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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 114 Zambrut Zambrut.com. Publication date: March 13, 2019. Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 104 Lungworms of Sheep and Cattle Slaughtered at Abattoir (Study of Debre Birhan Municipal Abattoir and Private Hotels in Central Ethiopia) Aweke Engdawork dr. Aweke Engdawork Doctor of Veterinary Medicine (DVM) Researcher at Ethiopian Biodiversity Institute Addis Ababa, Ethiopia 1. Introduction Ethiopia has one of the largest livestock populations in Africa with livestock ownership currently supporting and sustaining the livelihoods of an estimated 80 percent of the rural community [1]. The livestock sector in Ethiopia contributes 12 and 33% of the total and agricultural gross domestic product, respectively [2]. In the highlands, which account for over 75 percent of the livestock population, cattle provide traction power for 95% of grain production. The contribution of Ethiopian livestock and livestock products export to foreign exchange earnings is also significant [3; 4]. However, it is characterized by less productivity due to morbidity and mortality caused by different parasitic diseases. Lungworms are incriminated as one of the major and common parasitic diseases of ruminants around the world [5]. Abstract: The study was conducted from November, 2017 to April, 2018 at Debre Birhan municipal abattoir and private hotels, with the objectives of determining percentage, comparison of lungworms in sheep and cattle, identifying the species of the respiratory helminthes circulating in the area and assessing the possible risk factors of lungworms in sheep and cattle in the study area. Postmortem examination was conducted on 400 animals (204 sheep and 196 cattle) at Debre Birhan municipal abattoir and private hotels. An overall percentage of 20.8% lungworm was recorded as a result of postmortem examination. The occurrence of lungworm was 40.7% in sheep and 0% in cattle. Dictyocaulus filaria was the only lungworm species identified in this study. Age, body condition and season of the year have significant difference (p<0.05) on occurrence of lungworms in sheep. The occurrence of lungworm in sheep was significantly higher (p<0.05) in young sheep (54.9%) than in adult sheep (34.5%), also in sheep with poor body condition (58.1%) than in sheep with medium (37.5%) and good body conditions (25.9%); and during the Autumn season (51.4%) than during the other seasons of the study period, Winter (40.5%) and Spring (26.0%). However, significant difference in percentage of lungworms between male and female sheep was not observed (P>0.05). A mild (low) degree of lungworm burden was observed in sheep with good (9.26%), medium (7.95%) and poor (12.90%) body conditions. However, heavy lungworm burden was significantly higher in sheep with poor body conditions (27.42%) than those sheep with medium (12.50%) and good body conditions (3.70%). Likewise, heavy degree of lungworm burden was recorded during the Autumn (15.71%) and Winter (19.05%) seasons than during in the Spring (6.00%). Lungworms have great negative impact on livestock production and as a result emphasis should be given to regular and strategic de-worming to control and prevent lungworms in domestic animals and further studies are needed to clarify the economic significance and overall situation of lungworms in all species of domestic animals found in various agro-ecological zones of Ethiopia. Keywords: Cattle; Debre Birhan; Lungworm; Percentage; Postmortem; Sheep.

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Page 1: Lungworms of Sheep and Cattle Slaughtered at Abattoir · The signs of lungworm infection (verminous pneumonia), range from moderate coughing with slightly increased respiratory rates

International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 104

Lungworms of Sheep and Cattle

Slaughtered at Abattoir (Study of Debre Birhan Municipal Abattoir and Private Hotels in Central Ethiopia)

Aweke Engdawork

dr. Aweke Engdawork

Doctor of Veterinary Medicine (DVM)

Researcher at Ethiopian Biodiversity Institute

Addis Ababa, Ethiopia

1. Introduction

Ethiopia has one of the largest livestock populations in Africa with livestock ownership currently supporting and

sustaining the livelihoods of an estimated 80 percent of the rural community [1]. The livestock sector in Ethiopia contributes

12 and 33% of the total and agricultural gross domestic product, respectively [2]. In the highlands, which account for over

75 percent of the livestock population, cattle provide traction power for 95% of grain production. The contribution of

Ethiopian livestock and livestock products export to foreign exchange earnings is also significant [3; 4]. However, it is

characterized by less productivity due to morbidity and mortality caused by different parasitic diseases. Lungworms are

incriminated as one of the major and common parasitic diseases of ruminants around the world [5].

