
==== Front
Vet Med Sci
Vet Med Sci
10.1002/(ISSN)2053-1095
VMS3
Veterinary Medicine and Science
2053-1095
John Wiley and Sons Inc. Hoboken

10.1002/vms3.70002
VMS370002
Original Article
RUMINANTS
Original Article
Prevalence of bovine fasciolosis and direct financial losses in cattle slaughtered in Bamenda and Bafoussam abattoirs, Western Highlands, Cameroon
ATANGA et al.
Atanga Heinendez Merrius 1 2
Ntonifor Ngum Helen https://orcid.org/0000-0001-5044-8207
3 ngumnto@yahoo.com

Mahamat Oumar https://orcid.org/0000-0001-5170-1913
3
1 National Centre for Animal Husbandry and Veterinary Training Jakiri Cameroon
2 Department of Microbiology and Parasitology Faculty of Science The University of Bamenda Bamenda Cameroon
3 Department of Zoology Faculty of Science The University of Bamenda Bamenda Cameroon
* Correspondence
Ngum Helen Ntonifor, Department of Zoology, Faculty of Science, The University of Bamenda, Bamenda, Cameroon.
Email: ngumnto@yahoo.com

18 9 2024
11 2024
10 6 10.1002/vms3.v10.6 e7000203 7 2024
16 1 2024
07 8 2024
© 2024 The Author(s). Veterinary Medicine and Science published by John Wiley & Sons Ltd.
https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

Abstract

Background

Bovine fascioliasis is a parasitic disease that affects cattle. It leads to direct and indirect great economic loss due to animal mortalities, growth retardation and expenditure on anthelmintics, reduction livestock productivity and essentially condemnation of infected liver by inspection service. The study was carried out to determine the seasonal prevalence and estimated financial losses of fascioliasis in cattle in the Western Highlands of Cameroon.

Methodology

A total of 2167 cattle were selected. Later, the cattle, have being the carcasses, were dissected, and the livers were dissected and carefully examined for adult liver flukes. Faeces were collected immediately after the cattle were killed and examined using the formol‐ether concentration technique. Condemned livers were weighted to estimate the financial losses using the average price of a kilogram of liver.

Results

A total 428 of cattle were found with infected livers or egg in the faeces giving a total prevalence of 19.75%. Among the infected carcass, 18.64% had both the Fasciola eggs in the faeces and flukes in the liver while 1.10% had only flukes in the liver. Results revealed that prevalence of Fasciola spp. was significantly higher during the rainy season (23.48%) than 16% in the dry season (p = 0.00). A significantly (p = 0.000) higher prevalence was also observed in females (33.9%) than in males (13.1%). Age range showed significant (p = 0.000) influence with the animals of 8–10 years old recorded the highest prevalence of 39.3%. Furthermore, 433.1 kg of liver was condemned giving a direct financial loss of 1221,550 FCFA (2049.64 USD) and an annual financial loss due to liver condemnation estimated to 1814,775 (3045.01 USD).

Conclusion

Findings of this study indicated that bovine fascioliasis is prevalent in cattle in the Western Highlands of Cameroon, and it leads to an important financial loss particularly in the rainy season.

Bovine fasciolosis is a parasitic disease that affects cattle. It leads to direct and indirect great economic loss due to animal mortalites, growth retardation, expenditure on anthelmintics, reduction livestock productivity and essentially condemnation of infected liver by inspection service. The study was carried out in 2022/2023 to determine the seasonal prevalence and estimated financial losses of fascioliasis in cattle in the Western Highlands of Cameroon.

bovine
Cameroon
financial loss
fascioliasis
Western highlands
source-schema-version-number2.0
cover-dateNovember 2024
details-of-publishers-convertorConverter:WILEY_ML3GV2_TO_JATSPMC version:6.4.8 mode:remove_FC converted:19.09.2024
Atanga, H. M. , Ntonifor, N. H. , & Mahamat, O. (2024). Prevalence of bovine fasciolosis and direct financial losses in cattle slaughtered in Bamenda and Bafoussam abattoirs, Western Highlands, Cameroon. Veterinary Medicine and Science, e70002. 10.1002/vms3.70002
==== Body
pmc1 INTRODUCTION

