 bidity parameters were studied in traditionally reared Cambodian cattle. Four villages in
Received in revised form 7 October 2010
two provinces of West Cambodia were visited on monthly intervals over a period of 11
Accepted 12 October 2010
months, during which 2391 animals were faecal and blood sampled for parasitological and
haematological examinations. The body condition score (BCS), faecal consistency (diarrhoea
Keywords:
score, DS), colour of the ocular conjunctivae (FAMACHA© ) and packed cell volume were
Cattle
determined for each individual animal. The overall proportion of samples that was positive
Nematodes
Fasciola for gastrointestinal nematodes was 52%, 44% and 37% in calves (from 1 to 6 months), young
Paramphistomum animals (6 to 24 months) and adults (over 24 months), respectively, while geometric mean
Morbidity faecal egg counts (FECs) for each of these age categories were 125, 66 and 15 eggs per gram,
Cambodia respectively. Six genera of strongyles were found in the faecal cultures, i.e. in descending
order of occurrence, Cooperia, Oesophagostomum, Haemonchus, Trichostrongylus, Mecisto-
cirrus and Bunostomum. The prevalences of Fasciola and Paramphistomum, estimated by
coprological examination, varied between 5–20% and 45–95%, respectively. Logistic mixed
models were used to investigate associations of morbidity markers with the presence of
parasite infection. A low BCS was associated with gastrointestinal nematode and liver fluke
infections, and soft faecal consistency with Paramphistomum infections. However, other
factors such as nutritional deficiencies and intercurrent diseases are likely to enhance
the effects of parasites and should therefore be considered when using these morbidity
parameters as indicators of parasitism.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction

Throughout South East Asia, infections with gastroin-

testinal nematodes and trematodes are very common in
cattle because of appropriate climatic conditions year-
∗ Corresponding author at: Laboratory of Parasitology, Faculty of Vet- round for the development and transmission of the
erinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, infective stages (Holland et al., 2000; Tum et al., 2007;
Belgium. Tel.: +32 3247 6394; fax: +32 3247 6268.
Geurden et al., 2008). The most common symptoms caused
E-mail address: [email protected] (P. Dorny).

0304-4017/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.vetpar.2010.10.023
294 P. Dorny et al. / Veterinary Parasitology 175 (2011) 293–299

Fig. 1. Map of Cambodian provinces and location of the villages of study.