Abstract: The study was conducted from November, 2017 to April, 2018 at Debre Birhan municipal abattoir

and private hotels, with the objectives of determining percentage, comparison of lungworms in sheep and

cattle, identifying the species of the respiratory helminthes circulating in the area and assessing the possible

risk factors of lungworms in sheep and cattle in the study area. Postmortem examination was conducted on

400 animals (204 sheep and 196 cattle) at Debre Birhan municipal abattoir and private hotels. An overall

percentage of 20.8% lungworm was recorded as a result of postmortem examination. The occurrence of

lungworm was 40.7% in sheep and 0% in cattle. Dictyocaulus filaria was the only lungworm species

identified in this study. Age, body condition and season of the year have significant difference (p<0.05) on

occurrence of lungworms in sheep. The occurrence of lungworm in sheep was significantly higher (p<0.05)

in young sheep (54.9%) than in adult sheep (34.5%), also in sheep with poor body condition (58.1%) than in

sheep with medium (37.5%) and good body conditions (25.9%); and during the Autumn season (51.4%) than

during the other seasons of the study period, Winter (40.5%) and Spring (26.0%). However, significant

difference in percentage of lungworms between male and female sheep was not observed (P>0.05). A mild

(low) degree of lungworm burden was observed in sheep with good (9.26%), medium (7.95%) and poor

(12.90%) body conditions. However, heavy lungworm burden was significantly higher in sheep with poor

body conditions (27.42%) than those sheep with medium (12.50%) and good body conditions (3.70%).

Likewise, heavy degree of lungworm burden was recorded during the Autumn (15.71%) and Winter

(19.05%) seasons than during in the Spring (6.00%). Lungworms have great negative impact on livestock

production and as a result emphasis should be given to regular and strategic de-worming to control and

prevent lungworms in domestic animals and further studies are needed to clarify the economic significance

and overall situation of lungworms in all species of domestic animals found in various agro-ecological zones

of Ethiopia.

Keywords: Cattle; Debre Birhan; Lungworm; Percentage; Postmortem; Sheep.

Page 2: Lungworms of Sheep and Cattle Slaughtered at Abattoir · The signs of lungworm infection (verminous pneumonia), range from moderate coughing with slightly increased respiratory rates

International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 105

Lungworms are parasitic nematode worms of the order Strongylida that infest the lungs of vertebrates. The most

common lungworms belong to one of two groups, the superfamily Trichostrongyloidea or the superfamily

Metastrongyloidea [6]. The lungworms in the superfamily Trichostrongyloidea include several species in the genus

Dictyocaulus which infest cattle (D. viviparus), small ruminants (D. filaria) and equines (D. arnfeldi). These parasites have

direct life-cycles [7; 8]. The lungworms from the superfamily of Metastrongyloidea include Protostrongylidae

(Protostrongylus rufescens, Muellerius capillaries) that infest sheep and goats and this group have indirect life cycle which

involve intermediate host (IH) of either snail or slug [6].

Lungworms are widely distributed throughout the world but are particularly common in countries with temperate

climates, and in the highlands of tropical and subtropical countries, and it is common in Ethiopia [9]. Epidemiological

distribution of lungworms depends more on pasture contamination by carrier animals and pasture infectivity is related to

rainfall which stimulates the activity of the larvae and the mollusk [10]. The prevalence of lungworms of ruminants depends

on different factors like, the climate of area, intermediate hosts and favorable ecological conditions [71]. Overpopulation

increases the concentration of parasites and also forces animals to graze closer to the ground. Young animals at first grazing

are at high risk of infection than adult stocks [12].

