Adimasie, Balemual Abebaw, Atalel, Sisay Assefie: Prevalence of bovine hydatidosis and its economic significance in Debre Tabor Municipal abattoir, South Gondar Zone, Ethiopia
ABSTRACT
Background and Aim:
Hydatidosis is caused by the larval stage of Echinococcus granulosus. It is the most important zoonotic parasite. Dogs are the main definitive hosts, livestock (cattle, buffalo, goat, and sheep) are the intermediate hosts of E. granulosus, and humans are accidental hosts.
Materials and Methods:
Retrospective and cross-sectional studies were conducted to determine the prevalence of bovine hydatidosis and its economic losses in Debretabor municipal abattoirs from July to December 2023 and from January to April 2024 April, respectively. A total of 384 cattle were examined by the routine activities of ante-mortem and postmortem examination.
Results:
The present finding revealed that the overall bovine hydatidosis prevalence was 43.4%. Similarly, the prevalence of the parasite in male and local breed animals was 93.0% (357/384), and 81.0% (311/384) as compared to females and crossbreed animals, respectively. Female animals with sterility, reproductive problems, or an emergency case certificate were permitted to be slaughtered in the abattoir. Bivariable and multivariable logistic regression analysis was made to identify the association between factors and infectivity with hydatidosis. Variables as origin, age, and body condition were significantly associated with hydatidosis infection at 95% CI (1.603 ± 3.913, p-value=0.000), (0.227 ± 0.623, p-value=0.000), and (1.157 ± 3.826, p-value=0.015), respectively. There was no significant difference between other variables. The infection and distribution of hydatid cysts were different in different organs. The higher rate of infection and distribution were found in the lung (21.3%), liver (13.2%), and both in lung and liver (5.2%), respectively, while the infection rates were very low in the spleen (2.3%), kidney (0.8%), and heart (0.5%).
Conclusion:
The condemned organ multiplied by the current average price of the organ collected from the customers indicated that there was significant financial loss. The total economic loss of condemned organ due to hydatidosis in the study area was determined by adding direct total economic loss (127,978.636 ETB or 2245.239 USD$) and indirect total economic loss (6,550,596.36 ETB or 114922.743 USD$). The overall financial loss due to hydatid cyst was 6,678,574.996 ETB or 117,167.96491 USD$ (1 USD$=57 ETB).
KEYWORDS Abattoir; Bovine; Debre tabor; economic loss; hydatidosis; and prevalence
Introduction
Ethiopia is one of the developing countries and known to have the largest livestock population in the continent of Africa [ 1]. The livestock sector contributes about 16.5% and 35.6% of Ethiopian national gross domestic product (GDP) and agricultural GDP, respectively [ 2, 3]. However Ethiopian livestock potential is not appropriately utilized, primarily owing to the existing traditional management systems, limited genetic potential widespread animal diseases are one of the essential concerns for the livestock to lower the contribution of the Ethiopian national economy [ 3, 4].
Hydatidosis (cystic echinococcosis) is caused by the larval stage of Echinococcus granulosus. It is the most widespread parasitic zoonosis. Dogs are the usual definitive hosts whilst many mammalian species can be used as intermediate hosts, like domestic animals and man [ 5, 6]. Hydatidosis occurs throughout the world and causes considerable economic losses and public health problems [ 7]. In North Africa, an average of 600–700 cases of hydatid cyst is recorded in Algeria annually, and it is responsible for about 2,000 cases of surgery each year in Tunisia. In the same country, the annual surgical incidence rate was 15/10,000 inhabitants [ 6, 8]. The public health importance of echinococcosis includes the cost of hospitalization, medical and surgical fees, losses of income and productivity due to temporal incapacity to work, and social consequences, due to disability and mortality [ 9, 10].
