Species and Prevalence of Rabbit Gastrointestinal Parasites in

Berastagi Farm Karo District, North Sumatra, Indonesia

Masitta Tanjung and Putri Maura Rangkuti

Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Sumatera Utara, Medan, Indonesia

Keywords: Eimeria, flotation, Passalurus, rabbit, Strongyloides.

Abstract: Parasitic infection is one factor which hinder the success of rabbit breeding.The aims of this study was to

identify the species, prevalence, and intensity of parasitic attacks. The sample used is feces from rabbits on

the Berastagi farm, Karo District, Sumatera Utara. Rabbit feces samples were divided into young rabbits

(age>three months) as many as 15 rabbits and adult rabbits (aged> 3 months) as many as 25 rabbits. Sample

examination was carried out at the Parasitology Laboratory, Medan Veterinary Hall, Sumatera Utara using

the flotation method.The results showed that in young rabbits, threespecies of parasites were found with

their percentage of prevalences, namely Eimeria sp. (40%, common) and intensity of attacks 3,966 (super

parasitic infections); Strongyloides sp. (20%, often) and the intensity of attacks 233 (very heavy parasites);

and Passalurus sp. (13.33%, often) and intensity of attack 450 (very heavy parasites).In adult rabbits, only

onespecies of parasite was found i.e. Eimeria sp. (12%, often) and intensity of attacks of 900 (very heavy

parasites).Young rabbits have a greater risk of being infected with parasites than adult rabbits.

1 INTRODUCTION

Parasites often attack rabbits from both ectoparasites,

i.e. mites, fleas and endoparasites, i.e. helminths and

protozoa. Endoparasites that attack rabbits, both

worms and protozoa are generally gastrointestinal

parasites (parasites in the digestive tract).Worms that

commonly attack the digestive tract of rabbits are

Passalurusambiguus and Taeniapisiformis, while

protozoa which often attack the rabbit's digestive

tract are Eimeria sp. and Enchepalitozooncuniculi

(Harcourt, 2002). Endoparasites in the digestive tract

generally take part in the host's nutrients, consume

host tissues or use digestive organ cells to complete

the phase of their life (Levine, 1994).

Eimeria causes coccidiosis. Coccidiosis has

spread in almost all the world (Flynn, 1973). This

disease is pathogenic and causes 48% death of

livestock rabbits in Pelotas, Brazil (Varga, 1982).

Mortality of coccidiosis in various speciess of

animals ranges from 5-100% and can cause

economic losses in the form of weight loss,

decreased food efficiency and inhibits weight gain.

As many as fifty wild rabbits from urban areas

near Aachen (Germany) found nine species of

parasites consisted of four endoparasite species and

five ectoparasite species (Frank, et al., 2013).Wild

rabbits on the island of Tenerife (Canary Islands)

collected in 1998 and 2000 in seven zones based on

altitude and purpose, found five parasitic species

namely, three cestodes (Taenia pisiformis (larvae),

Andryacuniculi and Mosgovoyiactenoides) and two

nematodes (Trichostrongylus retortaeformis and

Passalurus ambiguus). Taenia pisiformi sshowed

anuneven distribution with a significant prevalence

within zones. Andrya cuniculi were only found in

two zones and there were no significant differences

in prevalence values.

Mosgovoyia ctenoides have a broad distribution

with a significant prevalence, which is higher in the

north compared to the southern zone.

Trichostrongylus retortaeformis does not exist at the

bottom of the southern zone of the island.

Passalurus ambiguus was found in all zones without

significant differences in the prevalence of infection.

Differences in prevalence tend to be caused by

environmental factors in the case of T.

retortaeformis and in the absence of compatible

hosts and intermediates. All parasitic species in

Tenerife are identified as common helminths in the

Iberian Peninsula (Foronda, et at., 2003).

Tanjung, M. and Rangkuti, P.

Species and Prevalence of Rabbit Gastrointestinal Parasites in Berastagi Farm Karo District, North Sumatra, Indonesia.

DOI: 10.5220/0008551601930198

In Proceedings of the International Conference on Natural Resources and Technology (ICONART 2019), pages 193-198

ISBN: 978-989-758-404-6

193

2 MATERIALS AND METHOD

The samples used in this research were feces from

15 puppies (ages 0-3 months) and 25 adult rabbits

(age>three months). Feces collection was carried out

at Brastagi ranch, Karo District, Sumatera Utara.

Feces were inserted into the sample cup, covered

with plastic and labeled 'Sp1' in the first feces

sample and so on. The sample was put into a cool

box and taken to Parasitology Laboratory, Medan

Veterinary Hall.

