Livestock Research for Rural Development 32 (6) 2020 LRRD Search LRRD Misssion Guide for preparation of papers LRRD Newsletter

Citation of this paper

The effect of strategic deworming programs on the prevalence of gastrointestinal Strongyles and Fasciola in sheep of selected districts of North Shewa Zone, Ethiopia

C Demis, T Asfaw, E Yitagesu and E Alemnew

Debre Birhan Agricultural Research Center, P.O.Box 112, Debre Birhan, Ethiopia
chekgetdvm07@gmail.com

Abstract

On-farm and on-station study was conducted from September 2014 to August 2018 in Menz Gera and Menz Mama Districts of North Shewa Zone and in Debre Birhan Agricultural Research Center (DBARC), Amhara Region, Ethiopia to evaluate the effect of strategic deworming programs on the prevalence of major gastrointestinal strongyle nematode and Fasciola eggs in naturally infected sheep. Sheep were dewormed four times per year in September, December, March and June using an anthelmintic drug that includes albendazole, tetraclozash, tetramisole, ivermectin and triclabendazole according to the manufacturers' recommendations. A total of 6728 faecal samples were collected and examined both before and after deworming using flotation technique for nematode eggs and sedimentation technique for Fasciola eggs. Before deworming, the on-farm prevalence of nematode and Fasciola eggs was 38.8% and 43.3%, respectively and the on station prevalence of the same parasite eggs was 29.2% and 33.8%, respectively. At the end of the study, after four successive years of strategic deworming programs, the on-farm prevalence of nematode and Fasciola eggs was reduced to 1.1% and 23.2% and the on station prevalence of these parasitic eggs was reduced to 2.6% and 19.0%, respectively, and the difference was found statistically significant (P<0.05). Similarly, significant (P<0.05) reduction in the on-farm and on-station prevalence of nematode and Fasciola eggs was recorded after the application of strategic deworming programs. The coprological investigation in this study revealed that irrespective of the production system and various risk factors, application of the strategic deworming programs can significantly reduce the parasite load in sheep. However, more tight and integrated parasite control programs should be implemented for better success in the reduction of parasitic burden in sheep flocks of highland areas with further studies on species identification.

Keywords: deworming, Fasciola, nematode, strongyle, North Shewa, prevalence, sheep, strategic


Introduction

Small ruminants play a very important role in human nutrition and, they have the potential of serving as tools for poverty reduction through the provision of meat, milk, household income, manure and skin. However, the productivity per animal is still low due to multitude of factors (Okorafor et al 2015). Parasites are among these factors which are responsible for a number of economic losses in a variety of ways.

Parasites cause losses through lower fertility, a reduction in feed intake, lower weight gains, lower milk and meat production, treatment costs and mortality in heavily parasitized animals (Carmichael 1972; Akerejola et al 1979; Nahed-Toral 2003). Gastrointestinal parasites are worldwide problems but their impact is greater in sub –Saharan Africa including Ethiopia due to the availability of a wide range of agroecological factors suitable for diversified host and parasite species (Fikru et al 2006).

Recently, in Amhara National Regional State, there are encouraging works on sheep breed improvement for mutton purpose, both through community based breeding programs at the farmer level and the research centres. Despite the breed improvement programs of the region, several sheep diseases, particularly those diseases which are caused by internal parasites are the commonest problems in the areas. Among these parasitic diseases, the ones that are caused by gastrointestinal nematodes and Fasciola are the primary challenges of the study area.

Hence, four times per year (September, December, March and June) deworming strategic programs are implemented in sheep flocks of the study areas as part of health monitoring and surveillance works that will help breed improvement activities. The strategic deworming is applied using broad-spectrum anthelmintic drugs like albendazole (albendazole 300mg, Chengdu Qiankun Veterinary Pharmaceuticals Co. Ltd., China), tetraclozash 900mg (oxyclozanide 450mg + tetramisole HCL 450mg, Ashish Life Science PVT limited, India), tetramisole (tetramisole HCL 600mg, Inner Mongolia Huatian Pharmaceuticals Co., Ltd, China) and ivermectin (ivermectin 5 mg, Ashish Life Science PVT limited, India) as well as narrow-spectrum drugs mainly triclabendazole (triclabendazole, 250mg, East African Pharmaceuticals P.L.C., Ethiopia) following the manufacturer recommended doses.