Fascioliasis is an economically important helminth infection which is caused by Fasciola hepatica and Fasciola gigantica. It affects domestic animals, wild animals and humans but is most important in ruminants (Soulsby, 1986). The number of grazing animals at the risk for fascioliasis exceeds 700 million worldwide (Mas‐Coma et al., 2005). F. hepatica and F. gigantica are two commonly reported liver flukes that cause fascioliasis in ruminants and humans. Fascioliasis is an important zoonotic infection affecting both animals and humans. In humans, due to the destruction of liver tissues, fascioliasis is responsible of hepatomegaly or cirrhotic liver. It is now recognized as an emerging human disease (World Health Organization, 2006), with an estimated 2.4 million people that are infected with Fasciola and 180 million are at risk of infection in 70 countries worldwide (Food and Agriculture Organization and World Organization for Animal Health, 2021). In animals, it is responsible for a significant loss in animal productivity, animal mortalities rate, growth retardation and liver changes which leads to its condemnation. In bovine, the feeding activity and the physical presence of large flukes in the bile ducts can lead to anaemia, inflammation, obstruction and cholangitis, which render the liver of the animals unacceptable for human consumption (Lalor et al., 2021; Madkour & Al‐Amgad, 2023). Economically, the disease is responsible of a large quantity of the condemnation of bovine liver at meat inspection. The financial losses due to this condemnation are estimated to about thousands of dollars (Nyirenda et al., 2019). In a recent study, the financial losses due to the liver condemnation only were estimated to 47,945.24 USD per year (Mathewos et al., 2023). Additional fascioliasis economic losses are due to the increasing in the expenditures for treatment, lowering of milk production, loss of weight and reduction of fertility (Diyana et al., 2019), which are responsible of the economic growth of so many countries, including Cameroon. This disease is therefore considered a major obstacle for the efficient production and maintenance of health as well as food safety of animal origin affecting countries with livestock industries as an important segment of the agricultural products.

In most African countries, where the disease is endemic, the prevalence of fascioliasis in ruminants is essentially determined through slaughterhouse surveys (Mungube et al., 2006; Mwabonimana et al., 2009). Informations gathered on animals slaughtered at an abattoir are taken as a convenient and relatively inexpensive source of information with the condemnation rates providing a useful guide to the prevalence of the sub‐acute, mild or chronic forms of the disease in the regions served by the abattoirs (Pfukenyi & Mukaratirwa, 2004). These data are therefore used to determine trends of prevalence and significance of the disease, especially where the reporting system is reliable (Roberts & Suhardono, 1996).

In Cameroon, livestock is one of the rapidly evolving sectors in agriculture offering potential opportunities for economic growth and alleviation of poverty among rural dwellers, by generating market opportunities for the poor livestock‐dependent and enhancing food security and nutrition (The Ministry of Livestock Fisheries and Animal Industries [MINEPIA], 2018). But, fascioliasis remains one of the most important neglected parasitic diseases of animals, whereas the favourable conditions of the intermediate snail hosts and the adaptation of parasites to a wide variety of mammalian definitive hosts contribute to the high transmissibility and distribution of the parasites. The Western Highlands agro‐ecological zone of Cameroon is characterized by diverse landscape, with grass‐covered plateaus, wooded valleys, numerous rivers and volcanic lakes. Animals graze these diverse lands where the climate is humid and favourable for the development Lymnea snails. Moreover, population activities are essentially agricultural activities such as rice and vegetable growing, which expose them to the infection. Moreover, although the efforts made towards tackling the disease in Cameroon, there is a paucity of information on its prevalence and financial losses of this disease. Population needs to be informed about the presence and the impact of fascioliasis. The present study therefore aims to determine the seasonal prevalence of bovine fascioliasis and the financial loss due to liver condemnation in cattle slaughtered at the two major abattoirs (Bamenda and Bafoussam) in the Western Highlands of Cameroon.

