O nline J ournal of A nimal and F eed R esearch

Volume 10, Issue 5: 216-230; September 25, 2020

SYSTEMATIC REVIEW ON GASTROINTESTINAL HELMINTHS

OF DOMESTIC RUMINANTS IN ETHIOPIA

Tewodros FENTAHUN

Unit of Biomedical Sciences, College of Veterinary Medicine and Animal Sciences, University of Gondar, P.O.Box 196, Gondar, Ethiopia

^Email: tedyvet@gmail.com;

: 0000-0002-2955-5638

^Supporting Information

ABSTRACT: This systemic review was conducted to identify, critically assess, and bring together available data

from primary researches conducted so far on gastrointestinal (GI) helminthes of domestic ruminants in Ethiopia.

In the country, GI helminths of domestic ruminants have been identified; examined and informative statistics

has been extracted since a few decades ago. For this review, relevant articles were retrieved from English

databases: PubMed, Google Scholar, Science Direct, Web of Science and Scientific Information Database (SID).

Additional studies were recognized by scanning the African Journal Online (AJOL) that includes the Ethiopian

Veterinary Journal and Bulletin of Animal Health and Production. Out of retrieved (n=154) articles, thirty three

(n=37) articles which fulfilled the eligibility criteria were selected. Accordingly, twenty three GI helminthes

species which belong to the three classes of helminthes have been found to occur in domestic ruminants in the

country. The main genera reported so far are Haemonchus, Strongyloides, Trichostrongylus, Oesophagostomum,

Bunostomum, Fasciola, Monezia and Paramphistomum whereas, Haemochus contortus, Moneizia expansa and

Fasciolahepatica are the most frequently reported species from Nematode, Cestode and Trematode classes

respectively. The overall GI helminths prevalence ranged from 2.3% to 100% were reported. Simple flotation,

sedimentation, modified McMaster technique and faecal culture are the most common and routine diagnostic

methods which have been used in the country. Management aspects like husbandry practices, climate and host

influences are found to be the principal contributing factors that affect GI helminths infections. So far, the

control of GI parasites in the country is mainly focusing on the use of anthelmintics. Consequently, due to the

lack of effective control strategies, antihelmintics are exclusively used which result in antihelmintics resistance.

Generally, occurrence, epidemiological features, realistic control strategies, common diagnostic procedures and

frequently encountered species are reviewed. Finally, the relevance of epidemiological knowledge and the

development of efficient, sustainable and conventional control measures which cover wider ago-climatic zones

of the country are suggested for controlling GI helminths infections and should be assessed timely.

Keywords: Anthelmintics, Domestic ruminant, Ethiopia, Gastrointestinal helminthes.

INTRODUCTION

As a result of having different agro-ecological zones and favorable environmental situations in Ethiopia, the country is

believed to be endowed numerous livestock species and suitable for livestock production. It has the largest livestock

population in Africa (Tilahun and Schmidt, 2012; CSA, 2013 ). According to CSA (2013) report, an estimated statistics

showed that about 54 million cattle, 25.5 million sheep and 24.06 million goats are found in the country. Of the total

cattle population, 98.95% are local breeds and the remaining are hybrid and exotic breeds. Furthermore, 99.8% of the

sheep and nearly all goat population of the country are local breeds (CSA, 2013 ).

However, diseases have numerous negative impacts on production and productivity. Among diverse animal diseases

encountered in the country, helminthes infections remain one of the most important limiting factors and a bottlenecking

production and productivity these days (Elsa et al., 2012). By chance, the gastrointestinal tract of ruminants harbors

variety of parasites particularly helminthes which can cause both clinical and subclinical parasitism. As stated by Lebbie

et al. (1994), GI helminthes infections are of a global concern for livestock industry, which have devastating impact in

Sub-Saharan Africa in general and in Ethiopia in particular as a result of wider range of agro-ecological factors which are

fitting for diversified hosts and parasite species. Hence, gastrointestinal (GI) helminthiasis has become among the most

important diseases encountered by livestock sector of Ethiopia and has been considered to be one of the major

constraints in the development of the sector (Regassa et al., 2006 ). In Ethiopia, helminthiasis is responsible for 25%

mortality and 3.8% weight loss in highland sheep (Bekele et al., 1992).

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

According to Zahid et al. (2005), the helminthes infections of ruminants are mostly caused by nematodes like

Strongyliodes spp., Ostertagia Spp., Bunostomum and Trichuris spp.; Cestodes such as Moniezia spp., Taenia spp. and

Trematodes such as Paramphistomum spp., Fasciola spp. and Shistosoma spp. Perry et al. (2002) reported that GI

nematodes have been ranked highest on globalindex with Haemonchus contortus on top. Moreover, Trichostrongyloidea

that include genera such as Haemonchus, Trichostrongylus, Cooperia, and Nematodirus, and the Strongyloidea and

Ancylostomatoidea with Oesophagostomum and Bunostomum, are the economically most important and widely prevalent

GI nematodes (Takele et al., 2013; Winter et al., 2018 ). In addition, such a pervasive occurrence of the metacestodes;

Cysticercus ovis and Cysticercus tenuicollis; Hydatid cyst (E.granulosus); Fasciola hepatic and Fasciola gigantic are most

prevalent in the country and considered to be of great economic importance (Lemma et al., 1985; Regassa et al., 2009;

Nigatu et al., 2009; Kebede et al., 2009; Feyesa et al., 2010; Nigatu, 2010; Endale et al., 2013; Abebe et al., 2015;

Beyene and Hiko, 2019 ).

