Prevalence and Associated Risk Factors of Cysticercosis bovis in Bishoftu Municipal Abattoir,Central Ethiopia

Abstract

Background:

Cysticercus bovis has zoonotic implications with economic losses from organ contamination and treatment costs. In developing countries such as Ethiopia, where hygienic standards are low and residents customarily eat raw or undercooked meat, the disease is prevalent.

Methods:

A cross-sectional study was carried out from December 2021 to June 2022 to determine the prevalence of Cysticercus bovis in cattle slaughtered at the Bishoftu municipal abattoir, in central Ethiopia. Study populations for the active abattoir survey were cattle presented to the abattoir for slaughtering and routine meat inspection conditions. The organ namely the tongue, masseter muscle, liver, and triceps muscle were inspected for the presence of C. bovis.

Results:

From a total of 330 cattle, 14 were found to be positive for C. bovis, with an overall prevalence of 4.24%. Based on the origin of the animals, the highest prevalence was recorded at Adama (7.27%), followed by Bishoftu (5.45%), Mojo (5.45%), Borana (3.63%), Dukem (3.63%), and Kaliti (0.00%). Similarly, out of 111 adults and 219 old-aged cattle slaughtered and examined at the abattoir, 4.5%, and 4.11% were positive for C. bovis, respectively. Among tested independent variables, sex, body condition score, age, and origin of animals had no relationships with the prevalence of C. bovis. From the detected organ, the tongue ranks first for the highest number of cysts, followed by the masseter muscle, liver, and triceps muscle, with total cysts of 6, 4, 3, and 1, respectively.

Conclusion:

C. bovis is a prevalent zoonotic parasite disease that causes carcass condemnation; an enhanced understanding of the health consequences of teniasis is required to protect the community.

Keywords

Bishoftu municipal abattoir Ethiopia prevalence

Introduction

Ethiopia has the largest livestock population in Africa, with an estimated 56 706 389 cattle, 29 332 382 sheep, and 29 112 963 goats.¹ However, national income and livestock populations were not comparable due to different factors. Consequently, livestock productivity is decreasing due to major constraints such as diseases, the low genetic potential of indigenous cattle, poor reproductive performance, scarcity of nutrition, and a lack of good husbandry practices.²

Among its constraints, livestock diseases cause extensive financial waste as a result of direct and indirect economic losses, which is a major concern for the livestock industry.³ Among highly prevalent diseases, Cysticercus bovis is the most common, resulting in economic losses and public health problems.⁴ It is a parasitic infection of cattle caused by the larval stage (Cysticercus) of the cestode Taenia saginata. This larva is meat-borne, and human infection occurs when raw or undercooked beef is consumed. Cysticercus bovis is a disease that affects the musculature of cattle and is caused by the metacestode stage of the human intestinal cestode and Taenia saginata.³

Taenia saginata is known as the “beef tapeworm” because beef is the main source of infection, it has a cosmopolitan distribution, and it causes anorexia, weight loss, abdominal pain, and digestive upset.⁵ T. saginata has 2 different stages in its life cycle, the intermediate host (cattle) and the final host (human). The larval stage (Cysticercus bovis) occurs in the heart and skeletal muscles of the intermediate host, and the adult worm is located in the intestine of the final host. Cattle are infected when they ingest water or feed on pastures or fodder containing the T. saginata eggs expelled in human feces. Cysticercosis in cattle often has no clinical features, but a heavy infection may cause myocarditis. Human infection occurs by consuming infected raw or semicooked beef.⁶

The infection is a problem in developed countries where considerably rare (ie, undercooked) beefsteak is consumed and is more widespread in developing countries where hygienic conditions are poor and where the inhabitants traditionally eat raw or insufficiently cooked meat. It is important to note that eggs have been demonstrated to survive almost all stages of sewage treatment.⁷ Cysticercosis is an important zoonotic disease in Africa, with a high reported incidence when compared with other continents of the world. The parasite is found in both developed and underdeveloped countries.⁸

Cysticercosis in cattle, caused by C. bovis, is a major cause of economic loss in the beef meat business due to the rejection of infected meat. The distribution of infection differs from that of teniasis in humans. Africa accounted for approximately 40% of the 77 million documented cases of bovine teniasis worldwide. In Ethiopia, several authors have reported its seroprevalence or infection prevalence in a wide range of 2.5% to 89.41% and 3.11% to 27.6%, in humans and cattle, respectively.⁸