Hydatidosis is one of the highly prevalent diseases in livestock sectors in Ethiopia and echinococcosis in dogs [ 10]. Cystic echinococcosis in farm animals causes considerable economic problems due to the loss of edible livers, and lungs, and significant losses of meat and milk production [ 11]. Hydatidosis has been known and documented in Ethiopia as early as 1970; it is still the major cause of organ condemnation in most Ethiopian abattoirs and leads to huge economic losses in the livestock sector [ 12].
The previous studies reveal that the prevalence of bovine hydatidosis in cattle slaughtered in the Adama municipal abattoir was 46.8% [ 13]; 52.5% were observed at the Shashemenie municipal abattoir [ 14]. In Harar municipality, abattoirs were 44.6, [ 15], and in another study in Harare 11.3% [ 16]. Dalomana municipal abattoir 19.1% [ 17, 18] in Dawa municipality abattoir revealed that 20.05% [ 19]. At Kara-Alo Abattoir PLC, Addis Ababa 25.7% [ 20] and cattle slaughtered at Bahir Dar Municipal Abattoir also was 18.75% [ 21] while cattle slaughtered at North Gondar Elfora Abattoir shows 28% [ 22].
Several reports have indicated that hydatidosis is widely prevalent in the livestock populations of various regions of Ethiopia [ 23], but its status was not known in the Debretabor municipal abattoir which is found in Amhara, Ethiopia. Even though raw beef consumption habit feeding of condemned organs to stray dogs and the distribution of backyard slaughtering practices are common in the area. However, by considering the public health significance, and the economic losses of the disease it had been very important to investigate the prevalence and evaluate its economic losses had a great relevance to the country. This in turn would help to establish appropriate control and preventive measures by determining the prevalence of bovine hydatidosis and its economic significance in the study area. Objectives: To study the prevalence of bovine Hydatidosis and to evaluate the economic significance of bovine hydatidosis in the Debre Tabor Municipal abattoir.
Materials and Methods
Study area
This study was conducted in the Debretabor municipal abattoir of South Gondar Zone, Amhara Regional State, Ethiopia ( Fig. 1). The study period was from July 2023 to April 2024. The area is found 100 km from, Bahir Dar and 664 km from the capital city Addis Ababa. The city has 6 rural kebeles and three sub-cities with an altitude from 1,500 to 4,231 MASL and a 13°C–27°C temperature range. The annual rainfall ranges from 600 mm to 1,200 mm. The total human population of the town is 201,787 (102,109 males and 99,678 females) and 39,882 households (31,485 males and 8,397 females). Both Governmental and private health and veterinary facilities exist in the city. The city contains one comprehensive hospital, four health centers, five private higher clinics, six medium clinics, thirteen pharmacies, six veterinary clinics, and seven private veterinary pharmacies [ 5].
Figure 1.
Map of Debre Tabor Town, South Gondar Zone, Ethiopia (created by QGIS version 3.10.2 software).
Sample size determination
The sample size was calculated by considering a 95% confidence interval with a 5% desired absolute precision [ 17]. Using a systematic sampling method, the samples were selected from cattle registered for slaughtering following the ante-mortem inspection.
where N=required sample size; pexp=expected prevalence; d=desired absolute precision. The study only included 384 cattle but did not include all bovines slaughtered in the study period.
Study Population
Diverse breeds of healthy cattle with varying body conditions, sex, and age groups were brought from Fogera, Adiszemen, Fareta districts, and surrounding Debre Tabor to the Debre Tabor municipal abattoir. The animal ID (identification numbers) was written on the body of the study animals with color markers by their owners for identification. Female animals with sterility, reproductive problems, or an emergency case certificate were permitted to be slaughtered in the abattoir.
Study design and methodology
The study was conducted using retrospective and cross-sectional study design. The retrospective study was conducted to collect the recorded data from the abattoir case record book on the causes of organ condemnation due to hydatidosis in the last 6 months by systematic sampling of the initial numbers of each day from July 2023 to December 2023. A qualified meat inspector inspected all slaughtered animals and all observed lesions were recorded on the record book of the abattoir. A cross-sectional study (active abattoir survey) was conducted from January 2024 to April 2024 using the regular meat inspection procedure to identify correctly the hydatid cyst as the major cause of organ condemnation. In this study, 3 days per week were the common working days associated with fasting days. On the working day, all antemortem and postmortem examinations of slaughtered cattle were performed correctly. The number of slaughtered animals was not constant.