Dictyocaulus have a direct life cycle and the adult females lay larvated eggs in the bronchi. The eggs are coughed up

and swallowed with mucus and the L1 hatch out during their passage through the GIT and L1 are excreted in faeces. On

pasture, the larvae molt into the second stage (L2) and develop to the infective L3. Then it is ingested by the animal while

grazing in the pasture [13]. Protostrongylus and Mulleries have indirect life cycle involving IH of several snails and slugs

[14]. Adult worms lay eggs which then coughed up with sputum toward bronchi and trachea. The eggs became hatched to

first stage larvae (L1- larvae) in the trachea or during its passage in GIT and L1-larvae are passed in the feces. Once in the

environment, larvae penetrate into the snails and develop to infective L3 larvae. Livestock becomes infected after eating

contaminated snails or slugs while grazing [15].

The pathogenesis of lungworms depends on their location within the respiratory tract, the number of infective larvae

ingested, the animal immune state, the nutritional status and age of the host. The signs of lungworm infection (verminous

pneumonia), range from moderate coughing with slightly increased respiratory rates to sever persistent coughing.

Unthrifitness, dyspnea, nasal discharge, weight loss, in case of associated bronchopneumonia, also fever and death are

important clinical signs [16]. Diagnosis can be based on the clinical signs and grazing history. Usually, the clinical signs,

the time of the year and a history of grazing are sufficient to make diagnosis [17]. The confirmation of lungworm is by

detecting the L1 stage in faecal samples using the Baermann technique [18].

The anthelmintics available for the treatment of lungworms are the modern albendazole, levamisole and ivermectin

[19]. These drugs have shown to be effective against all stages of lungworms with a consequent amelioration of clinical

signs [20]. The control and prevention of lungworm can be achieved by deworming all animals at the end of the rainy

season to avoid heavy parasitic burden during grazing and deworming all animals at the end of the dry season before the

rain starts as it is very important in reducing pasture contamination [7]. Providing balanced nutrition is very important to

keep animals healthy and help them to develop appropriate resistance to external pathogens [21]. The other method is

vaccination that was developed from larvae of Dictyocaulus [22].

In Ethiopia, the prevalence of lungworms in ruminants and the species of the parasite involved have been reported by

many researchers such as [23; 24; 25; 26; 27; 11; 28; 29]. But most of these researchers used coprology alone or with some

combination of postmortem examination of lungs. According to these studies, the prevalence of lungworms in Ethiopia

ranges from 13.4–72.4% in sheep and 1.5–3.1% in cattle. In contrast to the avialablity of several studies on ovine

lungworm, only very few studies are available on bovine lungworm. Due to the presence of diverse ecological and climatic

conditions suitable for survival and developement of lungworms in Ethiopia; studies that generate basic information on the

occurrence, species diversity and risk factors are extremely helpful to design practically appropriate control and prevention

strategies in Ethiopia.

Therefore, this DVM research was designed to attain the objectives:

To determine the occurence of lungworms in sheep and cattle and compare the percentage between sheep and cattle

slaughtered at Debre Birhan municipal abattoir and private hotels in Debre Birhan.

To identify the species of lungworm helminthes that circulating in sheep and cattle in the study area and

To assess the possible risk factors of lungworms in sheep and cattle in the study area.

2. Material and Methods

2.1. The study area

The study was conducted to determine the occurrence of lungworms in sheep and cattle slaughtered at Debre Birhan

municipal abattoir and private hotels from November, 2017 to April, 2018. Debre Birhan is a town located in North Shewa

administrative zone of Amihara regional state situated 130 km northeast of Addis Ababa. Debre Birhan town is

geographically located at latitude 09o

31’N and longitude 39

o 42

’ E with an altitude of 2840 meter above sea level (Fig 1).

This area is mountainous with large plane grazing lands and dissected by two rivers, namely Dalicha and Beressa. In the

study area indigenous and cross breed of cattle and sheep are the major livestock with traditional crop-livestock farming

[30]. Mean livestock holdings are larger than elsewhere in the Ethiopian highlands. The largest population of sheep and

cattle are the source of income and security [31]. Livestock population comprises of 144,638 cattle, 97,815 sheep, and

47,970 goats and 39,038 equines [32].