by these helminth infections are: (1) anaemia due to the and Kompong Speu) (Fig. 1). These villages were consid-
haematophagous activities of e.g. Haemonchus, Mecistocir- ered to have environmental conditions and management
rus, Bunostomum, Fasciola and Paramphistomum (Van Aken practices typical for South West Cambodia. As in many
et al., 1997; Diaz et al., 2006), (2) diarrhoea because of areas is Asia animal production is an integral component
digestion/absorption disruption effects (e.g. Trichostrongy- of the mixed crop-animal farming system (Devendra and
lus, Cooperia, Oesophagostomum and Paramphistomum) and Thomas, 2002). In particular, rice production is dependent
(3) chronic weight loss and weakness due to the depression on livestock because animals are used for draught power as
of appetite and reduction of feed digestibility (Vercruysse well as for production of manure and for smallholder asset
and Claerebout, 2001; Loyacano et al., 2002). security. The main sources of nutrition for livestock are
Although some of the ‘traditional’ parasitological and the byproducts of rice, especially rice straw and rice bran
serological tests can be used to identify helminth infec- (Taucher, 2000). The main cattle breeds are the small local
tions and target anthelmintic treatments, in general, these yellow cattle (Bos indicus) and the introduced Haryana and
tests are too laborious and expensive to be applicable Brahman breeds (B. indicus) (Sothoeun, 2003). Crossbreds
for the farmer. Recently, several studies exposed the use between the yellow cattle and the introduced breeds are
of morbidity parameters, such as weight gain, anaemia, common. Cattle are usually tethered near the homestead
milk production and body condition scoring to provide and fed using cut and carry methods with available fodder
and direct treatment decisions (Vercruysse and Claerebout, and rice straw. They can also graze on communal pasture,
2001; Vercuysse, 2009). However, although morbidity including the rice fields in the period between harvest and
markers have the potential for deciding on anthelmintic planting (from end of December to May). In April, at the
treatment, the attributable part of helminths on morbidity end of the dry season, feed availability is limited and cattle
has not been determined under tropical traditional hus- suffering from nutritional stress often show signs of under-
bandry conditions with a poor plane of nutrition and where feeding (Taucher, 2000; Sothoeun et al., 2006). The mean
infections with other pathogens (blood parasites, viral and annual temperature is 28 ◦ C with minimum and maximum
bacterial infections) can cause similar clinical symptoms or averages of 20 ◦ C in January and 38 ◦ C in April, respectively.
can obscure helminth infections (Booth, 1999). The area receives a yearly average of between 1000 and
Information on the clinical importance of helminth 1500 mm of rainfall, of which 75–80% during the monsoon
diseases in Cambodia may help determine whether the that lasts from May to October (Game-T2). The monthly
assessment of morbidity can be used for identification of average rainfall during the study period is presented in
the animals suffering from helminth infections and provide Fig. 2A.
a basis for strategic control. Therefore, the main objective
of this study was to investigate the relationships between 2.2. Sampling strategy
the helminth infections in cattle present in two provinces
in South West Cambodia and body condition, faecal con- During the first visit of the villages, cattle belonging
sistency and haematocrit. In addition, the value of the to randomly selected owner families (between 40 and 80
FAMACHA© method for detecting anaemia in cattle was animals/village: up to more than 50% and about 16% of
assessed. the animal populations of the selected villages in Kom-
pong Speu and Pursat, respectively) were selected and ear
2. Materials and methods tagged. Villages were visited at intervals of 4–6 weeks;
there were 10 visits in total in each village. During each
2.1. Study area of these visits as much as possible of these selected ani-
mals were sampled and inspected. Faecal samples were
From July 2008 to May 2009 a longitudinal study was collected rectally and were transported in a cooled box
conducted in four villages from two provinces (Pursat and kept at 4 ◦ C in the laboratory until analysis within 48 h.
 P. Dorny et al. / Veterinary Parasitology 175 (2011) 293–299 295

mals and therefore more exposed to metacercariae (Molina

et al., 2005). For this purpose, a qualitative sedimentation
flotation method with a zinc chloride flotation solution was
used (Charlier et al., 2008).

2.4. Morbidity parameters

Packed cell volume (PCV) was estimated using the

microhaematocrit method. The colour of the conjunc-
tiva was classified into 5 categories according to the
FAMACHA© eye colour chart, from red (1) through red-
pink (2), pink (3), and pink-white (4) to white (5) (Malan
et al., 2001). A body condition score (BCS) from 1 to
5 was given to each animal based on referred methods
adapted to the local conditions (Edmonson et al., 1989;
McKiernan and Sundstrom, 2006) (1: emaciated; 2: very
thin; 3: thin; 4: good; 5: very good). The faecal consis-
tency (diarrhoea score, DS) was scored from normal (1) to
soft (2) or watery (3) (Perez et al., 1998; Geurden et al.,
2006).

