Prevalence of Fascioliasis in Slaughtered Ruminants at Muyinga Slaughterhouse, Burundi

Salvator Minani1,2*, Eric Nsengiyumva1, Anatole Bigirimana1,2, Arnaud Cubahiro1,2, Dieudonné Ntakirutimana1,2 and Vénuste Bizoza1,2

1Department of Biology, Faculty of Sciences, University of Burundi, P.O. Box 2700, Bujumbura, Burundi; 2Center of Research in Natural and Environmental Sciences, Faculty of Sciences, University of Burundi, P.O. Box 2700, Bujumbura, Burundi.

Editor | Muhammad Abubakar, National Veterinary Laboratories, Park Road, Islamabad, Pakistan.

Received | April 12, 2023; Accepted | May 29, 2023; Published | June 09, 2023

*Correspondence | Salvator Minani, Department of Biology, Faculty of Sciences, University of Burundi, P.O. Box 2700, Bujumbura, Burundi; Email: [email protected]

Citation | Minani, S., E. Nsengiyumva, A. Bigirimana, A. Cubahiro, D. Ntakirutimana and V. Bizoza. 2023. Prevalence of fascioliasis in slaughtered ruminants at Muyinga Slaughterhouse, Burundi. Veterinary Sciences: Research and Reviews, 9(1): 65-73.

DOI | https://dx.doi.org/10.17582/journal.vsrr/2023/9.1.65.73

Keywords | Fascioliasis, Domestic ruminants, Prevalence, Muyinga slaughterhouse, Burundi

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Fascioliasis is a parasitic zoonosis infecting mainly domestic ruminants and occasionally humans, caused by Fasciola hepatica and Fasciola gigantica (Mehmood et al., 2017; Torgerson, 2013). F. hepatica is mainly distributed in temperate regions including Europe, America and Oceania, while F. gigantica is commonly found in tropical regions of Africa and Asia, although its range may overlap with that of F. hepatica (Mas-Coma et al., 2009). The life cycle of these parasites involves an intermediate host (snail) and a definitive host (livestock and humans). Humans and livestock get infected by ingesting encysted metacercariae with raw vegetables and contaminated pastures, respectively (WHO, 2006). Climatic conditions such as temperature, precipitation, and soil moisture influence the activity of Fasciola spp. and the increase in snails, which are crucial in the epidemiology of fascioliasis (Mas-Coma et al., 2009; Mehmood et al., 2017).

Fascioliasis leads to huge economic losses in the agricultural sector, due to the liver condemnation, emaciated carcasses, growth reduction, and reduced meat and milk production (Nyirenda et al., 2019; Torgerson, 2013). The annual economic losses ranging from 4 billion to 11 billion Australian dollars were estimated in South-East Asia cattle (Torgerson, 2013). In addition, in the public health sector, it is estimated that more than 2.6 million people worldwide are infected with Fasciola spp. and 180 million people are at risk of infection (Havelaar et al., 2015). The annual global burden of human fascioliasis was estimated at 90,000 disability-adjusted life years (DALYs) (Havelaar et al., 2015).