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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 106

Figure 1: The map of North Shewa zone and Debre Birhan (Right), and Ethiopia (Left) (Source: [70])

The climatic condition is characterized by the presence of biannual rainfall (short and long) and the dry season which

is relatively cool temperature. The rainy season of this area extends from February to April and June to September while the

dry season extends from November to January. The mean annual temperature of Debre Birhan is 15.84 oC, where the

minimum and maximum temperature is 6.1 o

C and 19.9 o

C, respectively. The average annual rain fall is 1728 mm and

relative humidity is 62.3%. Debre Birhan and the surrounding areas have apparently a well spread rainfall throughout the

year. The minimum (1.7 o

C) and maximum (21.60 o

C) temperature are registered in November and July, respectively [33].

In literatures, minimum temperature about 10 o

C and maximum temperature below 30 o

C are favorable to parasite

development and egg hatching [34].

2.2. Study population

Cattle and sheep brought for slaughter were the study animals with different body condition category of both sexes

that were slaughtered in Debre Birhan municipal abattoir and private hotels. Cattle and sheep slaughtered at Debire Birhan

municipal abattoir and in hotels were studied for the presence of lungworms by standard post-mortem examination methods

[35]. The sex, age and body condition of all animals included in the study were recorded during the study. The body

condition scoring was classified in to three categories as poor, moderate and good. As most bovines being slaughtered reach

maturity, age comparison was unavailable, but in sheep age comparison is available in this study [36; 37].

2.3. Sampling method and sample size determination

Simple random sampling technique where each individual is chosen entirely by chance was used as the sampling

strategy to collect all the necessary data from abattoir survey of the study. An investigation was carried out on cattle and

sheep by random selection with special emphasis on animals coming from grazing. To accommodate the sample size for this

study random sampling was applied for study cattle and sheep of any age and sex slaughtered in Debre Birhan municipal

abattoir and private hotels for post-mortem lung inspection. The desired sample size for the study was determined using the

formula described by Thrusfield [38].

n = 1.962 Pexp (1-Pexp)/d

2

Where

n = required sample size

Pexp = expected prevalence

d = desired absolute precision

1.962 =

z- value for 95% confidence interval

As there are no previous studies which establish the percentage and the risk factors of lungworm infestation of sheep

and cattle as a whole, the sample size was determined by taking the occurrence of 50% lungworm infestation. Accordingly

384 animals were sampled, but in order to increase the precession 400 study animals were used. In study undertaken on the

prevalence of lungworm in sheep alone, the prevalence of lungworm was found to be 56.3% in 2013/4 [25].

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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 107

2.4. Study design and sample collection methodology

A cross-sectional investigation on the occurrence of lungworms in ruminants of various age group, sex, body

condition score and sampled during different seasons was carried out from November, 2017 to April, 2018. In addition, the

degree of lungworm burden (degree of parasitic infestation) [39], and the species of the lungworm parasites were

determined by standard methods of post-mortem examination.

2.4.1. Postmortem examination

During ante-mortem examination each of the study animals were given an identification number by a paint mark on

their body. Detail records about the species, age, sex and body conditions of the study animals were performed using data

collection format (Annex 3). While during the postmortem examination, lungs were examined first by visual inspection,

palpation and then finally systemic incision to appreciate the presence, the size (the burden) and the species of lungworm

[40]. Each lung from study animals was inspected by incising it starting from trachea down to bronchi and bronchioles, and

then making multiple deep incisions of the lobes with a number of small sub cuts. The recovered worms were kept in 70%

alcohol and then were transferred to laboratory for examination. Adult parasites were examined under the stereomicroscope

for determining the degree of lungworm parasitic burden; [41; 42] and the identification (classification) of adult lungworm

parasites to the species level as has been done previously [43].

2.5. Data management and statistical analysis

The data that was generated entered into Microsoft excels spread sheet and summarized using descriptive statistics.