There are many associated risk factors influencing the occurrence and epidemiology of GI helminthes including age,

sex, weather condition and husbandry or management practices (Khan et al., 2009). Factors such as host age,

physiological status, breed, parasite species involved, and the epidemiological patterns (husbandry practices and climate

variables) determine the degree of infection (Tembely and Hansen, 1996; Menkir et al., 2007 ). In Ethiopia, several studies

have been conducted on ruminant helminthiasis in various regions reporting a prevalence ranged from 2.3–100% (Fikru

et al., 2006; Abebe and Esayas, 2001; Yirsaw and Zewdu, 2015 ).

A number of published research reports have been found on GI helminthes of domestic ruminants in Ethiopia.

However, these reports are found in a separate and unorganized way. So, comprehensive and well organized

documentation about GI helminthes of domestic ruminant in the country is essential to support researchers, professionals

and policy-makers to develop further actions on the control and prevention strategies. Therefore, the aim of this

systematic review was to identify, assess critically, and bring together available data from primary research conducted so

far on gastrointestinal (GI) helminthes of domestic ruminants in Ethiopia.

MATERIALS and METHODS

Source, selection strategies and protocol

This systematic review was carried out on GI helminthes of Ethiopian ruminant using available electronic and non-

electronic databases. The electronic search was used as the primary search method. The main electronic databases used

were PubMed, Google Scholar, Science Direct, Web of Science, Scientific Information Database (SID) were accessed from

University of Gondar, Ethiopia. Relevant studies have been identified from English databases in Pub Med, Google Scholar,

Science Direct, Web of Science, Scientific Information Database (SID). Additional studies were recognized by scanning the

African Journal Online (AJOL) that includes the Ethiopian Veterinary Journal and Bulletin of Animal Health and Production.

Moreover, complete and congress articles like original descriptive studies (designated as cross-sectional study) in sheep,

goats and cattle were also considered. Epidemiological parameters such as prevalence of GI helminthes infection among

sheep, goat and cattle, and main contributing factors like age, sex, and geographical sub-regions of Ethiopia were

considered thoroughly. An intensive data searching was made to collect available information (Figure 3). The searching

strategies used were combining the phrases close to GI helminths in large and small ruminants in Ethiopia as indicated in

Figure 1. Searches were restricted to peer-reviewed articles published nationally or internationally in English language.

Figure 1 - A diagram showing a strategy for words combination to access relevant articles.

217

Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Figure 2- Map of Ethiopia showing study sites of GI helminthes of domestic ruminants.

Figure 3 - Flow diagram describing the study design process and literature search on GI helminthes in domestic

ruminants.

Data type and collecting methods

Published papers were scanned by quick reading to select relevant articles. Important articles were defined and

included in the current review as one that contained information on GI helminthes of cattle, sheep and goat in Ethiopia.

References of all relevant articles were searched to identify articles that were missed by the electronic search. Any

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

identified article was subjected to the same inclusion process as a data type. Following that all relevant articles were

reviewed, extracted and compiled in a searchable database (Microsoft Access software, ver. 2007). Extracted information

included authors name, study sites, year of the study commenced and ended, year of publication, study design, species of

animals, sampling procedure, number of animals selected, body condition, sex, altitude of the study site, laboratory

procedure to detect the parasite, testing methodology and prevalence of GI helminthes reported including their associated

risk factors.

Reports collected on GI helminths in Ethiopia

The initial electronic searches yielded a total of (n=154) studies. After scrutinizing these and eliminating duplicates,

thirty three (n=37) were considered (Figure 4) including thesis containing relevant information concerning GI helminths of

ruminants in Ethiopia. This review work documented that of the relevant articles about 8% (3) were not retrieved by any of

the search engines, 19% (7) were retrieved by a single search engine, 27% (10) by two, 16% (6) by three and 30% (11) by

all four databases. Providing a balanced and an impartial summary of the topic using these representative studies was at

the core of this review. No restrictions other than identifying ovine, caprine and bovine GI helminthes in Ethiopia were

imposed on the inclusion criteria. This minimized literature selection bias and provided an exhaustive list of GI helminths.

However, for factors associated with domestic ruminant GI helminthes in Ethiopia, strict inclusion criteria were applied in

order to only select the critical studies. In order for the current review to be critically appraised, repeatability was crucial.

This was achieved by documenting every step of the review process.

Number of articles

1988 1990 1998 2001 2002 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015

Year of Publication

Figure 4 - Frequency of articles relevant to the systematic review on GI helminths of domestic ruminants in Ethiopia.

Occurrence and spatial distribution

The present review work revealed that the occurrences of GI helminthes infections were reported in different parts of

the country (Figure 2). The prevalence of GI helminthes is summarized in table 1. The majority of the prevalence studies

were specific on some helminthes genera like Strongyles, Fasciola, Shistosoma and some families like GI nematodes,

Trematodes and Cestodes. However, adequate sources were not accessed compared to the number of studies done on

specific species and families of the GI helminthes of domestic ruminants. In addition, most studies are based on the

coprological examinations and few studies were conducted on abattoir surveys in the country.

According to the result obtained from the review, the overall prevalence of GI helminthes is ranged from 13.2% in

Awash River Basin (Afar region) to 81.5% in Debre Zeit/Bishoftu (Bersissa et al., 2011; Moti et al., 2013 ). Furthermore,

the review underlined that the majority of the identified species are found from nematodes and the lowest from Cestode.

On the other hand, Haemochuscontortus, Moneiziaexpansa and Fasciolahepatica are the predominant species from

Nematode, Cestode and Trematode classes respectively. Furthermore, Nematodirus spp., Toxocaravitulorum and

Schistosoma spp. are less prevalent (Table 2). In Ethiopia the majority of the studies were focusing only on small

ruminants’ GI helminthes than large ruminants. Therefore, the highest prevalence of the parasite was reported from

sheep (91.2%) in Gode (Ogaden), Southern Ethiopia than cattle (21.9%) in Nekemete in Western part of Ethiopia (Table 1).