Ante-mortem inspection
During the ante-mortem inspection, each of the study animals was labeled with an identification number. Age, origin, sex, and body condition scoring of the study animals were also recorded. The body condition score of the study animals was classified into poor, medium, and good body condition categories [ 18]. Young and adult age categories were encountered based on their dentition.
Post-mortem examination
Postmortem examination was carried out through visual inspection and palpation of visceral organs (lung, liver, heart, spleen, and kidney), and the presence of hydatid cysts in different organs was recorded [ 23]. The number and type of organ condemned were recorded in the Debretabor municipal abattoir.
Financial loss assessment
The financial loss of condemned organs due to bovine hydatidosis was assessed using the formula [ 24]. The average market price of organs in the study area during the study period was recorded as liver (80 Ethiopian Birr (ETB)), lung (75 ETB), heart (55 ETB), kidney (60 ETB), and spleen 15 ETB the parameters considered. The total financial loss was calculated by the sum of direct and indirect losses due to hydatidosis.
Direct organ condemnation
The total economic loss due to organ condemnation was calculated as (PI1 × Tk × C1) + (PI2 × Tk × C2) + (PI3 × Tk × C3) + (PI4 × Tk × C4). Where PI1=Percent involvement of liver out of the total examined; PI2=Percent involvement of lung out of the total examined; PI3=Percent involvement of heart out of the total examined and PI4=Percent involvement of kidney out of the total examined. C1=Average market price of liver; C2=Average market price of lung; C3=Average market price of heart; C4=Average market price of kidney and Tk=Average annual slaughter of bovines. Carcass weight loss due to hydatidosis was 5% [ 25]. The average slaughter rates of animals at the Debre Tabor municipal abattoir were calculated from the 2-year slaughter animals counted from the record book and the average of the 2 years was 3,730 + 4,250=7,986/2=3,993. The average carcass weight (dressing percentage) of the Ethiopian zebu cattle breed was 126 kg and the carcass value of beef during the study period was 600 ETB/kg in Debretabor. The annual carcass weight loss due to hydatidosis was:
ACWL=ASCR × CW × BC × CP
ACWL=ACSR × 126 × 5% × BC × CP
where: ACWL=Annual cost from carcass weight loss; ASCR=average slaughtered cattle per annual in the study area; CWL=carcass weight loss in the individual=(126 × 5%); APC=average price of 1 kg carcass at study area; CP=the current prevalence rate of hydatidosis at Debretabor municipal abattoir were 43.4. Therefore, the total financial loss due to hydatidosis was the sum of organ condemned in birr (direct) and the cost of carcass weight (indirect) losses.
Data management and analysis
The data that was collected from the selected area was properly recorded, cleaned, and organized using a Microsoft Excel 2010 spreadsheet. The prevalence of hydatidosis was calculated by dividing the number of hydatid-positive animals by the total number of animals examined. The associations of explanatory variables (age, sex, breed, body condition scores, and origin of animals) with the disease were assessed using logistic regression. All statistical analyses were done using statistical software for social science (SPSS) version 20. A probability (p) value less than 0.05 was set as statistically significant.
Results
A total of 384 cattle were examined by using retrospective and active abattoir surveys by the routine activities of ante-mortem and postmortem examination. Out of the total slaughtered animals, 167 (43.4 %) were positive with hydatidosis. Based on the origin 226 (59%) were slaughtered from Adis zemen and Fogara. In the abattoir male animals slaughtered at higher frequency 357 (93.0%) than females. Female animals with sterility, reproductive problems, or an emergency case certificate were permitted to be slaughtered in the abattoir. In the abattoir, 311 (81%) of slaughtered animals were local breeds, and 291 (75.8%) were adult animals older than 5 years. Animals having poor, medium, and good body conditions were slaughtered at a frequency of 84 (21.8%), 143 (37.1%), and 158 (41.0%), respectively ( Table 1).