According to El-Bahy et al (2009), strategic parasite control programs are usually designed based on the identification of major types, incidence and seasonality of parasites, rainfall and temperature of an area as well as the availability of anthelmintic drugs in the target region. The same authors indicated that such treatment of parasites at critical times of the year induce enormous effects on their eradication, minimize the parasitic stress on the animal and improve its general health condition and productivity.

Several strategic deworming programs are applied in different countries all over the world. These programs include two times treatment during the year (Maingi et al 2002; Magona et al 2004), three times treatment program per year (Guimaraes et al 2000; Magona et al 2004), four times treatment program per year and even monthly treatment (Bukunzi and Serumaga-Zake 2000). However, selection of the effective time for massive chemotherapic prophylaxis differs from one country to another depending on the rainfall, atmospheric temperature and seasonality of parasites (El-Bahy et al 2009).

Therefore, the objective of this study was to evaluate the effect of available broad and narrow-spectrum anthelmintic drugs in the reduction of the prevalence of nematode and Fasciola eggs when they are applied in a strategic approach in sheep under the community based breeding programs at the farmer level and Debre Birhan Agricultural Research Center.


Materials and methods

Study areas

The study was conducted from September 2014 to August 2018 in Menz Gera and Menz Mama Districts of North Shewa zone and the station of Debre Birhan Agricultural Research Center (DBARC), Amhara Region, Ethiopia. All of the study areas are found in the central high lands of the country at road distances of 120 to 360 kilometres from Addis Ababa, the capital city of Ethiopia. Geographically, the areas lie between 9° 35’45” to 10° 18’0” north latitude and 39° 29’40” to 39° 40’ 0’’east longitude with average elevation ranges of 2800 to 3200 meters above sea level and with mean annual temperature ranges of 12.2 to 19.9°C. The average annual rainfall of the areas ranges from 897.8 to 1149 mm and it is characterized by the bimodal pattern with a cold, harsh climate that occasionally has frost, particularly between November and January. There are four climatic seasons which include the Kiremt (Summer or Meher), Belg (Autumn), Bega (Winter) and Tsedey (Spring). Kiremt ranges from June to August, Belg ranges from September to November, Bega ranges from December to February and Tsedey ranges from March to May (DBARC 2014; Menz Gera and Menz Mama Livestock Offices 2014 and www.ethiopiantreasures.co.uk/pages/climate.htm).

Study animals and their management

Indigenous breeds (Menz, Bonga and Washera breeds), crossbreeds (Dorper and Awassie breeds crossed with indigenous breeds) and exotic breeds (Dorper and Awassie breeds) were included in the study. The study animals were kept under traditional extensive management system in the areas of community-based breeding programs at the farmers level and in semi-intensive management system in the research centre. The sheep in the community based breeding programs at the farmers level depend mainly on grazing natural pasture in private and communal grazing lands while sheep in the research centre provided harvested hay and commercial concentrate feed (maize, oilseed cake, wheat bran and salt) in addition to the morning and afternoon pasture grazing. Moreover, these animals were treated using anthelmintic drugs that include albendazole, tetraclozash, tetramisole, ivermectin and triclabendazole. The drugs were applied in four rounds per year in September, December, March and June following manufacturers’ recommendations and deworming months were selected based on the epidemiological cycle of targeted parasite groups and the laboratory findings. They are also vaccinated against major infectious diseases which include pasteurellosis, sheep and goat pox and peste des petits ruminants (PPR).