On the other hand, most Abattoir survey reports have also shown a status of GI helminths of cattle than small ruminants.

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Table 1 - List of selected studies on GI helminthes of domestic ruminants in Ethiopia

Study animals and Sample size

Prevalence (%)

Diagnostic

technique

Study site(s)

Study period

Sample

Author(year)

Sheep

Goat

Cattle

Total

Sheep

Goat

Cattle

Total

Adama

Adami Tulu

Addis Ababa

560

208

499

852

1152

499

560

Nov2007-Apr2008

Jul1997-Jun1998

Sep 1985 - Jun 1986

PME

29.3

19.6

6.7

45.5

46.8

Liver

Getawa et al. (2010)

Etana (2002)

Bekele et al.(1988)

Temesgen and Walanso

(2015)

45.5

19.6

Ambo

120

Feb-May 2013

DS,FL,SD

47.8

53.3

SD,FL,

MM,PME

MMM

EAC

63.6;

Arba Minch

241+20

357+25

598 + 45

Jan2010-Aug 2011

79.7; 85

70.1;

F, GIT

Nejib et al. (2014)

Asella

Awash

384

408

3,697

Nov 2013-Apr 2014

Nov 2008-Apr 2009

Jan-Dec 2005

May 2005

68.1

13.2

Addisu and Berihu (2014)

Diriba et al. (2013)

Ahmed et al.(2007)

408

3,697

68.1

13.2

Bahir Dar

340

384

420

384

10.6

34.05

Liver

Nigatu et al. (2009)

- Dec2006

10.9;

16.9

32.3

31.5;

45.3

39.95

64.2

Ayalew and Endalkachew

(2013)

Fikirtemariam et al. (2013)

Yitayal et al. (2015)

Moti et al. (2013)

768

Nov2010-March 2011

SD, PME

F, Liver

Bahir Dar

Bedele

Bishoftu (Debre Zeit)

384

500

4134

384

500

2688

222

Nov2008-March2009

Nov2013-April 2014

Oct 2011-March 2012

Dec2005 - Jun 2006

Nov2007-Apr2008

SD, PME

SD, FL, MM

PME

39.95

32.3

64.2

F, Liver

Liver

1152

157

1536

58.5

81.0

43.8

83.0

Jibat et al. (2008)

Bersissa et al. (2011)

FL,SD, CC

81.5

Bishoftu (Debre Zeit)

326

Nov2011-Apr 2012

FL, SD,

Cheru et al. (2014)

Debre Berhan

Dembi Dolo

Dessie

2500

255

510

257

2500

757

930

1987

2003-2004

Nov2011-Mar 2012

SD,FL

DS, SD,FL, MM

PME

75.3

21.04

50.2

69.6

F, PME

OM, PE, Liver,MS

Njau et al.(1990)

Fikru et al.(2006)

Abebe et al.(2015)

245

420

84.1

27.61

26.4

24.6

Dire Dawa

425

420

845

Nov2011-April 2012

PME

22.8

Liver, PE OM

Endale et al. (2013)

Durbete

Gondar

Gondar, Finote Selam, Injibara

202-

458

100

330

22,755

532

558

22,755

Oct 2014- Apr 2015

Nov-Jan 2008

Sept 2002-2007

SD, FL

PME

2.3

46.07

24.6

79.5

26.9

47.67

79.5

Liver

Yirsaw and Zewdu (2015)

Shimelis et al. (2011)

Nigatu (2010)

Haremaya, Harar, Dire Dawa,

Jijiga

655

632

1,287

May 2003-Apr 2005

PME

GIT

Menkir et al. (2007)

Hawassa

Jimma

Kelala

Kombolcha

284

180

230

226

132

510

632

312

210

384

400

Nov2008-Feb 2009

Dec2008 – Mar 2009

Jan-Jun 2006

Nov2008-Apr 2009

Sept1997-Apr1998

2011

MMM

PME

47.2

91.1

38.9

87.1

52.6

77.6

Liver

Abebe et al. (2010)

Feyesa et al. (2010)

Thomas et al. (2007)

Hailu et al. (2011)

Tesfaye (1998)

Fufa et al. (2012)

Getachew and Ashwani

(2013)

632

210

154

400

52.6

77.6

FL,SD, MMM

FL, SD

PME

Liver

Mekelle

1023

Nov2007 - Feb2008

2007/8

PME

7. 23

22.1

7. 23

22.1

Liver

Mekelle, Adigrat, Axum,

Humera, Maichew, Shire

Metehara, Semera, Jigjiga

Nekemete

5,194

Kebede et al. (2009)

183

384

Nov1998-Apr 1999

Nov2011-March 2012

MMM, PME

PME

97.03

100

F , GIT

GIT

Abebe and Esayas(2001)

Alula et al. (2013)

384

21.9

Ogaden-Gode

Wolaita Soddo

Wukro

114

415

196

415

384

Aug2003-March 2004

Nov2007 - Apr2008

Nov 2013-Apr 2014

PME

91.2

82.9

11.3

Liver

Kumsa and Wossene (2006)

Regassa et al. (2009)

384

40.9

Lidya and Berihun (2015)

^_: No information available; ST=Study design; PME=Postmortem examination; CS=Cross sectional; SD=Sedimentation, FL=Flotation, MM=Mc Master; DS=Direct Smear; MMM=Modified Mc Master; F= Faeces; A=Abomasum; GIT=Gastrointestinal

content; EAC= Ethyl-acetate Centrifugation; PE=peritoneum; OM=Omentum; MS=Mesentry; RT= Retrospective

220

Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Table 2 - GI helminthes species/genus composition; collected from each selected studies in Ethiopia.