Many attribute data that was imported to database system includes; host risk factors including species, sex, age and body

condition of the sampled animals, the season of the year and examination result including the degree of parasitic infestation

and lungworm species. The occurrence of lungworms was calculated by dividing the number of animals affected to the total

number of animals examined. Variation in the percentages of lungworms between species, sex, age, body condition and

season of the year was determined by using logistic regression statistics. Statistically significant variation was considered to

exist when p-value is less than 0.05. The association between the percentage of lungworms, degree of lungworm infestation

and the hypothesized risk factors (animal species, sex, age, body condition and season of the year) was analyzed by using

logistic regression statistics analysis.

3. Results

3.1. Percentage of lungworms

Among 400 animals (sheep and cattle) examined for the presence of lungworms 83 (20.8%) were positive. Out of

204 sheep and 196 cattle examined for lungworms, 83 sheep (40.7%) and zero cattle (0%) were found positive. A

significant difference was observed in the occurrence of lungworm between sheep and cattle (P- value of 0.000, where p <

0.05). Dictyocaulus filaria was the only species of lungworm identified in sheep (Table 1).

Table 1: Percentages of lungworms in sheep and cattle slaughtered at Debre Birhan municipal Abattoir and private hotels

(Ref: Reference Category; CI: Confidence Interval; OR: Odds Ratio)

Species of the

Animal

No of animals

examined

No of animals

positive Percentage OR (95% CI) P-valve

Sheep 204 83 40.7 1 (Ref)

Cattle 196 0 0 0.01 (0.5-0.9) 0.000

Over all 400 83 20.8

3.2. Overall percentage of lungworm in sheep by risk factors

Different potential risk factors were evaluated in relation with the percentages of lungworm with logistic regression

statistical analysis in order to assess association between individual risk factors and presence of lungworms in sheep.

Among the presumed risk factors, age and body condition of the sheep and season of the year were found to have a

significant association with the prevalence of D. filaria (p<0.05), on the other hand the sex of the animals never showed

significant effect on the occurrence of lungworm in sheep (Table 2).

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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 108

Table 2: Percentages and logistic regression statistical analysis of ovine lungworm against hypothesized risk factors

Variables No of animals

examined

No of animals

positive Percentage OR (95% CI) P-valve

Sex

Male 114 47 41.2 Ref

Female 90 36 40.0 0.9 (0.5-1.7) 0.765

Over all 204 83 40.7

Age

Adult 142 49 34.5 Ref

Young 62 34 54.8 2.2 (1.2-4.2) 0.014

Over all 204 83 40.7

Body condition

Good 54 14 25.9 Ref

Medium 88 33 37.5 1.5 (0.7-3.2) 0.324

Poor 62 36 58.1 4.1 (1.8-9.4) 0.001

Over all 204 83 40.7

Season of the year

Autumn 70 36 51.4 Ref

Winter 84 34 40.5 0.6 (0.3-1.2) 0.173

Spring 50 13 26.0 0.3 (0.1-0.7) 0.005

Over all 204 83 40.7

Beyond assessing the occurrence of lungworm infection and its’ association with hypothesized risk factors, this study

also showed the parasitic burden (degree of parasitic infestation). The study showed that majority of animals were with

moderate degree (39.8%) and heavy (36.1%) degree of lungworm infestation and the rest 24.1% of them were with light

degree of lungworm burden (Table 3).

Table 3: Overall proportion of the degree of lungworm infestation in sheep slaughtered at Debre Birhan municipal abattoir

and private hotels

Degree of lungworm infestation No of sheep positive for lungworm Proportion (%) of degree of

infestation

Low 20 24.1

Moderate 33 39.8

Heavy 30 36.1

Over all 83 100

The result of the present study revealed that was no variation in parasitic worm burden between male and female

animals (p>0.05) (Table 4). Young sheep tend to possess significantly a higher moderate (27.42%) and heavy (17.74%)

degree of lungworm burden (P<0.05) than adult animals with odd ratio of 2.3. Statisitically significantly higher lungworm

burden was observed in sheep with poor body condition score (p>0.001) than those sheep with medium and good body

condition scores (Fig. 2). Likewise, significantly higher (p<0.006) lungworm burden was recorded in sheep during the

Autumn and Winter seasons of the study period than in Spring season (Table 4).