Study design and sample size

This study is a continuation of the first longitudinal monitoring study conducted from 2011 to 2014 before the full implementation of strategic deworming programs. In that study, the baseline (before deworming) prevalence of major gastrointestinal nematode and Fasciola parasite eggs was recorded in sheep from the same study areas and sample size. Then, implementation of strategic deworming programs was started in September 2014 and continued up to August 2018 to evaluate the impact of strategic deworming programs on the prevalence of major gastrointestinal nematode and trematode parasites. These activities were conducted through longitudinal follow up based on the laboratory analysis of monthly collected faecal samples for the presence of parasite eggs. Study districts and villages were selected purposively based on the presence of breed improvement works, while sheep were selected through stratified random sampling method. Sheep were stratified before sampling by their breed, age and sex and then animals were sampled based on the repeatable Fecal Egg Count (FEC) monitoring guideline of Abbott et al. (2012). According to this guideline, from sheep grazing together in the same field, at least 10 sheep in the strata of each group should randomly be sampled. For this particular study, however, about 15% (proportional sampling) of animals were sampled from each breed, age and sex using a systematic random sampling method. Accordingly, a total of about 6728 (1848 from the on-farm and 4880 from the on-station) sheep were sampled and followed for four successive years from September 2014 to August 2018.

Faecal sample collection and examination

Faecal samples were collected in the first week of every month directly from the rectum of sheep under study, using latex examination gloves and by inserting lubricated index finger. These samples were put in universal sampling bottles containing 10% chlorhexidine preservative and the sampling bottles were labelled with identification number, sex, age and breed of the animals sampled as well as the location and date of sampling. The collected samples were transported within a week of collection to the parasitology laboratory of Debre Birhan Agricultural Research Center and examined for the presence of nematode and Fasciola eggs using simple test tube floatation and sedimentation techniques as described by Charles (2006).

Data management and analyses

The data collected from the community-based sheep breed improvement villages and the research centre as well as from the laboratory investigation were coded with appropriate variables and analyzed using Statistical Package for Social Science (SPSS) statistical software version 20. Descriptive statistics was used to summarize the data and the prevalence was calculated by dividing the number of positive animals by the total number of animals examined and multiplied by 100. The percentage was used to measure prevalence and Chi-Squared (χ 2) test was used to measure the association between the prevalence of the parasite eggs before and after the application of strategic deworming programs and the risk factors including age, sex, breed and season. In all analyses, the confidence level was held at 95% and P<0.05 was set for statistical significance.


Results and discussion

The changes in the prevalence of Nematode and Fasciola eggs in the on-farm and on-station sheep before and after the application of strategic deworming programs were demonstrated in Tables 1 and 2, respectively. According to the result of this study, the initial (before deworming) on-farm and on-station prevalence of nematode eggs was 38.8% and 29.2%, respectively, with an overall prevalence of 31.8%. After four years of intervention using strategic deworming programs, the on-farm prevalence these eggs reduced to 1.1% and the on station prevalence of the same eggs reduced to 2.6% with an overall prevalence of 2.3%. The respective difference in the on-farm and on-station prevalence of Nematode eggs reached to 37% and 26.6% with an overall difference of 29.5% after application of strategic deworming programs.

In addition, the initial on-farm and on-station prevalence of Fasciola eggs was 43.3% and 33.8%, respectively, with an overall prevalence of 36.6%. However, the on-farm prevalence of these eggs reduced to 23.2% and the on station prevalence reduced to 19.0% after the deworming programs with an overall prevalence of 20.1%. In a similar trend to nematodes, the on-farm and on-station prevalence of Fasciola eggs also showed the respective difference of about 20.1% and 14.8% with an overall difference of 16.1%. The statistical analysis of this result indicated that the difference in the on-farm and on-station prevalence of both nematode and Fasciola eggs before and after the strategic deworming programs was found statistically significant (P<0.05) (Table 1 and 2).