Species of parasite identified (%)

Altitude

of study

area

Author

(year)

Location

Adama

Species of animal

Nematode

Cestode

Trematode

Sheep

Goat

Cattle

Sheep

Goat

Cattle

Sheep

Goat

Cattle

Getaw et al.

(2010)

852

Hydatid cyst

40.0

55.6

37.1

1770

H.contortus

30.3

16.4

13.8

2.2

2.8

5.0

Strongyloidesspp.

Trichostrongylus spp.

Trichuris spp.

Nematodirus spp

Chabertia ovina

Bunostomum spp.

M. expansa

M. benedeni

14.6

4.0

Adami Tulu

900

Etana (2002)

5.4

T.hydatigena and

Hydatid cyst

Addis

Ababa

Bekele et al.

(1988)

Temesgen and

Walanso (2015)

18.6

2,326

2185

Strongyles spp.

47.8

53.3

Fasciola spp.

4.4

6.7

Ambo

H.contortus

Trichostrongylus spp.

Teladorsagia spp.

T.colubriformis

Arba Minch

1400

Nejib et al. (2016)

Haemonchus spp.

Ostertagiaspp

Oesophagostomumsp

Strongloid spp.

Trychostrongylusspp

Hemonchusspp.

Bunostomum spp.

Strongylesspp

Strongyloidesspp

Trichurisspp

1.8

1.3

2.6

3.6

11.7

4.4

1500-

2300

Addisu and Berihu

(2014)

Assela

Asella

64.0

7.4

3.7

2500-

3000

Diriba et al.

(2013)

Ahmed et al.

(2007)

Nigatu et al.

(2009)

Fasciola spp.

13.2%

Awash

550-850

1784

E. granulosus

25.0

16.1

Bahir Dar

Ayalew and

Endalkachew

(2013)

F. hepatica and

F.gigantica

16.9

45.31

Bahir Dar

1784

F.hepatica

F.gigantic

Mixed

89.7

3.63

6.67

Fikirtemariam et

al. (2013)

Yitayal et al.

(2015)

F. hepatica

32.3

Bahir Dar

Bedele

1784

2060

Trichuris spp.

Trichostrongyles spp.

6 .8

11.0

Fasciola spp

Paramphistomu spp,

51.4

18.7

Moti et al. (2013)

9.5

12.1

St.hepatica

C.tenuicollis

Fasciola spp.

Fasciolaspp.

6.9

3.6

Bishoftu

2155

Jibat et al. (2008)

5.2

8.3

Strongyle type

Strongyloides spp.

56.60

8.2

61.0

15.4

Bersissa et al.

(2011)

M.expansa

29.2

0.63

221

Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Trichuris spp.

Strongyle spp.

Trichuris spp.

Toxocara spp.

Trichuris spp.

Trichuris ovis

T, axei

H. contortus

Ostertagia spp.

Ascaris spp.

5.0

25.4

19.4

2.9

1.5

1.6

70.2

4.3

4.5

0.0

2.5

78.4

1.2

9.8

41.4

5.2

2.8

0.4

1.6

Fasciola spp.

Paramphistomum

spp.

36.5

18.4

Cheru et al.

(2014)

Monezia spp.

2.8

Bishoftu

2155

C. ovis

Moniezia spp.

11.9

7.5

Debre

Berhan

2500-

300

Fasciola hepatica

4.5%

Njau et al. (1990)

Fikru et al. (2006)

Strongyle spp.

Dictyocaulus spp.

Trichuris spp.

Dembi

Dolo

1500-

2000

Fasciola spp.

0.4

45.69,

8.43

9.02

72.38,

8.57

1.90

C.tenuicollis, C.ovis

Abebe et al.

(2015)

Dessie

2,400

Hydatid cysts

C.tenuicollis

26.4

Endale et al.

(2013)

Yirsaw and Zewdu

(2015)

22.8

Dire Dawa

Durbete

1204

1600

Shistisoma spp.

2.3

24.6

F. hepatica

Paramphistomum

spp.

Strongyle spp.

Trichuris spp.

34.06

4.8

8.52

0.87

6.99

1500-

2000

Shimelis et al.

(2011)

Monezia Spp.

3.93

Gondar

Gondar,

Finote

Selam,

Injibara

1917-

2560

Hydatid cysts

38.8

Nigatu (2010)

M. expansa

Av.centripunctata

St.globipunctata

St.hepatica

H.contortus.

T.axei

T.vitrinus

P.microbothrium

F.hepatica

Trichostrongylus spp.

Nematodirus spathir

Cooperia curticei

Strongyloides spp.

Bunostomum spp

Oes.columbianum

Oesophagostomum

Chabertia ovina

Trichuris spp

Haremaya,

Harar, Dire

Dawa,

Menkir et al.

(2007)

2000

F. gigantica

Jijiga

Cysticercus ovis)

C.tenuicollis

Dicrocoelium

dendriticum

E. granulosus (cysts)

Haemonchus spp.

Trichostrongylus spp.

Oesophagostomum

Trichuris spp.

51.6

38.7

22.6

27.6

9.7

64.7

41.2

23.5

12.5

11.8

1790

Abebe et al.

(2010)

Hawassa

Bunostomum spp.

Feyesa et al.

(2010)

Hydatid cysts

6.9

Hawassa

1790

Haemonchus spp.