The method used in this research was the

flotation method. Feces was put into a test tube

measuring 5 ml as much as 10 g; then the Saturated

NaCl solution was poured into a tube to 2.5 ml.

Feces homogenized using an applicator. The test

tube was filled with a saturated NaCl solution to the

brim. A glass cover was placed above the mouth of

the test tube carefully. The glass cover was left idle

for 10 minutes and make sure it came into contact

with the liquid without air bubbles. The glass cover

was lifted carefully, a drop of liquid must be left on

the glass cover. The glass cover was placed on an

object glass then the preparation was observed under

a microscope. Identification was based on Yamaguti,

(1963; 1971) and Kabata (1992). The rate of

infestation by these parasites was calculated

according to the standard method: Prevalence, mean

intensity and abundance (Margolis, et al. 1982).

Prevalence and intensity levels were categorized

based on Williams & Williams (1996).

3 RESULTS AND DISCUSSION

3.1 Identification of Gastrointestinal

Parasites

Based on the examination results of 40 samples of

rabbit feces on the Berastagi ranch, Karo District,

Sumatera Utara by floatation method, threespecies

of parasites were obtained which can be seen in

Table 1.

Based on Table 1, it can be seen that 2 groups of

parasites were found in rabbit feces. The first

parasitic group came from the protozoa group,

Eimeria sp. found in feces with the oocyst stage.

Oocyst Eimeria sp. found in both puppies and adult

rabbits.The second parasitic group came from the

nematode group, namely Strongyloides sp. found in

the egg stage and Passalurus sp. which was in the

larvae stage, where both speciess of nematodes were

found only in baby rabbit feces.

Fifty wild rabbits in urban areas near Aachen

(Germany) nine species of parasites were found.

Four endoparasitic species consisting of Cittotaenia

denticulata, Graphidium strigosum, Passalurus

ambiguus, and Trichostrongylus retortaeformis and

five species of ectoparasites: Cheyletiella

parasitivorax, Ixodes ricinus, Leporacarus gibbus,

Haemodipsus ventricosus, and Spilopsyllus cuniculi.

When compared with the International survey found

the prevalence and mean intensity of C. denticulata,

G. strigosum, P. ambiguus, and T. retortaeformis

parasites (Frank et al., 2013). The rate of infection in

crossbreeding rabbits was 56.3%. Oocyst Eimeria sp.

(52.7%) and P. ambiguus eggs (3.6%) were detected

in rabbit manure (Sürsal et al., 2014).

As many as 71 wild rabbits (Oryctolagus

cuniculus) aged around 5 to 12 months from the

province of Fars, south of Iran. The sampling of

healthy rabbit feces samples was conducted directly

from the rectum and the oocyst was isolated using

sedimentation and salt-floatation techniques. Spore

forming oocysts were identified based on

morphology and biological characteristics.Twenty-

two (31.0%) rabbits were positively infected with

Eimeria and six species including Eimeria perforans

(18.3%), E. magna (16.9%), E. media (14.1%), E.

irresidua (11.2%), E. flavescens (4.2%), and E.

coecicola (2.8%). Eighty-six percent of infected

rabbits show mixed infections with two or three

Eimeria species.Lack of clinical signs may be due to

ecological and environmental conditions of rabbit

habitat, especially dry and hot. Also, immunity is

caused by long-term exposure to low-dose oocysts

which may have an important role in disrupting the

parasite development cycle and preventing acute

coccidiosis (Razavi et al., 2010).

Table 1: Species of Gastrointestinal Parasites in Rabbits from Berastagi Ranch, Karo District, Sumatera Utara.

Group

Species

Stadium

Category

Puppies (0-3 Months)

Adult (>3 Months)

Protozoa

Eimeria sp.

Oocyst

√

Nematode

Strongyloides sp.

Egg

√

Passalurus sp.

Larvae

√

Description: (√): exists, (-): none

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3.2 Prevalence of Gastrointestinal

Parasites

The prevalence of parasites based on the

examination results of 40 samples of rabbit feces on

the Brastagi ranch, Karo District, Sumatera Utara

can be seen in Table 2. Based on Table 2, the

prevalence value of the three species of

gastrointestinal parasites in baby and adult rabbits is

presented. The highest parasitic prevalence was

found in Eimeria sp. in baby rabbits with a

prevalence value of 40% and in the 'commonly'

category. Prevalence value of Eimeria sp. in baby

rabbits showed a higher number than the prevalence

of Eimeria sp. in adult rabbit which was worth 12%

and included in the 'often' category, this was due to

Eimeria sp. have a direct life cycle which means that

it does not require an intermediary host to cause

constant infection of vulnerable animals such as

younger animals (Rodríguez-Vivas et al., 1996).