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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

Zambrut

Zambrut.com. Publication date: March 13, 2019.

Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 109

Table 4: Logistic regression analysis of hypothesized risk factors against the degree of lungworm burden

Risk factors

No of animals

examined Degree of parasitic infestation OR (95% CI) P-valve

Low Moderate Heavy

Sex

Male 114 8 (7.02%) 24 (21.05%) 15 (13.16%) Ref

Female 90 12 (13.33%) 9 (10.00%) 15 (16.67%) 0.9 (0.4-1.6) 0.859

Age

Adult 142 14 (9.86%) 16 (11.28%) 19 (13.38%) Ref

Young 62 6 (9.68%) 17 (27.42%) 11 (17.74%) 2.3 (1.2- 4.2) 0.007

BCS

Good 54 5 (9.26%) 7 (12.96%) 2 (3.70%) Ref

Medium 88 7 (7.95%) 15 (17.05%) 11 (12.50%) 2.3 (1.1-4.4) 0.014

Poor 62 8 (12.90%) 11 (17.74%) 17 (27.42%) 2.0 (1.4-3.0) 0.001

Season

Autumn 70 10 (14.29%) 15 (21.43%) 11 (15.71%) Ref

Winter 84 5 (5.95%) 13 (15.48%) 16 (19.05%) 0.6 (0.3-1.2) 0.175

Spring 50 5 (10.00%) 5 (10.00%) 3 (6.00%) 0.5 (0.4- 0.9) 0.006

Figure 2: The relationship between body conditions with the degree of parasitic infestation

Heavy parasitic burden has a marked increase in animals in poor body condition (27.42%) followed by medium body

condition animal (12.50%); while, in animals with good body condition (3.70%), it was rarely occurred (Fig. 2). Heavy

degree of parasitic infestation also rises in the seasons when there are available infective larvae (Autumn 15.71%, Winter

19.05%, Spring 6.00%) due to the effect of climatic condition.

4. Discussion

Lungworm is the common health problem in ruminants particularly; in small ruminants and is associated with

significant economic losses due to unthriftness, loss of body condition and morbidity. This study revealed high percentage

of lungworms in sheep slaughtered at Debre Birhan municipal abattoir and private hotels which can represent the

occurrence and percentage of the disease caused by lungworms in and around Debre Birhan. However, the overall

percentage (0%) lungworms in cattle might not be representative of lungworm in cattle in the study area. Because cattle

slaughtered at Debre Birhan abattoir were mostly brought from feedlots which had low exposure to the disease [44; 45].

Furthermore, usually the owners of cattle kept for fattening normally treat these animals with broad spectrum

anthelmintic to get the possible maximum weight gain that significantly reduces the chance of lungworms. In agreement

with the present study, zero prevalence of bovine lungworm was already reported in the Kirikkale province of Turkey [46].

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International Journal of Agriculture & Agribusiness ISSN: 2391-3991, Volume 2 Issue 2, page 104 – 114

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Engdawork, A. 2019. Lungworms of Sheep and Cattle Slaughtered at Abattoir ............ 110

Low prevalence of cattle lungworm was already reported [36], who reported 0.5% in Addis Ababa abattoir. There is also

reported 1.5% and 3.1% in Addis Ababa abattoir and Gondar, respectively [28; 29].

The overall percentage of 40.7% lungworm in sheep recorded in this study was high and coincides with previous

prevalence of 43.33% lungworm reported in Dessie zuria [47], 42% in North Gondar Zone [48] and 48% in Addis Ababa

[49]. However, results of the present study is higher than the previous reports [50] in and around Bahir Dar, [51] in Bahir

Dar and [52] in Mekedella district, south east Ethiopia, who reported prevalence of 18.16%, 20.2% and 28.6%, respectively.