T.axei

Teladorsagia spp.

81.1

47.2

19.4

76.5

39.4

20.5

Thomas et al.

(2007)

222

Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Strongyels spp.

Strongyloid spp.

Trichuris spp.

Ascaris spp.

Capillaria spp.

Nematodirus spp.

32.4

3.3

1.9

2.4

1.4

0.9

Fasciola spp.

Paramphistomum

23.3

48.6

M. expansa

5.2

0.4

Jimma

1750

1580

Hailu et al. (2011)

Strongyles spp.

Trichuris spp.

Strongyloides spp.

27.58

2.95

3.20

0.49

3.6

0.74

0.6

Moniezia sp.

4.18

F. hepatica

1.47

4.8

Kelala,

Tesfaye (1998)

Nematodirus spp.

5.3

500 -

1840

2000-

2200

Hydatid cysts

4.25

Kombolcha

Fufa et al. (2012)

Getachew and

Ashwani (2013)

Cysticercus bovis

6. 74

Mekelle

Mekelle,

Hydatid cyst

(E.granulosus)

Adigrat, Axum, 1400 -

Kebede et al.

(2009)

8.1

Humera,

2500

Maiche, Shire

Haemonchus spp.

T.axei

T.colubriformis

Bunostomum spp.

Strongyloides spp.

Oesophagostomm.

Trichuris spp.

90.82

55.8

87.15

38.97

38.02

74.8

96.5

64.3

35.2

43.6

70.8

48.18

M.expansa

C. tenuicolis

Avitellina spp.

Stilesia spp.

27.6

32.8

33.7

31.6

20.6

34.0

35.1

28.8

Metehara,

Semera,

Jigjiga

Abebe and Esayas

(2001)

2300

51.75

Fasciola spp.

21.9

Nekemete

Ogaden

2,088

1200

Alula et al.(2013)

Haemonchus spp.

Trichostrongylus spp.

91.2

37.7

82.9

40.2

Kumsa and

Wossene (2006)

C. bovis

Hydatid cyst

0.0

9.9

Wolaita

Soddo

Regassa et al.

(2009)

2500

1977

Lidya and Berihun

(2015)

H.contortus

40.9

Wukro

: No information available, A*= no specific prevalence is mentioned

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Species composition and seasonal dynamics

In Ethiopia, the presence of GI helminthes infections in domestic ruminants is reported by many authors (Thomas et

al., 2007; Menkir et al., 2007; Abebe et al., 2010; Shimelis et al. 2011; Diriba et al., 2013; Addisu and Berihu, 2014 and

Cheru et al. 2014 ). According to the current review, about twenty three (23) GI helminthes species belonging to

Nematode, Cestode and Trematode categories have been reported from infected cattle, sheep and goats (Table 2).

Whereas, Menkir et al. (2007), Abebe et al. (2010), Hailu et al. (2011) and Shimelis et al. (2011) who reported that the

most prevalent genera of GI helminthes were Haemonchus, Trichostronglyus. Oesophagostomum, Nematodirus, Cooperia,

Toxocara and Bunostomum from Nematodes; Monezia and Cyticercusfrom Cestodes and Fasciola, Paramphistomum and

Shistosoma from Trematode classes (Table 3).

Table 3 - Summary of Species compositions of GI helminthes of domesticated ruminants in Ethiopia.

Major Class

Species

Host

Predilection site(s)

Haemonchus contortus

Haemonchus placei

Cattle, sheep, goats

Cattle

Abomasums

Small intestine

Ostertagia circumcincta

Trichostrongylus axei

Cattle, Sheep, Goats

Trichostrongylus colubriformis

Cooperia curticei

Strongyloides papillosus

Ostertagia Spp.

Chabertiaovina

Oesophagostomum columbianum

Cattle, Sheep, Goats

Sheep, Goat

Small intestine

Abomasum, Large intestine

Large intestine

Nematode

Large intestine

Strongyloidespapillosus

Trichuris ovis

Nematodirus filicollis

Nematodirus spathiger

Cattle, Sheep, Goats

Sheep

Small intestine

Large intestine

Small intestine

Trichostrongylus vitrinus

Toxocara vitulorum

Sheep, Goat

Cattle (calves)

Small intestine

Cestode

Monezia expansa

Sheep , Goat

Small intestine

Cysticercustenuicollis (Taenia hydatigena)

Ecchnoccocus granulossus

Sheep , Goat

Omentum Mesenteries Peritoneum, Liver

Small intestine

Cysticercus ovis (Taenia ovis)

Avitellina centripunctata (Av.centripunctata)

Stilesia globipunctata (St.globipunctata)

Stilesia hepatica (St. hepatica)

Small intestine

Liver, biliary ducts

Fasciola hepatica

Fasciola gigantica

Paramphistomum cervi

Sheep , Goat Cattle

Liver

Rumen

Trematode

Paramphistomum microbothrium

Sheep , Goat Cattle

Rumen

Liver, intestine, mesenteric lymph nodes

and mesenteric veins

Schistosoma bovis

Sheep , Goat Cattle

According to this systemic review, GI helminthiasis in domestic ruminants is severe and increasingly become an

important focusing area of research in the country situation. A study conducted in western Oromia on GI parasites showed

that Strangles were the most prevalent parasites encountered in the area (Moti et al., 2013). Similar study by Shimelis et

al . (2011); Cheru et al. (2014), Nejib et al. (2016) and Diriba et al. (2013) reported that Strongyles were the most

prevalent parasites encountered in North Gondar, Debre Zeit (East Shoa zone), Arbaminch (GamoGofa zone) and Asella

respectively. As it has been reported by Abebe et al. (2015); Endale et al. (2013); Feyesa et al. (2010); Nigatu (2010);

Kebede et al. (2009); Nigatu et al. (2009); Regassa et al. (2009); Jibat et al. (2008); Menkir et al. (2007); Bekele et al.