In Africa, fascioliasis due to F. hepatica is only distributed in the Mediterranean area, southern Zimbabwe, South Africa, Lesotho and some areas with high altitude in Kenya, Tanzania and Ethiopia, while fascioliasis due to F. gigantica is mainly distributed in most areas of the continent (Dermauw et al., 2021; Mehmood et al., 2017). Overall prevalence estimates in ruminants ranged from 0.19 to 73.7% in sheep, 1.2 to 91% in cattle, and 0.28 to 68.4% in goats (Mehmood et al., 2017). In sheep, the prevalence of fascioliasis was estimated at 20.7% in Ethiopia (Oljira et al., 2022), 23% in Chad (Jean-Richard et al., 2014), 27% in Cameroon (Takang et al., 2019) and 29.9% in Kenya (Kipyegen et al., 2022). The prevalence of fascioliasis in cattle was 0.09% in Botswana (Mochankana and Robertson, 2016), 3.8% in Sudan (Kheder and Mohamed, 2021), 6.7% in Tanzania (Mwabonimana et al., 2010), 18% in Cameroon (Takang et al., 2019), 19.9% in Rwanda (Sun et al., 2020), 20.24% in Ethiopia (Zewde et al., 2019), 27.68% in Nigeria (Magaji et al., 2014), 30.88% in Egypt (Elshraway and Mahmoud, 2017), 37.1% in Zimbabwe (Pfukenyi and Mukaratirwa, 2004), 46% in Kenya (Kipyegen et al., 2022), 64.4% in Zambia (Nyirenda et al., 2019), 65.7% in Uganda (Opio et al., 2021) and 68% in Chad (Jean-Richard et al., 2014). In goats, the prevalence of fascioliasis was 1.6% in Ethiopia (Oljira et al., 2022), 12% in Chad (Jean-Richard et al., 2014) and 24.1% in Kenya (Kipyegen et al., 2022).

Burundi is a landlocked country in East Africa. Agriculture and livestock are the pillars of the national and family economy (WFP, 2017). Domestic ruminants in Burundi are the main sources of proteins, income, and manure. The updated number of domestic ruminants is missing. In 2017, the total number of domestic ruminants in Burundi was 1,044,649 cattle; 512,882 sheep, and 3,043,059 goats (MEAE and Ministère des Finances, 2018). However, the liver condemnation due to Fasciola spp. infection during post-mortem inspection of carcasses and organs leads to significant economic losses for farmers and butchers (Mehmood et al., 2017). It was reported that in Eastern and Southern Africa, to which Burundi belongs, an overall prevalence of fascioliasis was 14.5% in cattle, 2.5% in goats, and 3.7% in sheep (Malatji et al., 2020). Fascioliasis has not been reported in Burundi, but extensive farming systems, water resources, and climatic conditions could contribute to the spread of that disease in Burundi (OIE, 2012; WFP, 2017). Epidemiological data on fascioliasis and liver condemnation of domestic ruminants due to Fasciola spp. at public slaughterhouses are lacking in Burundi. Therefore, this study was carried out to assess the prevalence of fascioliasis by liver inspection in slaughtered ruminants at Muyinga slaughterhouse in Burundi.

Materials and Methods

Study area and population

The study was conducted at the slaughterhouse of Muyinga city located in Muyinga commune of Muyinga province. Muyinga province is one of 18 Burundian provinces (Figure 1). This province borders Tanzania to the East and Rwanda to the North. It is adjacent to the provinces of Kirundo to the North, Ngozi to the West, Cankuzo to the South East and Karuzi to the South. It is made up of 7 communes such as Buhinyuza, Butihinda, Gashoho, Gasorwe, Giteranyi, Muyinga, and Mwakiro. It is characterized by a tropical climate with some differences in water and thermal regimes according to two natural regions, Bugesera and Bweru. Bweru region is characterized by an altitude varying between 1,600 and 1,800 m with a tropical climate with a long dry season (5 months), while Bugesera region is characterized by an altitude varying between 1,400 and 1,600 m with a hot tropical climate with irregular rains (Ministère de la Planification du développement et de la Reconstruction, 2006). Over the year, the temperature varies from 14ºC to 28ºC with an annual average temperature of 18.5ºC. The average annual rainfall in the two regions is between 1,000 and 1,100 mm (Ministère de la Planification du développement et de la Reconstruction, 2006). Muyinga province covers an area of 1836.26 km2 and the total population in 2020 was estimated at 880,706 people (ISTEEBU and UNFPA, 2013). The livestock population in 2017 was 32,745 cattle; 20,136 sheep; 261,482 goats; 29,200 pigs; 25,120 rabbits; 129,204 poultries and 165,078 guinea pigs (MEAE and Ministère des Finances, 2018). This study included all cattle, sheep, and goats brought to Muyinga slaughterhouse for slaughter.