2 MATERIALS AND METHODS

2.1 Study design

This study was conducted during routine meat inspection in Bamenda and Bafoussam abattoirs for 8 months (4 months during the rainy season and 4 months during the dry season). During ante‐mortem inspection, the animals were identified as male or female based on the appearance of the external genitalia (testes and udder). Using a stratified sampling technique, stool samples were collected from randomly selected cattle and used for coprological analysis. The livers of these animals were macroscopically inspected for the detection of flukes followed by quantification of condemned liver samples to evaluate the financial loss (Figure 1).

FIGURE 1 Fasciola infested livers of cattle. The blue arrows indicate the Fasciola in liver tissue.

2.2 Study area

The Western Highlands of Cameroon refers to an agro‐ecological zone that covers the territory of the North West and West Regions (Figure 2). The North West Region has Bamenda as the regional capital city, whereas the capital city of West Region is Bafoussam. The Western Highlands of Cameroon is located within an altitude of 500–3000 m above sea level, and it is characterized of fertile volcanic soils and colder temperatures (21°C on annual average but with distinct differences according to altitude). The Western Highland of Cameroon has two main seasons. The rainy season starts from March to October, and the dry season starts from November to February. The landscape is diverse, with grass‐covered plateaus, wooded valleys, numerous rivers and volcanic lakes. Bamenda abattoir, one of the abattoirs where research studies were carried out, is the only know abattoir in Bamenda and the biggest in the Northwest Region (Latitudes 5° 45″ and 9° 9″N; Longitudes 9° 13″ and 11° 13″E). Bafoussam, the headquarters of the West Region, has one main abattoir (Bafoussam II) where research was carried and two others secondary abattoirs (Latitudes 5°26′ and 5°30′ North and longitudes 10°20′ and 10°30′ East). Bafoussam has a constantly cold climate with temperatures oscillating between 15 and 27°C.

FIGURE 2 Localization map showing location of the abattoirs in the two regions representing the highlands of Cameroon.

2.3 Sampling method and sample size

This study was a cross sectional study. Data were collected three days per week in animals randomly selected (the same days were used for sample collection throughout the study period). All cattle slaughtered during day of collection were marked following the order of arrival at the abattoir. Each animal was given a number that was used for sample collection. The sample size required for this study was determined based on the expected prevalence (12%) of bovine fascioliasis and the 5% desired absolute precision and 95% confidence interval, using the formula as reported by Thursfield (2005): i.e.N=1.962×Pex1−Pexd2

where N is the required sample size, Pexistheexpectedprevalence=12%=0.12, disthedesiredabsoluteprecision=5%=0.05, 1.96 is the constant for 95% confidence interval. N=1.962×0.121−0.12/0.052=163

Accordingly, 163 cattle per season were expected to be sampled in each region given a total of 326 cattle in each region. A total of 652 cattle were expected for the 2 seasons in the 2 regions. However, 2167 cattle (1084 cattle in Bamenda and 1083 in Bafoussam) were sampled in this study.

2.4 Study population

This study was carried out in cattle (Bos taurus indicus) and three breeds (Red Fulani, White Fulani and Gudali) were examined. All cattle were of 2 years and above of both sex (female and male) as according to Cameroon legislation, cattle aged less than 2 years are not allowed for slaughter (Law No. 2000/017 of 19/12/2000). All cattle brought for slaughter at the Bamenda and Bafoussam slaughter houses during the period of study and during the days of collection were included. The age of each cattle was determined using dentition as described by Pace and Wakeman (1983). Before being killed, all animal selected for study were identified by the identification number.

2.5 Faecal sample collection

Immediately, after the animals have been killed, stool samples were collected directly from the rectum of the cattle with gloved hands (Cheesbrough, 1992). The samples were put in labelled tightly closed stool containers corresponding to the animal. The sample were transported in a flask to the Regional Veterinary Laboratory Bamenda and examined for Fasciola eggs.