(1988), metacestodes (larval cestodes) Cysticercus ovis (Taeniaovis), Cysticercus tenuicollis (T. hydatigena) and Hydatid

cysts (Echinococcus granulosus) are the most prevalent species in Eastern Ethiopia. On the other hand, gastrointestinal

infections as a result of adult cestodes such as Avitellina centripunctata, Moniezia expansa and Stilesia globipunctata,

and bile duct infections with Stilesia hepatica were frequently reported in different parts of the country (Abebe and

Esayas, 2001; Etana, 2002; Menkir et al., 2007; Bersissa et al., 2011 ). Nonetheless, a higher prevalence of strongyles

infection was recorded in the midland and highland than the lowland, and in wet season than the dry season. The mean

fecal egg count was found to be significantly higher in the midland area and in wet season (Nejib et al., 2016). However,

according to a study by Abebe and Esayas (2001) in the arid and semiarid zones of Eastern Ethiopia revealed that during

the dry seasons of the year, a greater prevalence rates of GI helminthes were recorded in sheep and goats, 95.6 % and

100 % respectively. Furthermore, according to an abattoir survey by Menkir et al. (2007) at 4 abattoirs located in the

semi-arid zone of Eastern Ethiopia, the mean burdens of adult nematodes were generally moderate in both sheep and

goats and showed patterns of seasonal abundance that corresponded with the bi-modal annual rainfall pattern, with

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

highest burdens around the middle of the rainy season. There were significant differences in the mean worm burdens and

abundance of the different nematode species between the four geographic locations, with worm burdens in the Haramaya

and Harar areas greater than those observed in the Dire Dawa and Jijiga locations (Abebe and Esayas, 2001; Menkir et

al., 2007; Abebe et al., 2010; Berssisa et al., 2011; Endale et al., 2013). The seasonality of the GI helminthes distribution

is associated with the relative humidity and rainfall (Debela, 2002; Menkir, 2007 ). A number of reports throughout the

country indicated that there are remarkable changes in faecal egg counts and prevalence of helminths infection as a

result of seasonal variation and seasonal rainfall pattern (Fikru et al., 2006; Menkir et al., 2007; Takele et al., 2013 ).

Furthermore, relatively higher GI Helminths egg counts were found in mid altitude and highland zones than in lowland due

to the influence of existing fluctuations in geographic and climatic conditions between each zone (Demelash et al., 2006;

Takele et al., 2013 ).

Epidemiological factors

The epidemiology of the GI helminthiasis relies on factors such as the infection pressure in the environment and the

susceptibility of the host, species and pathogen factor (Tilahun, 1995). From epidemiological point of view, the infective

stages which eventually become available to the host depend on the independent and interactive influences of several

factors in the macro- and micro-environment (Urquhart et al., 1994; Woledemariam, 2005; Regassa et al., 2006; Takele

et al., 2013 ). Parasitic, host and environmental factors are the most frequently reported determinants for the

epidemiology of helminths (Etana, 2002; Fikru et al., 2006; Ahmed et al., 2007; Menkir, 2007; Shimelis et al., 2011;

Yirsaw and Zewdu, 2015 ). As stated by Shimelis et al. (2011), the prevalence of helminthiasis at species level was about

46.07% and 55% in sheep and goats, respectively. Almost similar report was documented in and around Ambo town with

the proportion of 47.8% and 53.3% in sheep and goats, correspondingly (Temesgen and Walanso, 2015). Among the

collected articles, the highest post mortem examination result was reported in Eastern Ethiopia (100%) (Abebe and

Esayas, 2001 ). Strong association between GI helminths and poor body condition was coupled with heavy intensity of

infection in the majority of infected animals (Abebe et al., 2010; Diriba et al. 2013; Alula et al., 2013; Temesgen and

Walanso, 2015 ). According to Abebe et al. (2010) and Cheru et al. (2014), the burden of GI parasites and total EPG was

significant in different body conditions.

Host factor

Sex, age, breed, nutrition, physiological status and presence or absence of inters- infections aggravate the severity of

infection (Demelash et al., 2006; Menkir et al., 2007 ).Clinical parasitic gastroenteritis has been reported in young animals

whilst infections in mature animals are generally subclinical in nature (Thomas et al., 2007). The lower occurrence in

adults has been attributed to immunological maturity as the animals grow and the increase in acquired resistance due to

repeated exposure (Biffa et al., 2004). While, some local breeds are known to be genetically resistant to GIhelminths

infections than others (Tibbo, 2006 ). In Ethiopia, the local sheep breeds (Washera, Farta, Afar, Menz, Horo); Goat breeds

(Begait, Abewrgelie, Keffa,) and Cattle breeds (Boran , Fogera, Raya, Horro, Abigar, Shekko, Arssi) are relatively resistant

to GI worms than exotic breeds (Frisch and O’Neill, 1998; Negussie et al., 2000; Tibbo, M. 2006; Menkir et al., 2007;

Solomon et al., 2009; Kebede et al., 2012 ). In addition, Moti et al. (2013) reported that Physiological status of ruminants

like level of host immunity to the parasites is subjected to the number of eggs produced by adult female helminthes. In

the same way, the females are readily infected and existing worm burdens become more active and increase egg spassed

in the feces and develop Larvae (L₃) on the pasture (Woldemariam, 2005 ).