 

Study design and sampling method

A cross-sectional study was conducted at Muyinga slaughterhouse from December 2020 to January 2021. A convenience sampling method was applied to obtain the number of cattle, sheep, and goats slaughtered at each visit to the slaughterhouse. To assess the prevalence of fascioliasis, every slaughtered domestic ruminant was diagnosed with fascioliasis by liver inspection. After slaughter, the liver of each domestic ruminant was inspected by a veterinarian in accordance with meat inspection procedures. The liver was visually inspected, palpated, and incised with a knife to look for liver flukes in the bile ducts (Figures 2 and 3). A domestic ruminant was considered positive for fascioliasis if liver flukes were found in the bile ducts (Figures 4 and 5). According to the schedule, a regular visit to the slaughterhouse was carried out twice a week (Tuesday and Friday, market days) until the end of the study. A total of 14 visits were made to the slaughterhouse during the data collection period.

 

 

 

 

Data management and analysis

Prior to slaughter, descriptive data, including age, sex, and species of each domestic ruminant were recorded in Microsoft Excel 2007. After slaughter, positive and negative domestic ruminants for fascioliasis were also recorded. Then, data recorded in Microsoft Excel 2007 were exported in R software version 4.1 for analysis. The prevalence was calculated as a proportion of the number of infected domestic ruminants out of the total number of inspected domestic ruminants. Descriptive statistics to estimate the prevalence between age, sex and species were performed using the chi-square test. Odds ratio (OR) was used to calculate measures of associations. Results were calculated at 95% confidence intervals (CI) and the level of significance of α = 0.05 was considered.

Results and Discussion

Description of the inspected cattle, goats, and sheep

At each visit to Muyinga slaughterhouse, an average of 5 cattle and 14 goats were sampled and inspected. A total of 265 domestic ruminants composed of 69 cattle with 16 males and 53 females, 190 goats with 59 males and 131 females, and 6 sheep with 3 males and 3 females were inspected for the presence of Fasciola spp. in the liver. The majority of cattle slaughtered were of the Ankole breed (88%) and other cattle (12%) were of the crossed breed. According to age, 18 cattle (26%) were under 3 years old while 51 cattle (74%) were more than three years old. In addition, all goats and sheep were local breeds. Most goats (71%) were more than two years old while 29% of goats were less than two years old. Of the total number of sheep inspected, 83% were more than two years old.

Prevalence of fascioliasis in cattle, goats, and sheep

Of the 265 domestic ruminants examined by liver inspection, 15 domestic ruminants (5.66%) were positive for Fasciola spp. at Muyinga slaughterhouse. The prevalence of Fasciola spp. by liver inspection was estimated at 13.04% in cattle, 3.16% in goats, and 0.00% in sheep (Table 1). Based on the animal species, the prevalence of Fasciola spp. in cattle was significantly higher (p < 0.05) than in goats (Table 2). However, the association between age, sex, and breed categories with the prevalence of Fasciola spp. in cattle, goats, and sheep was not statistically significant (p > 0.05) (Table 2).

 

Table 1: Prevalence of Fasciola spp. in cattle, goats, and sheep at Muyinga slaughterhouse.

Animal species	Inspected animals	Positive animals	Prevalence (%, 95% CI)
Cattle	69	9	13.04 (5.10-20.99)
Goats	190	6	3.16 (0.67-5.64)
Sheep	6	0	0.00
Total	265	15	5.66 (2.88-8.44)

 

CI: Confidence intervals.