Table 1. On-farm and on-station prevalence of nematode eggs of sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ2

p-value

Before

After

Production System          

On-farm

1848

717 (38.8)

20 (1.1)

66.218

0.001

On-station

4880

1425 (29.2)

127 (2.6)

Total

6728

2142 (31.8)

147 (2.3)

N: number of animals sampled
N+: number of positive animals for parasite eggs



Table 2. On-farm and on-station prevalence of Fasciola eggs of sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ 2

p value

Before

After

Production System

On-farm

1848

801 (43.3)

428 (23.2)

103.190

0.000

On-station

4880

1649 (33.8)

927 (19.0)

Total

6728

2450 (36.4)

1355 (20.1)

N: number of animals sampled
N+: number of positive animals for parasite eggs

Concerning the risk factors, the difference in the on-farm and on-station prevalence of both nematode and Fasciola eggs before and the application of strategic deworming programs was found statistically significant (P<0.05) for age, sex, age and climatic seasons. The statistically significant (P<0.05) reduction in the on-farm prevalence of nematode and Fasciola eggs is demonstrated in Tables 3 and 4, respectively.

Table 3. On-farm prevalence and risk factors of nematode infection of Menz sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ 2

p-value

Before

After

Age

<1 year

414

202 (48.8)

6 (1.4)

23.923

0.000

>= 1 year

1434

515 (35.9)

14 (1.0)

Sex

Male

482

218 (45.2)

7(1.6)

12.787

0.002

Female

1366

499 (36.5)

13 (1.0)

Season

Sept – Nov

464

192 (41.4)

7 (1.5)

Dec – Feb

457

166 (36.3)

4 (0.9)

20.469

0.002

Mar –May

472

153 (32.4)

4 (0.8)

June – Aug

455

206 (45.3)

5 (1.1)

Total

1848

717 (38.8)

20 (1.1)

N: number of animals sampled
N+: number of positive animals for parasite eggs



Table 4. On-farm prevalence and risk factors of Fasciola infection of Menz sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ 2

p-value

Before

After

Age

<1 year

414

169 (40.8)

72 (17.4)

19.401

0.000

>= 1 year

1434

632 (44.1)

356 (24.8)

Sex

Male

482

179 (37.1)

94 (19.5)

28.511

0.000

Female

1366

622 (45.5)

334 (24.6)

Season

Sept – Nov

464

204 (44.0)

103 (22.2)

Dec – Feb

457

181 (39.6)

96 (21.0)

23.290

0.001

Mar –May

472

190 (40.3)

115 (24.4)

June – Aug

455

226 (49.7)

114 (25.1)

Total

1848

801 (43.3)

428 (23.2)

N: number of animals sampled
N+: number of positive animals for parasite eggs

The results in Tables 5 and 6 demonstrated a significant (P<0.05) reduction in the on-station prevalence of nematode and Fasciola eggs, respectively, after application of strategic deworming programs.

Table 5. On-station prevalence and risk factors of nematode infection of sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ 2

p-value

Before

After

Age

<1 year

716

237 (33.1)

28 (3.9)

13.225

0.001

>= 1 year

4164

1188 (28.5)

99 (2.4)

Sex

Male

1150

293 (25.6)

31 (2.7)

10.096

0.006

Female

3730

1132 (30.3)

96 (2.6)

Breed

Dorper

1277

456 (35.7)

59 (4.6)

Dorper x Local

933

275 (29.5)

13 (1.4)

Menz

2045

493 (24.1)

40 (2.0)

Bonga

139

44 (31.7)

4 (2.9)

92.2596

0.000

Washera

196

63 (32.1)

4 (2.0)

Awassie

50

18 (36.0)

0 (0.0)

Awassie x Local

240

76 (31.7)

7 (2.9)

Season

Sept – Nov

1224

382 (31.2)

56 (4.6)

Dec – Feb

1232

291 (23.6)

19 (1.5)

66.801

0.000

Mar –May

1208

340 (28.1)

21 (1.7)

June – Aug

1216

412 (33.9)

31 (2.5)

Total

4880

1425 (29.2)

127 (2.6)

N: number of animals sampled
N+: number of positive animals for parasite eggs



Table 6. On-station prevalence and risk factors of Fasciola infection of sheep in selected districts of North Shewa Zone

Risk Factors

N

N+ (Prevalence in %)

χ 2

p-value

Before

After

Age

<1 year

716

272 (38.0)

153(21.4)

14.536

0.001

>= 1 year

4164

1377 (33.1)

774 (18.6)

Sex

Male

1150

371 (32.3)

167 (14.5)