The most effective method of diagnosing Cysticercus bovis is postmortem examination. The primary method of detecting Cysticercus bovis in slaughterhouses is a visual inspection of cut muscles at specific predilection sites, such as the external and internal masseter pterygoid muscles, heart, tongue, diaphragm, and esophagus. Therefore, meat inspection is the main public health measure for the prevention of the transmission of T. saginata. The relative public health importance of this parasite, especially to humans and cattle, has necessitated this study to determine the prevalence of C. bovis in cattle slaughtered at the Bishoftu municipal abattoir. It is believed that the cultural habit of eating raw meat in the form of “Kurt”-meat cubes and “Kitfo”-minced meat in Ethiopia has favored the spread of this disease.⁹ Even though different authors have reported its prevalence in different areas at different times, a recently updated report is very important to ensure the surveillance as well as the public health and economic importance of the disease. Therefore, this study aims to determine the prevalence and risk factors of C. bovis in cattle slaughtered at the Bishoftu municipal abattoir.

Materials and Methods

Study area

The study was conducted in Bishoftu, central Ethiopia (Figure 1). Bishoftu is located approximately 45 km southeast of Addis Ababa, just on the escarpment of the Great Rift Valley, and the geography of the area is marked by creator lakes. It is found at 9°N latitude and 40°E longitude at an altitude of 1850 m above sea level in the central highlands of Ethiopia. It has a human population of approximately 95 000. It has a bimodal rainfall pattern, with the major rainy season lasting from June to September (with an estimated 84% of rain) and from March to May having a short wet season with an average annual rainfall of 800 mm. The mean annual minimum and maximum temperatures are 12.3°C and 27.7°C, respectively, with an overall average of 18.7°C. The mean relative humidity is 61.3%.¹⁰ The Bishoftu municipal abattoir are specialized in slaughtering cattle.

Figure 1.

Map of Ethiopia and Oromia region (A) and study area with slaughterhouse location (B).

Study design

A cross-sectional study was carried out from December 2021 to June 2022 to determine the prevalence of Cysticercus bovis in the Bishoftu municipal abattoir in central Ethiopia. Information regarding the age, sex, origin, and body condition score of the animals was recorded during preslaughter.

Study population

The study populations were cattle presented to the abattoir for slaughtering and routine meat inspection conditions. The study animals were brought from surrounding Bishoftu and other districts by traders for slaughter. Depending on where the animals were collected, they were carried to the abattoir by truck or on foot.

Sampling method and sample size determination

Sampling was conducted using multistage random sampling methods. The sample size of the active abattoir survey was determined using the expected prevalence of Cysticercus bovis in the Bishoftu municipal abattoir at 7.8% reported by Geinoro and Beredo,¹¹ with a 95% confidence interval at a desired absolute precision of 5% according to the formula given by Thrusfield.¹² Therefore,

n = \frac{1.9 6^{2} \times Pexp (1 - Pexp)}{d^{2}}

where n is the required sample size, Pexp is the expected prevalence, and d is the desired absolute precision, usually d = 0.05 at a 95% confidence level.

Thus, the required sample size was 110, but 330 cattle were sampled to increase the level of accuracy (triple fold samples) used in determining the updated prevalence.

Abattoir survey

Antemortem and postmortem examinations were carried out for every sampled animal. Before slaughter, 330 cattle were selected using a multistage sampling method for antemortem investigation for the presence of disease or abnormality. Animals were first grouped according to their sex. Then, they were grouped according to their region of origin, followed by their age. The number of animals brought to the slaughterhouse during the study period was taken into consideration when choosing the animals from each age group. Finally, each study animal was chosen at random from a group of animals classified by age (⩽5 years: adult; >5 years: old). Thus, 111 adult and 219 old animals were chosen from each area using multistage sampling. The regions where the animals were brought for slaughter (which are regarded as the animals’ places of origin) were Adama, Bishoftu, Borana, Dukem, Kaliti, and Mojo, and according to their body condition score, they were divided into poor, medium, and good categories.