This study is the first to assess the prevalence of fascioliasis in Burundi. The prevalence of fascioliasis found in cattle, goats, and sheep was lower than the prevalence reported in other African countries by liver inspection. This study found a prevalence of 13.04% in cattle, which was lower than the prevalence of 20.24% by liver inspection reported in Ethiopia (Zewde et al., 2019), 27.68% in Nigeria (Magaji et al., 2014), 30.88% in Egypt (Elshraway and Mahmoud, 2017), 37.1% in Zimbabwe (Pfukenyi and Mukaratirwa, 2004), 64.4% in Zambia (Nyirenda et al., 2019), 65.7% in Uganda (Opio et al., 2021), and 68% in Chad (Jean-Richard et al., 2014). However, the prevalence found in cattle was similar to that reported in Cameroon and Eastern and Southern Africa (Malatji et al., 2020; Takang et al., 2019), while it was higher than 0.09% in Botswana (Mochankana and Robertson, 2016), 3.8% in Sudan (Kheder and Mohamed, 2021), and 6.7% in Tanzania (Mwabonimana et al., 2010). In goats, the prevalence is in line with that found in Ethiopia (Oljira et al., 2022) and lower than that in Chad (Jean-Richard et al., 2014). No cases of Fasciola spp. in sheep were found during the liver inspection. This was due to the few sheep slaughtered at Muyinga slaughterhouse. In Burundi, sheep farming is less practised and accounts for one-sixth of the total number of goats (MEAE and Ministère des Finances, 2018). During sampling, only 6 sheep were slaughtered while 190 goats were slaughtered. In sheep, a prevalence of 23% was reported in Chad (Jean-Richard et al., 2014), 27% in Cameroon (Takang et al., 2019), 20.7% in Ethiopia (Oljira et al., 2022), and 7.7% in Iran (Khanjari et al., 2014).

 

Table 2: Prevalence of Fasciola spp. based on sex, age and breed of cattle, goats, and sheep slaughtered at Muyinga slaughterhouse.

Animals	Variables	Category	Inspected animals	Positive animals	Prevalence (%, 95% CI)	Chi-square (χ2)	OR (95% CI)	p-value
Cattle	Sex	Male	16	2	12.50 (-3.70-28.70)	1.4968e-31	0.94 (0.17-5.04)	1.000
		Female	53	7	13.21 (4.09-22.32)
	Age	<3years	18	2	11.11 (-3.41-25.63)	1.5515e-31	0.79 (0.15-4.18)	1.000
		>3years	51	7	13.73 (4.28-23.17)
	Breed	Ankole	61	8	13.11 (4.64-21.59)	7.6301e-30	0.95 (0.10-8.74)	1.000
		Crossed	8	1	12.50 (-10.42-35.42)
Goats	Sex	Male	59	4	6.78 (0.36-13.19)	2.154	4.69 (0.83-26.37)	0.142
		Female	131	2	1.53 (-0.57-3.63)
	Age	<2years	56	3	5.36 (-0.54-11.25)	0.443	2.47 (0.48- 12.64)	0.506
		>2years	134	3	2.24 (-0.27-4.74)
Sheep	Sex	Male	3	0	0.00	-	-	-
		Female	3	0	0.00
	Age	<2years	1	0	0.00	-	-	-
		>2years	5	0	0.00
Animal species	Species	Cattle	69	9	13.04 (5.10-20.99)	7.345	4.60 (1.57-13.46)	0.007*
		Goats	190	6	3.16 (0.67-5.64)

 

OR: Odds ratio, CI: Confidence intervals, *significant difference at p < 0.05

 

The findings of this study show that the prevalence of fascioliasis in cattle was higher than in goats, which is in line with findings in Chad (Jean-Richard et al., 2014). Husbandry practices and feeding patterns are likely the sources of infection in cattle and goats (Jean-Richard et al., 2014; Takang et al., 2019). Livestock movements in search of fodder, water points, and grazing in marshes are favourable conditions for bovine fascioliasis in Burundi. Jean-Richard et al. (2014) indicated that small ruminants prefer grazing and browsing on dry ground while avoiding wet areas. Nevertheless, dry pastures are not completely safe because fluke metacercariae may remain viable longer in previously flooded areas and on vegetation (Jean-Richard et al., 2014). It was demonstrated that rainfall and high temperatures (>10°C) influence Fasciola egg hatch and snail growth (Mas-Coma et al., 2009). The tropical climate with an average annual temperature of 18.5°C and annual rainfall of 1,100 mm could explain the presence of Fasciola spp. in Burundi (Ministère de la Planification du développement et de la Reconstruction, 2006). Furthermore, the findings of this study are not in agreement with the findings in Cameroon and Iran, where sheep were more susceptible to contracting fascioliasis than goats (Jean-Richard et al., 2014; Khanjari et al., 2014). They revealed that the high occurrence of fascioliasis in sheep could be explained by the fact that sheep graze on ground cover, while goats browse the leaves and branches of bushes, shrubs, and trees (Jean-Richard et al., 2014; Khanjari et al., 2014).