Environmental factor

As far as Ethiopia is among the tropical African countries, the temperature is permanently favorable for larval

development in the environment. The favorable environment for larvae development is ranged at temperature about 10–

36 °C and humidity proportion of 85% (Debela, 2002 ). In the arid tropical climates of lowland areas of the country has an

environment which ranges from extensive pasturelands and browse plants to intensive grazing areas (Nejib et al., 2016).

This environment is ranged from harsh to favorable for growth and survival of free-living stages of the GI helminthes

(Tilahun, 1995; Debela, 2002 ).

Pathogen factor

The epidemiology of GI helminthes is also strongly influenced by host-parasite biology after infection has been

occurred (Abebe et al., 2010; Diriba et al., 2013). Hypobiosis has been undergone by GI helminthic the abomasal or

intestinal mucosae of the host (Cheru et al., 2014 ). Whereas, Abebe and Esayas (2001) stated that the immune status of

the host influenced the rates of hypobiosis and usually arrested during external environments are unfavorable for the

development and survival of eggs and larvae. Such development cycle usually coincides with the onset of rainy seasons

and favourable period for larval development and transmission (Kumsa and Wossenie, 2006; Feyisa et al., 2010; Hailu et

al., 2011; Nejib et al., 2016 ).

Currently applied diagnostic techniques

The diagnosis of helminthes of ruminants is based on demonstrating the presence of eggs or larvae in fecal samples

or parasites recovered from the digestive tracts or other viscera of the animals (Hailu et al., 2011; Addisu and Berihun,

2014 ). Although a great variety of methods and modifications have been described fordiagnosis, standardized techniques

such as egg or larval counts, worm counts and pasture larval counts did not exist. Therefore, most diagnostic laboratories

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

as well as teaching and research institutions were applied their own set of protocols and test procedures (Kassai, 1999 ).

Common diagnostic procedures for helminthes infections in Africa in general and in Ethiopia in particular are simple

flotation, sedimentation, modified McMaster and faecal culture methods (Hansen and Perry, 1994; Kassai, 1999; Waller,

1997 ). Some nematode genera such as strongyloides produce eggs that are identical in appearance which couldn’t be

identified easily by faecal examination alone. So to identify these faecal cultures are required (Hansen and Perry, 1994;

Urquhart et al., 1996; Kassai, 1999; Van Wyket al., 2004 ). However, Nematodirus, Strongyloides and Trichurisspecies

have eggs that can be differentiated by their distinctmorphological features. Post-mortem examinations and identification

of adult worms and arrested larvae in animals are the definitive means of identifying the parasite. Similar to faecal egg

counts; there are many procedures that are described for post-mortem examination for nematode parasites (Hansen and

Perry, 1994; Urquhart et al., 1996; Kassai, 1999 ).

Chemotherapies and control options

Effective helminthic control is a major element in ensuring the sustainability of animal production. The main aim of

control is therefore to ensure that the biotic potential of a parasite is restrained at a level compatible with the biological

requirements of economic livestock production (Waller, 1997 ). Since eradication of gastrointestinal parasites is not

practical, only integrated control methods can be envisaged. Some of the basic principles include grazing management,

acquisition of natural or artificially induced immunity, biological control and the judicious use of anthelmintic (Hazelby et

al., 1994 ).The main methods for control of helminthic parasites are prophylactic treatment with antihelmintics combined

with grazing management (Van Wyk et al., 1999 ). Despite the accumulation of drugs in animal products and undesirable

effects on non-target organisms in the environment, together with an increase in anthelmintic resistance, the use of

antihelmintics still remains the corner-stone of helminth control (Waller, 1997; Van Wyk et al., 1999; Bersissa and Girma,

2009). Since animals are often infected with a wide range of helminths, the need for broad-spectrum compounds against

trematodes, cestodes and nematodes, and their larval stages is obvious (Hazelbyet al., 1994 ). The epidemiological

information on GI helminths parasites of domestic ruminants gathered in Ethiopia can be used to design appropriate

control measures. In principle, control should aim at the reduction of transmission rates. Several control methods, which

include cultural husbandry, chemical, biological, ethno-veterinary medicine and immunological control, have been

proposed (Nejib et al., 2016).

Husbandry pattern, control and prevention

A thorough husbandry practices such as controlling stocking rates, rotational grazing, and providing hygienic grazing

can be considered as an alternative husbandry control technique (Diriba and Birhanu, 2013; Abebe et al., 2015;

Temesegen and Walanso, 2015 ). The best way to prevent GI helminthes is to keep animals away from potentially

dangerous environment. An absolute separation of stock from intermediate host zone is only practical in intensive

farming husbandry systems (Woldemariam, 2005 ) which the country has a limited effort to do so. However, in communal

grazing condition which is very common and traditional in Ethiopia, animals are communally grazed and therefore;

practices such as rotational grazing and provision of clean pastures would not be feasible (Menkir et al., 2007; Cheru et

al., 2014 ).

Chemotherapeutic interventions

Nowadays, the control of GI parasites of livestock in Ethiopia is mainly based on the use of anthelmintics. The

most commonly used generic broad spectrum antihelminthics that are available in Ethiopia are the Benzimidazoles,

Imidazothiazoles and Macrocyclic lactones which consist albendazole, levamisole and ivermectin, respectively

(Woldemariam, 2005; Kumsa, and Wossene, 2006; Menkir et al., 2007 ). It is readily available wherever in the country

since it has been imported massively by the government and non-government institutions; and used by every individual

including farmer. However, the use of antihelmintics at regular intervals for a long period of time and treating by mass

whenever an animal manifest clinical syndrome has become the major issue for the development of multiple

resistances; for instance against benzimidazoles (Woldemariam, 2005 ). Targeted or selective application of

anthelmintic treatment might be an important tool to keep susceptible GI nematode strains in livestock and to delay

this case. An alternative approach for selective anthelmintic treatment was studied using experimental small

Woldemariam (2005) and Menkir (2007). Such system can be used by the farmers themselves by checking their

animals for signs of anaemia (VanWyketal, 2004). Unfortunately, it was not practiced very well in Ethiopia where mixed

parasitc infection, and where traditional feeding practice is followed (VanWyk et al., 2004; Kumsa and Wossene, 2006 ).