On the other hand the percentage reported in this study is lower than those reported [25] in and around Debre Birhan, [27]

around Dessie, Kombolcha and [53] around Chilallo area which reported prevalences of 56.3%, 60.5%, 67.83% and 81% in

sheep, respectively. Such variation in percentages of lungworms in sheep could be attributed to the difference in study type,

number of sample size, study area and month and seasons of the year of sample collections by different studies.

Dictyocaulus filaria was the only species of lungworm identified in the present study. The small lungworms, P.

rufescens and M. capillaris, were not detected. The absence of small lungworms in the present study area could be

associated with their life cycle and the season of the study. Unlike D. filaria , which has a direct life cycle, P. rufescens and

M. capillaris have an indirect life cycle requiring a molluscan intermediate host to complete their development [19]. As this

study was conducted in relatively non rainy seasons, the climatic conditions in the study area might not be conducive for the

survival and breeding of the intermediate hosts. In agreement with this finding, [9] in and around Wollayita Sodo reported

that D.filaria was the only lungworm species. Many other previous studies [26; 54; 55; 11] also reported D. filaria as the

predominant species circulating in Ethiopian sheep and goats managed under traditional husbandry system although mixed

infections with the small lungworms was reported by some previous investigators at low proportions. In contrast, other

studies reported the preponderance of the small lungworms over D. filaria [23; 24; 12].

The absence of significant (p>0.05) difference in the percentages of lungworm between male and female sheep using

logistic regression analysis in the current study is in agreement with previous researchers [25; 9], who reported insignificant

difference between sex groups. However, a result of the present finding is not in agreement with the earlier study around

Bahir-Dar [56], in six districts of Wollo [57] and in Gojam [51], who reported significant variation between sexes. These

variations among different studies probably reflect the fact that improper distribution of sample selection between the two

sexes. For example in study reported earlier, there were 179 males and 277 females, around 100 additional females over the

number of males [51].

The observation of significant variation between age (young and adult) groups (P<0.05) in this study agrees with

previous researchers, who reported significant difference among age groups [23; 58; 27; 29]. But there was a study that

reported insignificant difference between age groups (young, adult and old sheep), this difference might reflect the

variations regarding the cut point for age classification of sheep or other types unforeseen factor [59].

The observation of sheep with poor (58.06%) or moderate (37.50%) condition were 3 times more likely to shed D.

filaria with an odd ratio of 4.1 and 1.5, respectively than those in good (25.93%) condition might be attributed to the

nutritional status of the animals. This study was conducted during the dry season where feed shortage is a serious problem

for small ruminants kept under extensive management system in Ethiopia. Therefore, during the dry season free-ranging

animals are not able to meet their maintenance requirements, and lose a substantial amount of weight [60]. It is well

documented fact that poor nutrition lowers both the resistance (ability to resist the parasites) and resilience (ability to

tolerate or ameliorate the effects of the parasites) of the animal thus enhancing the establishment of worms and increasing

the prevalence in sheep with poor body condition score [61].

The observation of significantly higher percentages of lungworms in sheep with poor body condition in the present

study agrees with many other previous reports, which includes earlier reports, who reported prevalence of 64.5%, 25.13%

and 18% in poor, medium and good body condition, respectively in and around Tseadaemba [62]; There was also a reported

prevalence of 79.1%, 52.1% and 30.9% in poor medium and good body condition respectively in Assela area [63; 64]. This

may be due to, immune suppression in sheep with poor body conditions, concurrent infection by other parasites including

GIT helminthes and/or malnutrition that reduce the ability of the animal to resist or ameliorate the infection [65]

The findings of the highest percentage of D. filaria during November in Autumn (51.4%) and Winter (40.48%) in the

present study is in agreement with the previous reports by other researchers [66; 67; 23; 24; 68). This suggests that damp

and cool environment is very suitable for the development of D. filaria and third stage larva (L3) is resistant to cold [69].