2.5. Statistical analysis

Associations between morbidity parameters and nema-

tode faecal egg counts, and morbidity parameters and
prevalence of trematodes (Fasciola and Paramphistomum)
were investigated by logistic mixed regression models
with animal and village as random effects. The depen-
dent variable was infection status (faecal egg count < 200
EPG vs. ≥200 EPG for gastrointestinal nematodes and
positive vs. negative for Fasciola and Paramphistomum
spp.) and age, location (Pursat vs. Kompong Speu
provinces) and morbidity parameters were evaluated
as fixed effects. Variables were only retained in the
Fig. 2. Rainfall (mm) (A), geometric mean faecal egg counts (FECs) of gas- model when they had a significance level ≤ 5%. Rele-
trointestinal strongyles (GIS) for all villages and each age category (B), and
vant two-way interactions between significant parameters
prevalence of Paramphistomum and Fasciola for all villages for animals over
2 years from July 2008 to May 2009 (C). were evaluated. All analyses were performed in MLWin
v2.10.
The sensitivity and specificity of the FAMACHA© scoring
Blood was taken from an auricular capillary into a micro- method as compared to packed cell volume (PCV) values
haematocrit tube for haematocrit determination. During (=reference test) for the detection of anaemia were eval-
sampling, the body condition score, faecal consistency uated by 2 × 2 tables as previously described by Reynecke
and FAMACHA© score were recorded for each individual et al. (2009) and Di Loria et al. (2009) in sheep. Two by two
animal. None of the animals received any anthelmintic tables were created for each visit (n = 1–10). Because no
treatment prior to and during the study period. reference PCV-thresholds for anaemia are available for the
local breeds in Cambodia, different PCV-thresholds (in %)
2.3. Parasitological techniques were considered for anaemic animals: PCV = 27, PCV = 29,
PCV = 30 and PCV = 32. The FAMACHA© score was evaluated
Individual nematode egg counts were carried out to indicate anaemia when the score was ≥3 or ≥4.
on the faecal samples using the quantitative McMaster
method with a sensitivity of 50 eggs per gram/faeces 3. Results
(EPG) (Thienpont et al., 1986). Mean faecal egg counts are
presented as geometric means. Identification of the gas- 3.1. Coprological examinations
trointestinal nematode genera was achieved based on the
morphology of third stage larvae obtained from coprocul- The results of the samples collected in the four vil-
tures on pooled samples (Van Wyk et al., 2004). Samples lages are presented together because of similar climatic
were pooled per visit and per age category (calves: 1–6 and husbandry conditions (Fig. 2). During the 10 visits
months, young animals: 6–24 months and adults: over 24 a total of 2391 faecal samples were collected (mean of
months). The presence of trematode eggs was determined 250 animals/visit; range 195–321). The proportion of pos-
in faecal samples of animals of over two years only, because itive samples for gastrointestinal nematodes over the 10
they are more used in farming activities than younger ani- visits was 52% in calves, 44% in young animals and 37%
296 P. Dorny et al. / Veterinary Parasitology 175 (2011) 293–299

5
4,5
4 BCS <2Y
BCS >2Y
3,5
FS <2Y
3
FS >2Y
2,5
DS <2Y
2 DS >2Y
1,5
1

ec

ril
ch
b
pt
08

ct

ay
st

09

Fe

Ap
O
Se
gu

ar

M
ly

M
Au

ar
Ju

nu
Ja
Fig. 3. Mean of scores of body condition (BCS), FAMACHA® (FS) and diarrhoea (DS), for animals of less than two years (<2 years) and adult animals (>2
years), from July 2008 to May 2009.

in adult cattle. The geometric average faecal egg counts The monthly prevalence of trematode infections is
(FECs) for each of these age categories were 125, 66 and 15 shown in Fig. 2C. The prevalence of Fasciola and Param-
eggs per gram (EPG), respectively. Monthly average FECs phistomum varied between 5 and 20% and 45% and 95%,
showed a clear seasonal pattern: they increased from 43 respectively. For both parasites, the lowest prevalences
EPG in the dry season (November–April) to 359 EPG in the were observed in January and February, after which they
rainy season (May–October) in calves, and from 41 to 108 increased to reach the highest levels in May.
EPG in young animals during the same periods (Fig. 2B).
No seasonal effect on FECs was observed in adult ani- 3.2. Morbidity parameters
mals. The faecal cultures of the pooled samples indicated
the presence of six genera of strongyles. Cooperia was the The patterns of the mean body condition, FAMACHA©
most abundant genus (>60% of all larvae found); the other and mean diarrhoea scores during the 10 visits are shown
genera found were Oesophagostomum (15%), Haemonchus in Fig. 3 for animals younger than 2 years and adult animals.
(11%), Trichostrongylus (10%), Mecistocirrus (1%), and Bunos- For these three parameters differences between the age
tomum, which was very rarely detected (0.3%). Negligible classes were observed, i.e. younger animals having a bet-
differences in genus composition were observed between ter body condition (higher BCSs), lower FAMACHA© scores
villages, age and season. and a lower diarrhoea score.