During the antemortem examination, the study animal was given an identification number. After being slaughtered, the carcasses were examined for C. bovis. The post-mortem examination was carried out in accordance with the Ministry of Agriculture’s¹³ guidelines. It includes visualization, palpation, and incisions. In addition, the examination included a longitudinal incision of the heart from base to apex, 2 longitudinal ventral incisions of the tongue from tip to root, 1 deep incision into both sides of the triceps muscles of the shoulder, a deep incision into the external and internal muscles of the masseter parallel to the plane of the jaw, 3 parallel incisions into the long axes of the neck muscles on both sides, and 1 extensive incision. The results were recorded according to the organs examined.

Data management and analysis

All data collected from the slaughtered cattle were entered into a Microsoft Excel worksheet in 2016 and were analyzed by Pearson Chi-square, or Fisher Exact test where appropriate (STATA-14, Stata Corporation, Texas, USA, 2014). Descriptive statistics, such as percentages, were used to determine the level of organ condemnation. The associations between the various potential risk factors, such as age, origin, sex, and body condition score, of animals were assessed by Pearson Chi-square (X²) or Fisher Exact test, and a P-value <.05 was considered significant.

Results

Prevalence of C. bovis

In the current study, out of 330 inspected cattle, the overall prevalence of cysticercosis was 4.24% (95% CI; 2.52, 7.05).

Role of risk factors for C. bovis

Among 311 males and 19 females slaughtered and examined cattle at Bishoftu municipal abattoir (n = 330), 4.18% of males and 5.26% of females were positive for C. bovis. Similarly, out of 111 adults and 219 old-aged cattle slaughtered and examined at the abattoir, 4.5%, and 4.11% were positive for C. bovis, respectively. Moreover, the prevalence of C. bovis according to origin and body condition score is presented in Table 1. However, the present study revealed that there was no statistical association (P > .05) between the sex, body condition score, origin, and age of animals and the prevalence of Cysticercus bovis.

Table 1.

Prevalence of Cysticercus bovis based on risk factors (n = 330).

Variables	Categories	No. of animals examined	No. of positive animals	Prevalence (%)	Chi-square/Fisher Exact test value	P-value
Sex	Male	311	13	4.18	0.572	.820
Sex	Female	19	1	5.26	0.572	.820
Age	Adult	111	5	4.50	0.028	.866
Age	Old	219	9	4.11	0.028	.866
Body condition score	Good	298	11	3.69	0.173	.316
	Medium	21	2	9.52
	Poor	11	1	9.09
Origin	Adama	55	4	7.27	0.473	.524
	Bishoftu	55	3	5.45
	Borana	55	2	3.63
	Dukem	55	2	3.63
	Kaliti	55	0	.0
	Mojo	55	3	5.45

The tongue with 42.9% cysts ranks first for the highest number of cysts, followed by the masseter muscle at 28.6%, the liver at 21.42%, and the triceps muscle at 7.14%. The abattoir survey analysis indicated that there was a significant variation in the anatomical distribution of C. bovis in the inspected organs of slaughtered animals (Table 2).

Table 2.

Anatomical distribution of cysts among inspected organs and their degree of association.

Variable	Categories	Positive	Prevalence (%)	Fisher exact	P-value
Organs	Tongue	6	42.9	0.000	.0001
	Masseter muscle	4	28.6
	Liver	3	21.42
	Triceps muscle	1	7.14

As indicated in table 3, the univariable analysis revealed that there was no statistically significant association (P > 0.05) between sex, age, body condition score, and origin and prevalence of C. bovis.

Table 3.

Univariable logistic regression output of risk factors and their odds of exposure.

Variables	Categories	No	NPA	OR	95% CI	P-value
Sex	Male	311	13	Ref.
Sex	Female	19	1	1.27	0.16-10.28	.821
Age	Old	219	9	Ref.
Age	Adult	111	5	1.10	0.36-3.37	.866
Body condition score	Poor	11	1	Ref.
	Good	298	11	0.38	0.05-3.26	.380
	Medium	21	2	1.05	0.08-13.08	.968
Origin	Adama	55	4	1.36	0.29-6.38	.697
	Bishoftu	55	3	Ref.
	Borana	55	2	0.65	0.10-4.08	.649
	Dukem	55	2	0.65	0.10-4.08	.649
	Kaliti	55	0	1
	Mojo	55	3	1	0.19-5.18	1.00

Abbreviations: CI, confidence interval; No, number of animals examined; NPA, number of positive animals; OR, odds ratio; Ref, reference cell.