Eimeria sp. has the highest maximal prevalence

of 9% in adult pigs without clear geographical

differences (Roepstorff, et al., 1998). According to

Yadav, et al (2006) the prevalence of Eimeria sp

from cow and goat feces was 6.73%.Prevalence

studies were also reported from gastrointestinal

parasites of cows, buffaloes, sheep, goats and

poultry in the Korutla region of Andhra Pradesh's

Karimangar (Telangana region) district. The highest

prevalence was from Toxocara vitulorum in cattle

and buffaloes with 16.7%, respectively.Prevalence

of Amphistome, Eimeria, Moniezia, Strongyle,

andTrichuriswere less than 11% while prevalence of

Capillaria sp. and Eimeria sp. in poultry were less

than 7.0%. The overall prevalence of gastrointestinal

parasites in cattle and buffaloes was 40.0%, 38.7%

in sheep and goats, and in poultry was 13.0%. Two

Eimeria species were identified from sheep, namely

Eimeria granulosa and Eimeria parva (Murthy and

Rao, 2014).

Total 580 goats were randomly examined in

representative areas of five Zimbabwean regions

during the dry and rainy season. Blood and feces

samples were collected from each animal and

eggs/oocysts per gram of feces (epg/opg) were

measured usinglaboratory culture and packed cell

volumes (PCV).Factors that influence parasitic

infections were identified. The highest prevalence

was identified fromEimeriaoocysts with 43%,

followed by Strongyles with 31%, and a few

trematodes and cestodes. The parasites were

identified were Haemonchus, Strongyloides and

Oesophagostomum. Region, season, sex and age

significantly influence the gastrointestinal infection

pattern (P <0.05). Statistical analysis showed that the

composition of parasites varied by region and the

impact of risk factors was also different.The

infection risk was very high for samples of goats in

Natural regions (NR) I, II, III (OR = 6.6-8.2; P

<0.05) compared to those in NR IV and V. The

highest worm infections and Eimeria were observed

in the rainy season vs the dry season (P <0.05).

Their study reported that newborn or young animals

were more susceptible to parasitic infections (P

<0.05) and the prevalence was considerably intense

in males than females, with the possibility of three

times infection to males than to females (P <0,0001)

(Zvinorova, et al., 2016).

The prevalence of puppies rabbit parasites was

higher than the prevalence of parasites in adult

rabbits. The high prevalence of parasites in baby

rabbits was caused by the immunity of young

animals is still less effective and is still in a state of

weaning from the mother. Based on the survey

results in the field, still found puppies-rabbits that

were not weaned at the time they were supposed to,

this was due to the lack of available cages. Levine

(1990) stated that rabbits should be weaned as early

as possible and separated from their parents, this is

because adult rabbits are a source of infection for

puppies rabbits.

Table 2: Prevalence of Gastrointestinal Parasites in Rabbits from Berastagi Ranch, Karo District, Sumatera Utara.

Species

Category

Puppies (0-3 Months)

Adult (>3 Months)

Prevalence

Category

Prevalence

Category

Eimeria sp.

40%

Commonly

12%

Often

Strongyloides sp.

13,33%

Often

Passalurus sp.

20%

Often

Description: (-): none

Species and Prevalence of Rabbit Gastrointestinal Parasites in Berastagi Farm Karo District, North Sumatra, Indonesia

195

Table 3: Intensity of Gastrointestinal Parasites in Rabbits from Brastagi Ranch, Karo District, Sumatera Utara.

Species

Category

Puppies (0-3 months)

Adult (>3 months)

Intensity

Category

Intensity

Category

Eimeria sp.

3.966

Super parasitic infections

900

Very heavy parasite

Strongyloides sp.

233

Very heavy parasite

Passalurus sp.

450

Very heavy parasite

Description: (-): none

A total of 960 goat feces samples were sampled and

processed by sedimentation and salt-flotation

methods.The study reported percentage of

prevalence reached 94.48%with dominant parasitic

genus from Coccidia (82.4%), Strongyles (69.27%),

Amphistomes 22.71%, and lesser parasites, i.e.

Fasciola, Moniezia, Schistosomes, Strongyloides

Trichuris. The parasites showed a higher infection

during rainy season than in winter season.

The incidence of gastrointestinal parasitism was

found to be higher in lambs (96.25%) compared to

goats (93.89%) (Singh, et.al., 2015).The next highest

prevalence value was Passalurus sp. in puppies

rabbits with a prevalence value of 20% and in the

'often' category, whereas in adult rabbits this worm

was not found, this can be caused by the Passalurus

sp. has a direct life cycle which means it does not

require an intermediary host to be infective, hence

the babies are more susceptible to infection. The

next prevalence is Strongyloides sp. with a value of

13.33% and included in the 'often; category.