Table 1
Results from 3 logistic mixed regression models to investigate the associations of morbidity parameters (anaemia, body condition diarrhoea score) and
presence of infection with gastrointestinal nematodes, Fasciola and Paramphistomum in cattle in SW Cambodia.

Odds ratio Confidence limits (95%) P-value

1. Gastrointestinal nematodes
Pursat 0.49 0.33–0.74 <0.001
Age 1–6 months Reference <0.001
6 months to 2 years 0.49 0.29–0.83
>2 years 0.15 0.09–0.25
Diarrhoea score Normal Reference 0.029
Soft 0.74 0.57–0.95
Liquid 0.62 0.46–0.84
PCV 0.96 0.93–0.99 0.003
Body condition BCS 1 1.19 0.20–7.29 0.003
BCS 2 2.35 1.44–3.85
BCS 3 1.41 1.00–1.99
BCS 4 1.02 0.75–1.37
BCS 5 Reference

2. Fasciola
Body condition BCS 1 8.52 1.13–64.00 0.046
BCS 2 1.71 0.86–3.41
BCS 3 1.53 0.91–2.59
BCS 4 0.96 0.58–1.57
BCS 5 Reference

3. Paramphistomum
Diarrhoea score Normal Reference
Soft 1.91 1.49–2.46 <0.001
Liquid 2.54 1.91–3.38
PCV 0.96 0.94–0.98 0.002
 P. Dorny et al. / Veterinary Parasitology 175 (2011) 293–299 297

Table 2
Sensitivity (se) and specificity (sp) of FAMACHA® related to several PCV limits, corresponding to different PCV-thresholds. The FAMACHA® score was
evaluated to indicate anaemia when the score was ≥3 or ≥4.