Table 1.All over results of the animals slaughtered and examined proportionally in Debretabor municipal abattoir in 2023–2024.
Variables |
N |
Percentage |
Health status of animals |
Negative with Hydatidosis |
217 |
56.6% |
Positive with Hydatidosis |
167 |
43.4% |
Origin of animals |
Debretabor and Fata zuriya |
158 |
41.0% |
Adis zemen and Fogara |
226 |
59.0% |
Sex |
Male |
357 |
93.0% |
Female |
27 |
7.0% |
Breed |
Crossbreed |
73 |
19.0% |
Local |
311 |
81.0% |
Age group |
<=5 years |
93 |
24.2% |
>=5 years |
291 |
75.8% |
Body condition scoring |
Poor |
84 |
21.8% |
Medium |
143 |
37.1% |
Good |
158 |
41% |
Number and types of organs examined and their health status
The infection and distribution of hydatid cysts were different in different organs ( Fig. 2). The higher rate of infection and distribution (multiple cyst infection) were found in the lung and liver at the frequency of 82 (21.3%), and 51 (13.2%), respectively. Both Liver and lung infections accounted for 20 (5.2%). The infection rates were very low in the spleen, kidney, and heart at the frequency of 9 (2.3 %), 3 (0.8 %), and 2 (2.5 %), respectively, as described in Table 2.
Figure 2.
Cattle liver with a cross-section of hydatid cyst [ 10].
Table 2.Number and types of organs examined and their health status in the Debretabor municipal abattoir in 2023–2024.
No, the types of organs examined |
Health status of organs |
Percent |
Healthy organs |
217 |
56.6 |
Spleen |
9 |
2.3 |
Kidney |
2 |
0.5 |
Heart |
3 |
0.8 |
Lung |
82 |
21.3 |
Liver |
51 |
13.2 |
Liver and lung |
20 |
5.2 |
Total |
384 |
100.0 |
The number and types of organs condemned its average unit price and economic loss
Hydatidosis is a zoonotic disease that transmits from animals to humans. The hydatid cyst infects many organs of bovines slaughtered in the Debretabor municipal abattoir. Due to the zoonotic importance organs infected by hydatid cysts were necessarily condemned and not approved for human and animal consumption. In the study area, the infection rates were encountered in the lungs, liver, kidney, heart, and spleen. The organs infected by hydatidosis were condemned to protect the community and animals [ 26]. The economic losses due to organ condemnation encountered in the abattoirs were 82 (21.3%), 51 (13.2%), and 20 (5.2%) in lung, liver, and both lung and liver, respectively. Spleen, heart, and kidney were condemned at lower rates 9 (2.3%), 3 (0.8%), and 2 (.5%) consequently in the study period. The condemned organ multiplied by the current average price of the organ collected from the customers (hotels, ristorantes, and abattoir workers) indicated a huge financial loss due to hydatidosis in the study area. The economic loss due to hydatidosis in the study area was determined by direct total economic loss TEL=127,978.636 and by indirect total economic loss 6,550,596.36. The overall financial loss due to hydatid cyst was the sum of the indirect loss and direct economic loss 127,978.636 + 6,550,596.36=6,678,574.996 ( Table 3).
Table 3.Number and types of organs condemned their average unit price and economic loss description in Debretabor municipal abattoir in 2023–2024.