2.6 Liver incision technique

During the inspection, livers were incised transversely on the ventral side in such a way that bile ducts were cut open in several directions (Figure 3). Adult Fasciola were recovered by squeezing the liver using thumbs. The worms were immediately cleaned using distilled water and measured using a ruler in millimeters for morphometric identification (total worm length and width). In addition, livers were examined for capsular perforation, sub capsular haemorrhage, traces of damaged parenchyma tissue. Fasciola adult fluke identification was carried out using morphology and size parameters as described by Soulsby (1986). Any flat leaf shaped worm found was collected and examined using a hand lens for the characteristics of Fasciola spp.

FIGURE 3 Images of the incised liver in search of Fasciola.

2.7 Faecal examination using the formol‐ether concentration technique

Formol‐ether concentration technique was used to search for the presence of eggs in the faeces as described by Cheesbrough (2009). In a small mortar, 2 g of faeces was put and 7 mL of 10% formalin added to it. The faeces were then dissolved with a wooden stick applicator. A sieve of mesh size 90 was used to filter the stool sample into a centrifuge tube. Three mL of diethyl ether was then added to the solution in the centrifuge tube and the tube shaken vigorously for 30 s. The mixture was then centrifuged at 3000 rpm for 2 min. The supernatant was discarded and the sediment observed for Fasciola eggs using the 10× objective lens of the microscope. Eggs were stained with malachite green. The length and width measured. The obtained morphometric parameters of eggs were compared with those described previously (Soulsby, 1986). Each sample was analysed by at two different persons. In cases of contradictory results of two persons, a third person is required for the analysis.

2.8 Estimation of economic losses due to liver condemnation

All livers having Fasciola species were registered, and the number of flukes recovered from each liver counted. Recordings were also made of the weights of the livers condemned by the Veterinary Meat Inspectors. The average price of a kilogram of liver was gotten from butchers as it was sold in the commercial section of the abattoir to have the standard. The financial loss within the period of the survey or direct financial loss was calculated using the condemned liver for 8 months with the complete data collected. The total cost of the quantity of condemned liver was considered in francs CFA and converted to USA dollars (USD), whereas the annual financial loss was estimated by using the estimated annual condemned liver.

The direct financial loss due to fascioliasis was calculated using the following formula (F 1) as reported by Rahmeto et al. (2010): (F1)Directfinancialloss(DFL)=P×W

where W is the total weight of condemned liver, and P is average liver price (francs/kg).

The total annual financial loss incurred due to liver condemnation was determined according to method used by Ephrem et al. (2012): (F2)Annualcostofcondemnedliver=NAL×%COND×CL

where NAL: Average number of cattle slaughtered per year at Bamenda and Bafoussam abattoirs (per retrospective). It was obtained from the abattoir records for the last 3 years which was estimated to be 18,159 cattle; CL: Mean cost of liver is the mean price of liver as sold in Bamenda (2800 FCFA/kg) and Bafoussam (2850 FCFA/kg) abattoirs; %COND: The percentage of liver condemned due to fascioliasis is obtained using the following formula: %COND=actualwtofcondemnedliverliverwtexamined

where actual weight (wt) of condemned liver is the weight of condemned obtain during the current study; and liver weight (wt) examined is equal to the number of examined carcasses multiplied by the mean weight of liver in cattle (equal to 5.7 kg).

2.9 Statistical analysis

Data collected were entered into Microsoft 2020 and analysed using the statistical package for social sciences (SPSS) version 23. Data were expressed into means ± standard deviation and percentages. The total prevalence of fascioliasis and the prevalence following the month, gender, age and season were determined by computing descriptive statistics. Monthly, gender and age seasonal variations in prevalence of fascioliasis were determined by chi square test. Logistic regression was used to determine the odd ratio. A p value of ≤0.05 was considered statistically significant.

3 RESULTS

3.1 Characteristics of the studied animals

A total of 2167 cattle were examined, out of which the majority were males (68.11% [1476/2167]). Equally 49.33% (1069/2167) of the slaughtered cattle were animals of age group between 5 and 7 years. A total of 1086 cattle were examined during the rainy season, whereas 1081 were examined during the dry season in the two regions (Table 1).

TABLE 1 Distribution and category of animals examined during the study period.