Discussion

In livestock production, Cysticercus bovis is a significant problem. It causes severe economic loss in the meat industry due to meat condemnation or carcass downgrading.¹⁴ The present study revealed that the overall prevalence of C. bovis from the carcasses inspected at the Bishoftu municipal abattoir was 4.24%. This finding agreed with the prevalence rate of 2.59% in Wolaita Sodo,¹⁵ 3.6% in Addis Ababa Municipal Abattoir,¹⁶ 2.93% in Jimma municipal abattoir,¹⁷ and 6.4% in Kombolcha Elfora.¹⁸

However, the present study lowers the prevalence of C. bovis obtained to 26.25% in the Awassa abattoir,⁸ 18.49% in northwestern Ethiopia,¹⁹ 7.5% in the Addis Ababa abattoir,²⁰ and 22.9% in the Hawassa municipal abattoir.²¹ On the other hand, the current C. bovis prevalence was higher than the report of Swai and Schoonman²² 1.49% in the Tang city abattoir, Tanzania. This variation between previous prevalence and current prevalence might be due to differences in agroclimatic conditions, animal size sampled, people living or management systems, and the area from which animals came. In addition, in the routine inspection of beef carcasses, many infestations remain undetected due to the fact that there is a practical limitation to the degree of incision permissible because a grossly visible incision lowers the marketability of the carcass.

The present study has revealed that there was no significant difference between the sex of animals with the prevalence of Cysticercus bovis, and it was lower in males (4.18%) than in females (5.26%). This finding agrees with Teklemariam and Debash⁹ in and around Batu, Ethiopia. However, this finding disagreed with Ibrahim and Zerihun¹⁶ in the Addis Ababa municipal abattoir, where they explained that there was a significant difference (P < .05) in the occurrence of Cysticercus bovis between the sexes of animals. This result could be due to the equal susceptibility of cattle to Cysticercus bovis irrespective of sex. Moreover, the possible reason for this variation of significance among different studies might be the sample size variation between female cattle slaughtered at different municipal abattoirs and females kept in the herd for breeding and milk production and thus rarely sent to slaughter.¹⁶

In the current study, the prevalence of Cysticercus bovis was higher in adult-aged animals (4.5%) than in old-aged animals (4.11%). This finding agreed with the report of Engdaw et al¹⁸ in the Kombolcha Elfora Abattoir but contrary to the report of Teklemariam and Debash⁹. However, the current study showed that there was no significant difference between the ages of animals with the prevalence of Cysticercus bovis. One possible explanation for this variation might be that any age group of animals has similar susceptibility to T. saginata eggs, and most of the animals slaughtered in this abattoir were adults and old and had similar management systems.

In the present study, the prevalence of Cysticercus bovis was higher in medium (9.52%) than in good (3.69%) and poor body-conditioned animals (9.09%). This finding was lower than the report of Netsanet et al³ with medium (14.2%) and good body condition (11.8%). The majority of the animals slaughtered in the abattoir were brought from the fattening systems of the individual farmer. And also the animals from such farms were less exposed to eggs of T. saginata as they grazed on relatively clean defined pasture land, tying the system to the pegs and intensive feeding system in the house for fattening purposes, and used anthelminthic drugs.³ This study showed that there was no significant difference between the body condition of animals and the prevalence of Cysticercus bovis. However, this result disagreed with the report of Netsanet et al³ in Dessie, which showed that there were statistically significant body conditions of the animals with the prevalence of Cysticercus bovis.