Regarding sex in cattle and goats, no significant difference was found between the prevalence of Fasciola spp. in males and females. Similar findings were reported by Abdi et al. (2015), Oljira et al. (2022), and Opio et al. (2021), where they found that sex had no impact on the occurrence of fascioliasis and that males and females are equally exposed to the infection when they move together in search of fodder and water. However, there may be a disparity in susceptibility between sexes due to intrinsic factors (genetics, physiology and immunology) and extrinsic factors (environment and management practices) (Magaji et al., 2014).

Concerning age, our results demonstrated that there was no significant difference in the occurrence of fascioliasis in cattle under 3 years old and cattle over 3 years old. In addition, no difference in the occurrence of infection in goats under 2 years old and goats over 2 years old. This was not in agreement with the findings of Opio et al. (2021) and Zewde et al. (2019), who showed that the infection with Fasciola spp. was significantly higher in 4-years old cattle than in young cattle because they graze longer, which could increase the rate of exposure to fluke metacercariae.

Although routine meat inspection is a good veterinary practice to detect infected animals, the liver examination was performed by cutting the liver along the bile ducts, which may leave some immature parasites in the liver. It would be better to inspect the entire liver by cutting it into small pieces to see liver flukes in all bile ducts. Nevertheless, the entire liver inspection could reduce the quality and cost of meat, leading to losses for butchers. During the study, livers with light infections were trimmed, which may allow some immature liver flukes to enter the food chain. Consumption of raw or undercooked liver containing immature flukes has been shown to lead to infection in humans (Mas-Coma et al., 2018). However, human fascioliasis has not been reported in Burundi. This study recommends deworming livestock twice a year, especially before and after the rainy season, as a method of controlling liver flukes. Moreover, grazing livestock with marsh fodder should be avoided, which would reduce the rate of exposure to fluke metacercariae.

This study had limitations related to the confirmation of Fasciola species during the liver inspection. We did not confirm that all cases were F. gigantica, species highly distributed in Africa because F. hepatica was also reported in neighbouring countries like Tanzania (Mehmood et al., 2017). The sampling was carried out in the short dry season, which requires another sampling in the rainy seasons to better explain and understand the epidemiology of fascioliasis in Burundi.

Conclusions and Recommendations

This study revealed the prevalence of fascioliasis in cattle and goats. The occurrence of fascioliasis by sex, age, and breed was not statistically significant. Our study found that cattle were more susceptible to infection than goats. Further studies assessing the epidemiology and socio-economic impacts of fascioliasis as well as the ecology of snails and larval fluke transmission in the definitive hosts should be conducted in Burundi. Post-mortem inspection, regular deworming of livestock and improved husbandry systems should be implemented to control fascioliasis in Burundi.

Acknowledgements

The authors greatly thank the Provincial Directorate of Environment, Agriculture, and Livestock in Muyinga for the research authorization. We also thank veterinarians, livestock traders, and butchers of Muyinga slaughterhouse for their effective cooperation.

Novelty Statement

This study is the first to assess the prevalence of fascioliasis in cattle, goats and sheep in Burundi. The funding of this study will contribute to the implementation of parasite control methods by stakeholders and policy makers and to the development of future research.

Author’s Contribution

SM and EN conceived and designed the study, collected and analyzed the data. SM, EN, AB, AC, DN and VB wrote the paper. All authors reviewed and approved the final manuscript.

Conflict of interest

The authors have declared no conflict of interest.

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