A cost-effective preventive control programs for helminth infection in ruminants is based on sound epidemiological

knowledge of the time relationship between contamination of pastures and the seasonal availability of infective larvae in

a given geographic area. Epidemiological knowledge, its application in grazing management whenever feasible and

access to antihelmintics of high efficacy are key factors for the success of controlling helminth infections in domestic

ruminants (Aynalem et al., 2009; VanWykand Mayhew, 2013). Projecting models derived from more complete

information on the ecology of GI helminth infection and anthelmintic resistance, climate and local management factors

provide a basis for improved control schemes based on chemotherapy, management and immunization within similar

climate (VanWyk and Mayhew, 2003; Woldemariam, 2005; Menkir et al, 2007 ).

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

Ethno-veterinary practices

As a result of the gradually increasing anthelmintic resistance, residual effect on animal products, environmental

pollution, scarcity and high cost of such drug especially to poor farmers have enforced to reconsider other alternative

helminthic control technique in the country (Bersissa and Girma, 2009). Of these, Ethno-veterinary medicine has become

a substantial and most expanding interest of options for Ethiopian farmers. Although such a kind of conventional

veterinary medical system was yet very poor in the country, a very limited effort have been done to encourage the widely

used ethno-veterinary plants in the country (Lulekal et al., 2008; Fullas, 2010; Asfaw and Fentahun, 2020). In order to do

so, several Ethno-veterinary surveys were conducted so far in the country which indicated as if several traditional healers

use medicinal plants for de-worming livestock (Jemal et al., 2011 ). To mention few examples, Herbal preparations from

fresh leaves of Dodonea viscose, Albizia gummifera and Vernonia amygdalina against mixed natural infections in sheep

was evaluated by Biffa et al. (2004) to show the anthelmintic activities. In addition, an In-vitro antihelmintics activity study

from Rhus glutinnosa, Syzygium guineensa, Albizia gummifera, Croton macrostachyus, Ekebergia capensis, Acacia

nilotica and Terminalia schimperiana against Haemonchis contortus have been reported by Eguale et al. (2006) and

Jemal et al. (2011). Furthermore, anthelmintic activity of plants such as Allium sativum, Zingiber officinale, Cucurbita

mexicana, Ficus religiosa, Artemisia brevifolia, Calotropis procera, Nicotiana tabacum, Butea monosperma, Coriandrum

sativum, Ocimum, Thymus schimperi and Echinops kebericho have been reported by Abera (2003), Biffa et al. (2004) and

Giday et al. (2007).

CONCLUSION

This review work assessed the GI helminthes in Ethiopia and provides a clue on perspectives and constraints encountered

in researches which were done on GI helminths in ruminants. Twenty three (23) GI helminthes species that belong to all

the three major classes of helminths have been found to occur in domestic ruminants in Ethiopia. In addition, nematodes

are the most commonly encountered GI helminths while Cestodes are the least. In most reports, a higher rate was

recorded in small ruminants. The most prevalent genera of GI helminths reported in order of prevalence are Haemonchus,

Trichostronglyus, Oesophagostomum, Nematodirus, Cooperia, Toxocara and Bunostomum from Nematodes; Moneziaand

Cyticercus from Cestodes. Whereas, Fasciola, Paramphistomum and Shistosoma are found from Trematode category.

Both the abattoir and coprological studies have indicated that infection by GI helminthes in ruminants is highly prevalent

and widespread in all agro-ecologies and livestock production systems in Ethiopia. Fecal diagnostic techniques such as

simple flotation, sedimentation, modified McMaster have been used routinely in Ethiopia. It has been also shown that

prevalence of GI helminthes parasites was related to the agro-climatic conditions such as quantity and quality of pasture,

temperature, humidity and grazing behavior of the host and the susceptibility of any intestinal helminthic parasites were

also influenced by age, breed, species, health status, physiological factors and previous exposure to parasites.

Due to the lack of effective helminthes control strategies in Ethiopia, antihelmintics are exclusively used. Though

Ethiopia has a huge amount of small and large ruminants population, the country is facing a direct and indirect economic

lose as a result of GI helminthes infection. Hence, immediate remedies shall be taken into action on control and

prevention methods against such anthelmintic resistant GI parasites. In order to this, it is advantageous to collect and

looking over the previous researches done so far to reconsider their gaps for the future short and long term actions on

prevention and control strategies. So, all-inclusive and well organized documentation about GI helminthes of ruminants in

the country is essential to support researchers and policy makers to develop such remedies. Finally, applicable field

diagnostic technique should be introduced as far as mixed parasitic infection and traditional feeding practice is

common in the country which can aggravate GI helminthes infection.

DECLARATIONS

Consent to publish

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Funding

This study was funded by the University of Gondar.

Availability of data and materials

Data will be made available up on request of the primary author

Acknowledgment

The authors’ heartfelt thanks the University of Gondar, Research and Community Service V/President for the

financially supporting in the study.

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Citation: Fentahun T (2020). Systematic review on gastrointestinal helminths of domestic ruminants in Ethiopia. Online J. Anim. Feed Res., 10(5): 216-230.

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