Parameters	Bamenda	Bafoussam	Total number examined (%)	
Number examined (%)	Number examined (%)	
Sex				
Male	760 (51.14)	716 (66.11)	1476 (68.11)	
Female	324 (29.88)	367 (33.88)	691 (31.89)	
Total	1084	1083	2167	
Age group (years)				
2–4	226 (20.84)	246 (22.71)	472 (21.78)	
5–7	570 (52.58)	499 (46.07)	1069 (49.33)	
8–10	288 (26.56)	338 (31.20)	626 (28.89)	
Total	1084	1083	2167	
Season				
Dry	541 (49.90)	540 (49.86)	1081 (49.88)	
Rainy	543 (50.09)	543 (50.13)	1086 (50.11)	
Total	1084	1083	2167	
Note: Dry season: November to February; rainy season: May to August.

John Wiley & Sons, Ltd.

3.2 Prevalence of fascioliasis in cattle slaughtered in the Western Highlands of Cameroon

Independent of the region of collection, it was observed that season influenced the prevalence of fascioliasis in cattle (Table 2). The risk of having fascioliasis in cattle was significantly higher during the rainy season compared to the dry season (OR = 0.55; p = 0.001) (Table 2).

TABLE 2 Total proportion of Fasciola spp. (infected animals) in cattle at abattoirs in the Western Highlands of Cameroon.

Season	Number examined	Number infected (%)	Multivariate analysis	
Odd ratio	Sig.	95% C.I.	
Lower	Upper	
Dry	1081	173 (16)	Reference	
Rainy	1086	255 (23.48)	0.551	0.001	0.413	0.671	
Total	2167	428 (19.75)					
Note: Dry season: November to February; rainy season: May to August; N: total number examined.

John Wiley & Sons, Ltd.

Following the region and compared to the Bafoussam abattoir, the results (Table 3) showed that the Bamenda abattoir recorded a higher prevalence of 18.9% (102/541) and 29.8% (162/543) in the dry and rainy seasons, respectively. However, there was a significant variation in the infection rates only during the dry season (p = 0.014). According to the abattoir, the analysis of seasonal prevalence showed that the rainy season recorded significantly higher infection rates in Bamenda (p = 0.003) as well as in Bafoussam (p = 0.03) (Table 3).

TABLE 3 Seasonal prevalence of Fasciola among cattle in the two regions (Bamenda and Bafoussam) in the Western Highlands of Cameroon.

Location	Dry season	Rainy season	Significant difference	
N	Positive cases (%)	N	Positive cases (%)	
Bamenda	541	102 (18.9)	543	162 (29.8)	χ 2 = 23.601, p = 0.003	
Bafoussam	540	71 (13.1)	543	93 (17.1)	χ 2 = 15.465, p = 0.030	
Total	1081	173 (16.0)	1086	255 (23.5)	χ 2 = 36.335, p = 0.000	
Significant difference	χ 2 = 15.924

p = 0.014

		χ 2 = 8.952

p = 0.346

		
Note: Dry season: November to February; rainy season: May to August; N: total number examined. p values in bold are significantly different.

John Wiley & Sons, Ltd.

3.3 Prevalence of Fasciola spp based on the diagnostic method in the study area

As shown in Table 4, following the diagnostic methods, 24 cattle (1.1%) had only flukes in the liver without eggs in their faeces, whereas 404 cattle (18.64%) had only eggs in the faeces or combined eggs and flukes.

TABLE 4 Seasonal prevalence of Fasciola spp eggs and flukes recorded by the faecal sample and liver incision techniques in the study areas.