Based on the survey results on the ranch site,

rabbit cages at the research site are usually cleaned

at least once a day, but feces that is not immediately

cleaned when the rabbits are defecated causes the

worm larvae to have the chance to infect rabbits.

Levine (1994) stated that infective larvae of

Strongyloides sp. infect animals by penetrating the

skin and having a very short premenstrual period

hence regular cleaning of the cage once a day still

allows the occurrence of strongyloides infection.

Based on the survey results at the research site,

rabbit feed is generally a vegetable crop residue, in

contrast to rabbit breeders in the lowlands who

generally feed rabbits in the form of pellets and

weeds, this is because Brastagi is a fertile area so

vegetables are very easy to obtain.The time for

collecting the forage varies, this is due to managers

adjusting the time for taking forage with farmers

harvesting the vegetables, but because farmers in

Brastagi generally harvest vegetables in the morning,

taking forages used to feed rabbits is often done in

the morning.

The high prevalence rate of parasites can be

caused by the taking of forages by farmers

conducted in the morning and evening, where at that

time forages tend to be polluted which increases the

likelihood of rabbits being attacked by disease.The

cause of low prevalence in an area is probably

caused by taking food during the daytime in which

the parasite will die when exposed to sunlight even

though sanitation in the area is classified as dirty.

Moist forage drying needs to be done to minimize

contamination of forages by parasites.

3.3 Gastrointestinal Parasite

Intensity

The intensity of parasitic attacks based on the

examination results of 40 rabbit feces samples on the

Brastagi ranch in Karo District, Sumatera Utara can

be seen in Table 3.

Based on Table 3, the intensity value of the three

speciess of gastrointestinal parasites in puppies and

adult rabbits. The highest parasitic intensity was

found in Eimeriasp. from baby rabbits with an

intensity value of 3966 and was in the category of

'super parasitic infections'. The intensity value of

Eimeria sp. in baby rabbits showed a higher

intensity value than the intensity of Eimeria sp. in

adult rabbits which was worth 900 and included in

the category of 'very heavy parasite'.Observations on

feces samples from 197 cows, 37 horses, 11 sheep,

25 pigs, 21 dogs, one cat and 62 chickens from

livestock of 10 large private properties and 75 from

rural settlements in the Atlantic Rain Forest in Brazil

found Eimeria sp. appear in almost all hosts, except

horses, dogs and cats (Sevá, et al., 2018)

The intensity value is a degree of parasite species

that infects an animal. Some rabbits with high

parasitic intensity show less healthy symptoms such

as less weight, diarrhea and bloody feces. Some

rabbits were even found dead.Based on the interview

results with livestock managers, the death of rabbits

is a common thing, especially at the age of less than

one month. Symptoms of unhealthy and death in

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rabbits may be caused by parasites that infest the

rabbit too high.

According to Barnes et al. (1984), a disease

caused by Eimeria sp. can be acute or chronic

depending on the number of oocysts that are

swallowed by the host.In infections with less than

150 infective oocysts there will be a bleeding point

on the mucosal surface of the cecum with a slight

discoloration of the cecum wall. The dose of 150-

500 oocysts will result in bleeding, injury and

thickening of the cecum wall.In 1000-3000

infections of oocysts will potentially cause death in

animals. Infection of 5000 or more oocysts can

cause the highest mortality in two weeks old host.

Some other infected rabbits did not show any

clinical symptoms; this may be due to the rabbit's

immune system that is different in each. Antibiotics

and vitamins treatment was also one of the factors

that cause rabbits to look healthy even though they

were attacked by quite severe parasites.

The next highest intensity value was Passalurus

sp. with an intensity value of 450 and was in the

category of 'very heavy parasite'. The lowest

intensity value was found in Strongyloides sp. with a

prevalence value of 233 and also included in the

category of 'very heavy parasite'.

Cheng (1973) stated that infection by the

Strongyloides sp. is rare except in humid

conditions.Based on the measurement results, the

location of rabbits ranch in Brastagi has a moderate

temperature of 21

C and the humidity is quite high

at 71.6%. Larvae that live in humid conditions will

produce large numbers of infective larvae.

4 CONCLUSIONS

The species of gastrointestinal parasites found in

rabbit feces on Brastagi ranch, Karo District,

Sumatera Utara were three species, namely: Eimeria

sp. found in puppies rabbits (ages 0-3 months) and

adult rabbits (> 3 months old), Strongyloides sp. and

Passalurus sp. were only found in baby rabbits.

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