Number and the types of organs condemned |
Percent involvement(PI) |
Direct total economic loss TEL=(PI1 × Tk × C1) + (PI2 × Tk × C2) +(PI3 × Tk × C3) + (PI4 × Tk × C4 ) |
Indirect total economic loss ACWL=ACSR × CL × BC × CP |
Healthy organs |
217 |
56.6 |
Unit price |
|
3993*.434 *600birr*0.05%*126 kg=6,550,596.36 |
Spleen condemned |
9 |
2.3 |
16 |
0.023*3,993*16=1,464.424 |
Kidney condemned |
2 |
0.5 |
60 |
0.005*3,993*60=1,197.9 |
Heart condemned |
3 |
0.8 |
55 |
0.008*3,993*55=1,756.92 |
Lung condemned |
82 |
21.3 |
80 |
0.213*3,993*80=68,040.72 |
Liver condemned |
51 |
13.2 |
75 |
0.132* 3,993*75=39,530.7 |
|
Liver and lungs are condemned |
20 |
5.2 |
75+80 |
0.052*3,993*77=15,987.972 |
|
Total |
384 |
100.0 |
127,978.636+6,550,596.36=6,678,574.996 |
*Superscripts describes multiplication or times during dict and indirect economic loss analysis.
Bivariable and multivariable logistic regression results
Bivariable and multivariable logistic regression analysis tests were performed to determine the association between factors such as origin, age, and body condition and the prevalence of bovine hydatidosis. Age and body condition scoring was significantly associated with the prevalence of Hydatidosis on both bivariable and multivariable logistic regression ( Table 4) at 95% CI (1.603 ± 3.913, p-value=0.000), (0.227 ± 0.623, p-value=0.000), and (1.157 ± 3.826, p-value=0.015), respectively. Origin, age, and body condition scoring of the animals were significantly associated with bovine Hydatidosis infection.
Table 4.Bivariable and multivariable logistic regression results of factors associated with infection with hydatidosis in Debretabor municipal abattoir 2023–2024.
Health status of animals with Hydatidosis |
Negative |
Percent |
Positive |
Percent |
95% CI |
p-value |
217 |
56.6% |
167 |
43.4 |
|
|
Origin of animals |
Debretabor and Fata zuriya |
158 |
41.0% |
48 |
30.37 |
1.603 ± 3.913 |
0.000 |
Adis zemen and Fogara |
226 |
59.0% |
119 |
52.42 |
. |
. |
Sex |
male |
357 |
93.0% |
151 |
42.17 |
0.721 ± 3.920 |
0.229 |
female |
27 |
7.0% |
16 |
59.25 |
. |
. |
Breed |
Crossbreed |
73 |
19.0% |
39 |
53.42 |
0.360 ± 1.080 |
0.092 |
Local breed |
311 |
81.0% |
128 |
41.02 |
. |
. |
Age group |
<=5 years |
93 |
24.2% |
57 |
61.29 |
0.227 ± 0.623 |
0.000 |
>=5 years |
291 |
75.8% |
110 |
37.67 |
|
|
Body condition scoring |
Poor |
84 |
21.8% |
45 |
53.56 |
1.157 ± 3.826 |
0.015 |
Medium |
143 |
37.1% |
64 |
44.76 |
0.511 ± 1.345 |
0.448 |
Good |
157 |
41.0% |
58 |
36.9 |
. |
. |
Discussion
The overall prevalence of hydatidosis in cattle slaughtered in the Debretabor municipal abattoir during the study period was 43.4%. The current finding is in close agreement with that reported in the Adama municipal abattoir was 46.8% [ 13]; 52.5% at the Shashemenie municipal abattoir [ 14, 27]; 44.6% in the Harar Municipality Abattoir [ 15]; 47.2% in backyard slaughtering at southern regions of Ethiopia [ 16]. The present finding was higher than the previous works reported from different parts of the country ranging 11.3% from the study’s reveals in Harare [ 28]. Other studies were also reported as 19.1% in Dalomana municipal abattoir [ 18]; 20.05% in Dawa municipality abattoir [ 19]; 18.75% at Bahir Dar Municipal Abattoir [ 21]; 25.7% Kara-Alo Abattoir Addis Ababa [ 20]; and 28% North Gondar Elfora abattoir [ 22]. The prevalence of bovine hydatidosis among the different studies in different areas and abattoirs was different due to the difference in availability and exposure of the final hosts to the infected intermediate hosts and vice-versa [ 29].