Based on the origin of the animals, the highest prevalence was recorded at Adama (7.27%), followed by Bishoftu (5.45%), Mojo (5.45%), Borana (3.63%), Dukem (3.63%), and Kaliti (0.00%). The reason for the overlap rate occurrences in Bishoftu and Mojo as well as in Borana and Dukem might be due to equal sampled cattle and similarity in management systems. The statistical analysis showed that there was no statistical association between the origin of animals and the prevalence of C. bovis. This finding agreed with the reports of Teklemariam and Debash⁹ in Batu, Ethiopia, who reported no statistical association between the origin of animals and the prevalence of C. bovis. This variation in prevalence could be associated with geographical differences, habits of society toward raw meat consumption, the presence or absence of sanitary problems, and likely associated with the number of animals brought to the abattoir.³

Anatomical distribution of cysts

An active abattoir survey found that the anatomical distributions of C. bovis in the examined cattle organs varied. The most frequently affected organ was the tongue, with the highest number of cysts (6, 42.9%), followed by the masseter muscle (4, 28.6%), the liver (3, 21.42%), and the triceps muscle (1, 7.14%). These organ-specific figures agree with Teklemariam and Debash⁹ and Tesfaye et al,²³ who reported tongues with the highest number of cysts. However, this organ-specific prevalence disagreed with Netsanet et al,³ who reported the liver with the highest cyst number, and Belachew and Ibrahim²¹ at Hawassa Municipal Abattoir, Mohamed et al²⁴ at Addis Ababa enterprise abattoir, who reported the triceps muscle to be the first to harbor C. bovis. The abattoir survey analysis indicated that there was a significant variation in the anatomical distribution of C. bovis in the inspected organs of slaughtered animals. This demonstrated that the tongue was the first ranked to confirm C. bovis at abattoirs. This variation might be due to the ability of the meat inspector to identify the cases, sample size, method of meat inspection, and several cuts.

Conclusion and Recommendations

Cysticercus bovis is an important zoonotic disease. It is strongly associated with raw or undercooked beef consumption and occupation. The present study revealed that Cysticercus bovis is slightly prevalent in the Bishoftu municipal abattoir. Among the risk factors, sex, body condition score, and age of the animals were not significantly associated with the prevalence of Cysticercosis bovis. This implies that all animals without their status of sex, age, and origin were equally infected by C. bovis. Based on the above conclusions, the following recommendations are forwarded: An all-inclusive approach focused on improving sanitary conditions and strengthening meat inspection and reporting systems among abattoirs should be improved; a routine meat inspection procedure should be applied.

Footnotes

Acknowledgements

We would like to thank the regional laboratory staff for providing us with the required laboratory facility during the study period. Finally, we would also like to thank the cattle owners who generously contributed to this study by providing the appropriate sample.

Funding:

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests:

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Author Contributions

All authors contributed to the study design, data gathering, data analysis, manuscript write-up, and editing of the manuscript. All authors have approved the submission of the manuscript.

Consent for Publication

Not applicable.

Data Availability Statement

The data will be provided upon the request of the corresponding author.

Ethics Approval and Consent to Participate

Ethical clearance was obtained from the University Review Board. The purpose of the study was well explained to the cattle owners before taking the samples, and informed consent was obtained to take the appropriate sample through verbal consent.

ORCID iDs

Haben Fesseha

Isayas Asefa

References

Metaferia

Cherenet

Gelan

, et al. Ministry of Finance and Economic Development and Ministry of Agriculture: A Review to Improve the Estimation of Livestock Contribution to the National GDP. IGAD Livestock Policy Initiative; 2011.

Megersa

Tesfaye

Regassa

Abebe

Abunna

. Bovine cysticercosis in cattle slaughtered at Jimma municipal abattoir, south western Ethiopia:prevalence, cyst viability and its socio-economic importance. Vet World. 2010;2:257-262.

Netsanet

Yesuf

Abrha

Lewtnesh

. Prevalence and public health importance of Cysticercus bovis in and around Dessie, Amhara region, North East Ethiopia. Niger J Anim Sci. 2020;22:173-185.

Beyene

Hiko

. Zoonotic metacestodes and associated financial loss from cattle slaughtered at Yabello municipal abattoir, Borana-Oromia, Ethiopia. Parasite Epidemiol Control. 2019;5:e00096.

Basem

Abdo

Sayed

Hussein

Mohsen

Arafa

. Occurence of cysticercosis in cattle and buffaloes and Taenia saginata in man in assiut governance of Egypt. Vet World. 2009;2:173-176.