The absence of significant variation in the load lungworm of infestation between male and female sheep in the

present study showed similar pattern in lungworm occurrence in both sexes. The possible explanation for the finding of

3.70%, 12.50% and 27.42% heavy parasitic infestation in good, medium and poor body condition sheep, respectively in the

resent study could be an increase in degree of pasture contamination in extensive system of production may increase degree

of exposure, so result in high degree of parasitic burden [5]. In addition, the reason for this could partly be due to the fact

that poorly nourished animals appeared to be less competent in getting rid of lungworms although it is not usual for well-fed

animals to succumb to the disease provided the right environmental conditions are available [65].

The finding of heavy degree of infestation during the Autumn (15.71%) and winter (19.05%) while minimal heavy

parasitic burden (6.00%) during the Spring was due to the highest availability of active infective lungworm larvae in

Autumn and Winter as the climatic condition favors them. This allowed sheep to ingest large amount of infective larvae.

Late summer/autumn is the key risk period for young animals so treat at intervals during this time, according to the

anthelmintic used [11; 10].

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5. Conclusion and Recommendation

The current study revealed that the overall occurrence of D. filaria was 40.7% in sheep and zero percent of in cattle.

The main reason assumed for zero percent occurrence of bovine lungworm is that, cattle brought for slaughter comes from

feedlot and possibly received broad spectrum antihelimentics deworming. While, most of the sheep brought for slaughter

comes from rural areas that graze in a free range, the probability for presence of the parasite in the lung was high. D. filaria

is the only ovine lungworm species isolated in the current study. The probable reason for this is D. filaria has a direct life

cycle. Compared with the Dictyocaulus filaria, transmission of P. rufescens and M. capillaries are epidemiologically

complex event involving host, parasite and intermediate host. There was no significant difference in lungworm prevalence

between male and female animal. Age (young and adult), body condition (poor, medium and good) and season of the year

(Autumn, Winter and Spring) were significantly associated with percentages of lungworm in sheep. There was found

seasonal variation in parasitic load, significant heavy degree of infestation was observed in autumn and winter. Sheep with

good body condition harbor lower parasite than sheep with medium and poor body condition. Further research is required to

investigate if improving the nutritional status, thereby improving BCS, will result in lower occurrence of lungworm.

Based on the aforemetioned points, the following recommendations are forwarded:-

Prohibition of animals from grazing early in the morning and evening when there is high activity of larvae due to

moisture when pasture contamination is very high.

Strategic anthelmintic drug treatment should be implemented at the beginning of rainy season and at the end of rainy

season could appear to be most effective.

Further studies are needed to clarify issues regarding seasonal variations of lungworms in all domestic animals

6. Acknowledgements

First and foremost I would like to praise the Almighty GOD, the most exalted, the most merciful and the most

gracious, who explores me throughout my life, making me a curious being and endowed me with the potential to lead my

life. My special thanks go to the Blessed Virgin Mary, Whose praying saved me.

I would like to express my deep and sincere appreciation and thanks to my advisor, Dr. Bersissa Kumsa (DVM,

MSc, PhD, Assoc. Professor), for his valuable advice, encouragement, guidance and intellectual support throughout my

work in completing my thesis research.

My heartfelt and deepest thanks go to all my families, particularly my beloved mother Alemnesh Demerew and my

father Engdawork Gebrekidan who sacrifices a lot for me. My deepest gratitude also goes to all my lovely brothers and

sisters, who provided me with the necessary moral and financial support. Without them I cannot have any success. I would

like to express my deep gratitude to all my classmates, and my friends for their moral support and assistance.

7. List of Abbreviations

BCS Body condition score

CI Confidence Interval

D.filaria Dictyocaulus filaria

D.viviparous Dictyocaulus viviparous

ESGPIP Ethiopia Sheep and Goat Productivity Improvement Program

FAO Food and Agriculture Organization

GIT Gastrointestinal tract

IH Intermediate host

L1 First stage larvae

L3 Third stage larvae (infective stage)

M. capillaris Muellerius capillaries

No Number oC Degree Celsius

OR Odds Ratio

P. rufescens Protostrongylus rufescens

Ref Reference Category

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