PCV 27 PCV 29 PCV 30 PCV 32

Famacha® score ≥ 3 Se 77.4 69.9 67.2 63.7

Sp 46.3 47.6 48.5 50.9

Famacha® score ≥ 4 Se 29.8 24.5 22.2 20.1

Sp 85.6 86.4 86.6 88.0

No seasonal differences were observed for FAMACHA© est prevalences were observed in May, which may indicate
and diarrhoea scores. The BCSs decreased from February that animals became infected when they were allowed to
until the end of the dry season (April) for all age categories. graze on rice fields after harvesting (December and March)
There was a low frequency of animals with a BCS of 1 (0.3%) (Sothoeun et al., 2006; Suon et al., 2006; Tum et al., 2007).
and 2 (7.3%); most animals had a BCS of 3 (26.4%), 4 (43.7%) The clinical condition of most animals sampled in this
and 5 (22.2%). High frequencies of FAMACHA© scores 2 study was acceptable, except for a large proportion of the
(34.5%) and 3 (40%) were recorded, while the FAMACHA© animals at the end of the dry season, which displayed low-
score 5 (very anaemic) was detected only in a few animals ered BCSs, most probably as a result of nutritional stress;
(0.7%). The determination of faecal consistency revealed and also suffered from diarrhoea. Interestingly, adult ani-
that 42.7%, 32.2% and 25.1% of the animals had normal mals had worse body condition scores, lower haematocrits
faeces, soft faeces and diarrhoea, respectively. and more frequent diarrhoea than younger animals that
The results of the logistic mixed models for associations are supposed to be more susceptible to parasitic infec-
of morbidity markers with parasitic infections are given in tions. It is likely that nutritional stress is greater in adult
Table 1 There was a significant negative relation between pregnant, lactating and/or draught animals explaining the
FECs and PCV values. BCSs were significantly related to the higher morbidities in that age group.
intensity of nematode infection, animals with low BCSs dis- However, the results of the logistic regression showed
playing higher FECs. There was also a significant relation some significant relations between morbidity parameters
between BCS and Fasciola infection (Fasciola infected ani- and parasitic infections. Both nematode and Fasciola infec-
mals having a lower BCS). Diarrhoea score and anaemia tions were associated with lower BCSs. Effects on reduced
were related to Paramphistomum infection. food intake and reduced weight gains have been described
both for nematodes and Fasciola infections (Vercruysse
3.3. Assessment of FAMACHA© for evaluating anaemia in and Claerebout, 2001; Diaz et al., 2006). Obviously, the
cattle effects on body condition that are attributable to helminth
infections and to nutritional stress cannot easily be dis-
The mean sensitivity and specificity over the 10 vis- tinguished in traditional livestock systems in a tropical
its are reported for each category of PCV and FAMACHA© environment. Poor body condition during the rainy season
scoring in Table 2. The highest values of sensitivity were is more likely to be caused by helminth infections, whereas
77.4% in the FAMACHA© categories of 3, 4 and 5 for a PCV poor nutrition is probably the main cause of weight loss
limit of 27. The highest values of specificity were 88% in the during the dry season. However, local practices, such as
FAMACHA© category of 4 and 5 for a PCV limit of 32. cut and carry during rainy season, to prevent animals from
grazing in the crop fields, may also lead to poor nutrition,
4. Discussion when not properly applied. In addition, the level of nutri-
tion can influence both the resilience and resistance of the
The results of this longitudinal survey on helminth host to parasitic infection (Coop and Kyriazakis, 1999).
infections in cattle in South West Cambodia are in line Higher nematode FECs were associated with lower PCV
with observations made in other countries of the Southeast values, which is not unexpected because we demonstrated
Asian region (Holland et al., 2000; Van Aken et al., 1998, infections with haematophagous species. A lower haema-
2000; Grace et al., 2007; Geurden et al., 2008). Overall, tocrit was also related to infections with Paramphistomum
both prevalence and intensity of gastrointestinal nema- spp. The immature stages of this parasite can be responsi-
tode infections were moderate to low. Cooperia was the ble for blood losses (Diaz et al., 2006). Surprisingly, there
dominant genus found in coprocultures, but also larvae of was no association between Fasciola infection and lower
haematophagous genera were found, such as Haemonchus, PCV. Bovine fasciolosis causes a normocytic, hypochromic
Mecistocirrus and Bunostomum. There were expected age anaemia and the most important aetiology of the anaemia
and seasonal patterns in intensity of infection: faecal egg is the chronic blood loss due to the blood-sucking activ-
counts were highest in calves and young animals and in the ity of the adult flukes and leakage of blood from the
rainy season. The prevalence of liver fluke infections in the bile duct to the intestine, which results in iron deficiency
studied region was rather low (10%), but similar to observa- (Lotfollahzadeh et al., 2009). In this study, we did not per-
tions of Tum et al. (2007) in the same provinces (Sothoeun form a quantitative assessment of fasciolosis. However, it is
et al., 2006). In contrast, the prevalence of Paramphistomum likely that infections were reasonably light and therefore,
was high: over 50% during most of the study period with did not result in anaemia. By using geographic information
an overall prevalence of 66%. For both trematodes, high- systems techniques in conjunction with determinants of
298 P. Dorny et al. / Veterinary Parasitology 175 (2011) 293–299

fasciolosis, Tum et al. (2007) designed predictive models for Acknowledgments

bovine fasciolosis in Cambodia, and concluded that Kom-
pong Speu and Pursat provinces have a moderate predicted This study was carried out within the framework of
risk of infection. the Parasitology project in Cambodia funded by the Flem-
As an alternative for haematocrit evaluation, which is ish Interuniversity Council (VLIR) and implemented at the
an invasive and rather laborious method, the FAMACHA© Royal University of Agriculture (RUA) and the National Vet-
eye colour chart has been developed and extensively eval- erinary Research Institute (NaVRI) in Phnom Penh. The
uated in sheep (Malan et al., 2001; Reynecke et al., 2009). authors would like to express their gratitude to the cattle
It is an uninvasive technique that can easily be applied owners for their kind cooperation, as well as to the techni-
by the farmer and gives a quite accurate estimate of the cians and students from RUA and NaVRI for their assistance
degree of anaemia caused by haemonchosis. Few stud- during the field sampling and the laboratory analysis.
ies have demonstrated the usefulness of the FAMACHA
method for detecting anaemia in cattle. Grace et al. (2007)
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