Season	Number examined		Multivariate analysis	
Egg and adult flukes n (%)	Adult flukes n (%)	Total of positive n (%)	Odd ratio	Sig.	95% C.I.	
		Lower	Upper	
Total	2167	404 (18.64)	24 (1.10)	428 (19.75)					
Rainy season					
Bamenda	543	158 (97.5)	4 (2.5)	162 (29.8)	0.388	0.000	0.283	0.533	
Bafoussam	543	73 (78.5)	20 (21.5)	93 (17.13)	Reference	
Total	1086	231 (90.6)	24 (9.4)	255 (23.48)					
Significant difference		χ 2 = 180.1, p = 0.919	χ 2 = 24.0, p = 0.404	χ 2 = 192.41, p = 0.944					
Dry season					
Bamenda	541	102 (18.9)	0 (0.0)	102 (18.9)	0.557	0.002	0.388	0.801	
Bafoussam	540	71 (13.1)	0 (0.0)	71 (13.1)	Reference	
Total	1081	173 (16.0)	0 (0.0)	173 (16.0)					
Significant difference		χ 2 = 191.32, p = 0.931	NA	χ 2 = 180.12, p = 0.954					
Note: Dry season: November to February; Rainy season: May to August, n: total number infected. p Value in bold are significantly different.

John Wiley & Sons, Ltd.

In rainy season, the results showed that infected animals have flukes or/and eggs. Comparing the prevalence in Bafoussam and Bamenda, there was no difference in the prevalence based the incision techniques (p = 0.944) or coprological analysis (p = 0.919). In dry season, only eggs were found in animals in Bamenda and Bafoussam, but there was no difference between the two areas (p = 0.931). Multivariate analysis of the influence of locality showed that seasonal prevalence of infection was associated with locality, with Bamenda having a higher risk of infection than Bafoussam during the dry season (OR = 0.557; p = 0.002) as well as during the rainy season (OR = 0.38; p = 0.000) (Table 4).

3.4 Monthly variation of seasonal prevalence of Fasciola infection in the different abattoirs

Table 5 presents the monthly variations of the prevalence of fascioliasis during the rainy and dry seasons. During the rainy season, a statistically significant difference was observed in the monthly prevalence (p = 0.009) with the month of August recording the highest prevalence of 24.6% (73/287). Equally during the dry season, monthly variations in infection rate showed that there was a significant difference (p  =  0.043) in prevalence with the highest prevalence of 21% (57/271) observed in the month of November.

TABLE 5 Monthly variation in the prevalence of Fasciola spp recorded in rainy and dry seasons at the study area.

Month/Season	Bamenda	Bafoussam	Overall prevalence	Significant difference of prevalence	
N	Number infected (%)	N	Number infected (%)	N	Number infected (%)	
Rainy season	
May	135	42 (31.1)	122	18 (15.0)	257	60 (23.5)	χ 2 = 43.333, p = 0.798	
June	151	41 (27.2)	135	24 (17.8)	286	65 (22.7)	χ 2 = 52.119, p = 0.693	
July	120	33 (27.5)	136	24 (17.6)	256	57 (22.3)	χ 2 = 50.847, p = 0.558	
August	137	46 (32.2)	150	27 (17.8)	287	73 (25.4)	χ 2 = 46.049, p = 0.764	
Total	543	162 (29.8)	543	93 (17.2)	1086	255 (23.5)	χ 2 = 192.418, p = 0.944	
Significant difference	χ 2 = 684.00, p = 0.487	χ 2 = 372.00, p = 0.432	χ 2 = 1003.256, p = 0.009		
Dry season	
November	135	35 (26.0)	136	22 (16.2)	271	57 (21.0)	χ 2 = 57.000, p = 0.438	
December	136	28 (20.6)	134	19 (14.2)	270	47 (17.4)	χ 2 = 47.000, p = 0.431	
January	135	20 (14.8)	120	18 (15.0)	255	38 (14.9)	χ 2 = 37.000, p = 0.324	
February	135	19 (14.1)	150	12 (8.0)	285	31 (10.9)	χ 2 = 31.000, p = 0.415	
Total	541	102 (18.9)	540	71 (13.1)	1081	173 (16.0)	χ 2 = 346.601, p = 0.312	
Significant difference	χ 2 = 578.63, p = 0.201	χ 2 = 321.24, p = 0.243	χ 2 = 1021.11, p = 0.043		
Note: Dry season: November to February; rainy season: May to August; N: total number examined. p values in bold are significantly different.

John Wiley & Sons, Ltd.