Hashemnia

Shahbazi

Afshari Safavi

. Cysticercus bovis with special attention to its prevalence, economic losses, and food safety importance in Kermanshah, west of Iran. J Food Qual Hazard Control. 2015;2:26-29.

Kebede

. Cysticercus bovis: Development and evaluation of serological tests and prevalence at addis ababa abattoir. MSc thesis, Addis Ababa University; 2004.

Abunna

Tilahun

Megersa

Regassa

Kumsa

. Bovine cysticercosis in cattle slaughtered at awassa municipal abattoir, Ethiopia: prevalence, cyst viability, distribution and its public health implication. Zoonoses Public Health. 2008;55:82-88.

Teklemariam

Debash

. Prevalence of Taenia saginata/Cysticercosis and community knowledge about zoonotic Cestodes in and around Batu, Ethiopia. J Vet Sci Technol. 2015;6:273.

10.

Lielt

Desalew

Tsegabirhan

Teshale

Yohannes

. Prevalence and public health significance of bovine cysticercosis at Elfora Abattoir, Bishoftu, Ethiopia. J Public Health Epidemiol. 2015;7:34-40.

11.

Geinoro

Beredo

. Prevalence of Cysticercus bovis in cattle slaughtered at Bishoftu Municipal Abattoir; public health significance and community perception about zoonotic importance of taeniosis in Bishoftu. Int J Adv Res Biol Sci. 2019;6:52-61.

12.

Thrusfield

. Veterinary Epidemiology. John Wiley & Sons; 2018.

13.

Ministry of Agriculture. 2011: Meat Inspection Regulations. Legal notice No. 428 Negarite Gazexa. Addis Ababa, Ethiopia.

14.

Laranjo-González

Devleesschauwer

Jansen

, et al. Epidemiology and economic impact of bovine cysticercosis and taeniosis caused by Taenia saginata in northeastern Spain (Catalonia). Parasit Vectors. 2018;11:1-15.

15.

Tesfaye

Sadado

Demissie

. Public health and economic significance of Cysticercus bovis in wolaita soddo, southern Ethiopia. Glob Vet. 2012;9:557-563.

16.

Ibrahim

Zerihun

. Prevalence of Tania saginata cysticercosis in cattle slaughtered in Addis Ababa municipal abattoir, Ethiopia. Glob Vet. 2012;8:467-471.

17.

Tolosa

Tigre

Teka

Dorny

. Prevalence of bovine cysticercosis and hydatidosis in Jimma municipal abattoir, South West Ethiopia. Onderstepoort J Vet Res. 2009;76:323-326.

18.

Engdaw

Alemneh

Ambaw

. Study on the prevalence of Cysticercus bovis in Kombolcha Elfora, north-eastern Ethiopia. Eur J Appl Sci. 2015;7:152-157.

19.

Kebede

. Cysticercosis of slaughtered cattle in northwestern Ethiopia. Vet Sci Res. 2008;85:522-526.

20.

Kebede

Tilahun

Hailu

. Current status of bovine cysticercosis of slaughtered cattle in Addis Ababa Abattoir, Ethiopia. Trop Anim Health Prod. 2009;41:291-294.

21.

Belachew

Ibrahim

. Prevalence of Cysticercus bovis in Hawassa Municipal Abattoir and its public health implication. Am J Sci Res. 2012;7:238-245.

22.

Swai

Schoonman

. A survey of zoonotic diseases in trade cattle slaughtered at Tanga city abattoir: a cause of public health concern. Asian Pac J Trop Biomed. 2012;2:55-60.

23.

Tesfaye

Bekele

Abera

. Public health implications of Cysticercus bovis from cattle slaughtered at Dilla Municipal abattoir, southern Ethiopia. East Afr J Biophys Comput Sci. 2020;1:54-61.

24.

Mohamed

Abebe

Birhanu

Abdirahman

Wali

. Prevalence of Taenia saginata cysticerci in Addis Ababa Abattoir Enterprise, Ethiopia. Food Waterborne Parasitol. 2021;25:e00135.

25.

Duresa

Kitessa

Feyissa

. Prevalence of indigestible foreign bodies and its associated potential risk factors in rumen and reticulum of domestic ruminants at Bishoftu Elfora Export Abattoir. Vet Med Sci. 2022;8:2623-2630.