In the present study, the variables such as origin, age, and body condition of animals were significantly associated with hydatidosis, both in bivariable and multivariable logistic regression. Origin, animal’s age, and body condition of the animals were strongly associated with hydatidosis as a p-value close to zero shown in Table 4. In this study, animals originating from far and in debre tabor were highly infected with Hydatidosis than other origins were coming to the abattoir. This is due to improper disposal of abattoir waste products in Debre Tabor municipal abattoir, using a widespread backyard slaughtering system in the area and the presence of stray dogs in the town freely consume abattoir by-products, which disseminate the diseases into neighbor kebeles [ 5]. This finding result is agreed to Yalew [ 30].
The rate of infection of Hydatidosis in different age groups of cattle had a significant association ( p < 0.005). Animals older than 5 years of age were highly infected with CE (cystic echinococcosis). The difference in infection rate could be mainly due to longer exposure time to hydatid cysts and decreased immunity as older. This finding is agreed to the following finding [ 8, 28]. Animals having poor body conditions were found to have higher cysts burden, which can be explained due to the retarded growth, weight loss, and moderate to severe infection [ 25].
In the present study, the highest infection rate occurred in the lung followed by the liver than other organs examined during the study period. This finding agrees with the study [ 15, 20, 26, 31]. This high infection rate in the lung is due to the possibility of the hexacanth embryo entering the lymphatic circulation and being carried via the thoracic duct to the lung [ 29]. On the other hand, the higher infection rate in the lung and liver as compared to the other organs may be due to the reason that the liver and lung possess greater capillaries so that the ingested hexachant or oncospheres primarily affect the hepatic and pulmonary system sequentially before any other peripheral organ invasion [ 32].
The total economic loss from organ condemnation and carcass weight loss due to bovine hydatidosis was determined by direct total economic loss [TEL]=127,978.636 and by indirect total economic loss 6,550,596.36. The overall financial loss due to hydatid cyst in the study period was the sum of indirect loss + direct economic loss=127,978.636 + 6,550,596.36=6,678,574.996 ETB (Ethiopian birr) or [117,167.96491 $ USD]. The current finding is close to [ 14, 15, 26, 27]. The results of the present study revealed that bovine hydatidosis resulted in significant economic loss in the study area.
Conclusion
The present study showed that the prevalence and estimated financial loss due to organ condemnation of bovine hydatidosis were high. It was also evident that the lung and liver were the two organs with the highest cystic echinococcosis prevalence as compared to other organs, which potentially led to a higher rate of condemnation of these organs. Therefore, control of the parasite directed both in the intermediate and definitive host should be carried out. Additionally, appropriate meat inspection, proper disposal of infected organs, and deworming of dogs in the study area should be carried out. Appropriate control measures should be taken to stop the sale of infected offals for definitive host consumption. The government should give attention to building abattoirs with good facilities and to control backyard slaughtering activities.
Acknowledgments
The authors wish to sincerely express a profound thanks to co-worker Mr. Beyene Asnakew who is a meat inspector at Debretabor municipal abattoir, for his great help and encouragement during the study period. The authors would also like to thank other staff at the Debretabor Municipal Abattoir for helping in all the processes of working on the research.
Competing interest
The authors declare that, to the best of their knowledge, there is no known conflict of interest associated with this manuscript.
Funding
There is no funding for this research.
Data availability
The material set used in this research article is available from the corresponding author and can be accessed through reasonable request.
Authors’ contributions
Both authors took part in the title suggestion, report writing processes, and manuscript preparation. Sisay Assefie contributed to the conception of the idea, data collection, drafting, and writing of the manuscript. Balemual Abebaw contributed to the interpretation of results and manuscript preparation. Furthermore, both authors are responsible for the accuracy and originality of this work.
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