28.386

0.000

Female

3730

1278 (34.3)

760 (20.4)

Breed

Dorper

1277

521 (40.8)

271 (21.2)

Dorper x Local

933

297 (31.8)

173 (18.5)

Menz

2045

594 (29.0)

358 (17.5)

Bonga

139

57 (41.04)

29 (20.9)

95.371

0.000

Washera

196

82 (41.8)

42 (21.4)

Awassie

50

20 (40.0)

10 (20.0)

Awassie x Local

240

78 (32.5)

44 (18.3)

Season

Sept – Nov

1224

437 (35.7)

244 (19.9)

Dec – Feb

1232

375 (30.4)

222 (18.0)

22.563

0.001

Mar –May

1208

387 (32.0)

227 (18.8)

June – Aug

1216

450 (37.0)

234 (19.2)

Total

4880

1649 (33.8)

927 (19.0)

N: number of animals sampled
N+: number of positive animals for parasite eggs

In the current study, highly significant (P<0.05) reduction in the on-farm and on-station prevalence of both nematode and Fasciola eggs was recorded for all risk factors considered after the application of four times per year strategic deworming programs. This result is in agreement with the reports of EL-Bahy et al (2009) who indicated absolute freedom of the animals from their previous parasitic infection after four times per year treatment regime. The current result is also in line with previous reports by Dalton (1999) who indicated that the prevalence of liver flukes in sheep was reduced significantly from 75% to 1% after five anthelmintic treatments per annum during 3 years. Similarly, Francisco and Sergio (2009) indicated a marked decrease in the prevalence of Fasciola hepatica parasites from 63.16% to 13.64% over a two years intervention period.

The study conducted in cattle by Jakob et al (2000) indicated that the overall prevalence of Trichostrongyle faecal eggs was 32% in the treated animals and 47% in the untreated control animals. Although the effects of anthelmintic drugs in body weight changes of treated sheep is indirect, a large-scale, randomized intervention field study conducted by Zinsstag et al (1997) also showed that two annual fenbendazole treatments increase live weights of one to four years old animals between 8 and 17%. This was also in agreement with the works of Bukunzi and Serumagas-Zake (2000) which indicated that repeated treatment of animals leads to a gradual decrease in the number of infective stages of parasites shed from treated animals.

A study conducted by Maes L Veys et al (1993) showed a reduction in the prevalence of liver fluke infections from 93% to 5% even when the annual treatments were reduced from four times per year to three times per year in the second year of strategic parasite control campaign. The findings of this study are also in agreement with the works of Maichomo et al (2004) and Magona et al (2004) that indicated improvements in the general health status of animals as a result of strategic application of anthelmintic drugs. As Jakob et al (2000), two annual strategic treatments during the peak of gastrointestinal nematode excretion reduce contamination with Trichostrongyle eggs by 31-57%. Maingi et al (2006) also reported that strategic anthelmintic treatment leads to improvements in some physiological parameters of treated animals in the form of high weight gain and Packed Cell Volume (PCV).

According to ILCA (1990), reduction in the prevalence of parasites through strategic regular deworming programs is much more important in highland areas than the midland and low land areas found elsewhere in the country because gastrointestinal parasites contribute for about 50% of all sheep morbidities on farms in the Ethiopian highlands.

However, the fluke prevalence of this study is higher than the findings of Njau et al (1990) who reported Fasciola infection rate of 10% after regular deworming programs at the International Livestock Centre for Africa research station at Debre Berhan. These relative differences in the prevalence of parasites might arise due to existence of different climatic and environmental factors (ecological diversity and climatic variation in temperature and rainfall) that could support survival and development of infective larval stage of parasites.

In addition, the multitude of other factors including overstocking, poor nutrition (starvation), poor housing and hygiene, the sample size considered, types of techniques utilized, frequent exposure to the contaminated communal grazing lands and resistance of parasites to the frequently used anthelmintic drugs could also be responsible for the variation in the prevalence of parasite eggs recorded in this and other studies.


Conclusions


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Received 30 April 2020; Accepted 6 May 2020; Published 1 June 2020

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