3.5 Influence of sex on the prevalence of Fasciola infection in the different slaughtered cattle in dry and rainy seasons

As presented in Table 6, females were more infected than males during the study recording a prevalence of 33.9% (234/691), and these results were statistically significant at p = 0.000. However, there was no significant difference between the prevalence of fascioliasis recorded in female and male cattle in Bamenda (χ 2 = 162.0, p = 0.46) and Bafoussam (χ 2 = 93.0; p = 0.451) during the rainy season. Moreover, no difference was seen between males in Bamenda and Bafoussam (χ 2 = 114.83, p = 0.66) and between females (χ 2 = 109.95, p = 0.66). Additionally, the prevalence of fascioliasis was not associated to sex during the rainy season (OR = 0.952; p = 0.806), although the females were more infected.

TABLE 6 Frequency of sex‐related rate of Fasciola spp recorded in rainy and dry seasons at the abattoir in Bamenda and Bafoussam.

		Prevalence				Multivariate analysis	
		Bamenda	Bafoussam						95% C.I.	
Season	Sex	N	Number infected (%)	N	Number infected (%)	Total examined	Total infected (%)	Significant difference	Odd ratio	Sig.	Lower	Upper	
Overall (rainy and dry)	Males	760	120 (15.78)	716	74 (10.3)	1476	194 (13.1)						
Females	324	144 (44.4)	367	90 (24.5)	691	234 (33.9)						
Sig. difference		χ 2 = 88.62, p = 0.000		χ2 = 86.5630, p = 0.000		χ2 = 170.78, p = 0.000						
Rainy Season	Males	376	83 (22.1)	350	47 (13.4)	726	130 (17.9)	χ 2 = 114.83, p = 0.66	0.952	0.806	0.64	1.41	
Females	167	79 (47.3)	193	46 (23.8)	360	125 (34.7)	χ 2 = 109.95, p = 0.66	Reference				
Total	543	162 (29.8)	543	93 (17.1)	1086	255 (23.5)	χ 2 = 192.41, p = 0.94					
Sig. difference		χ 2 = 162.0, p = 0.46		χ 2 = 93.0, p = 0.451		χ 2 = 224.9, p = 0.488						
Dry season	Males	384	37 (9.6)	366	27 (7.4)	750	64 (8.5)	χ 2 = 112.23, p = 0.43	2.022	0.003	1.26	3.22	
Females	157	65 (41.4)	174	44 (25.3)	331	109 (32.9)	χ 2 = 103.46, p = 0.53	Reference				
Total	541	102 (18.9)	540	71 (13.1)	1081	173 (16.0)	χ 2 = 113.31, p = 0.45					
Sig. difference		χ 2 = 137.00, p = 0.043		χ 2 = 82.00, p = 0.032		χ 2 = 213.75, p = 0.041						
Note: Dry season: November to February; rainy season: May to August; N: total number examined. p values in bold are significantly different.

John Wiley & Sons, Ltd.

During the dry season, the prevalence of infection in females (32.9% [109/331]) was statistically higher than in males (8.5%; [64/750], p = 0.043). In a similar manner, females in Bamenda were statistically more infected than males (χ 2 = 137.00; p = 0.043. Similarly, there was a significant difference between females and males (χ 2 = 82.00; p = 0.032) in Bafoussam, with a prevalence of 25.3% (44/174). Multivariate analysis showed that the risk of infection was two times less in males than in females (OR = 2.022; p = 0.003).

3.6 Influence of age on the seasonal prevalence of Fasciola spp in study area

Table 7 shows the prevalence of fascioliasis during the rainy and dry seasons with respect to the ages of the cattle. During the rainy season, the results showed that both in Bamenda and Bafoussam there was no significant difference in the prevalence of fascioliasis in the different age groups. Multivariate analysis, however, showed a significant influence of the ages of the animals on the prevalence of the infection. Cattle of 5–7 years and 8–10 years had a higher risk of having an infection (OR = 2.613, p = 0.000; OR = 10.031, p = 0.000) than the other age group.

TABLE 7 Frequency of age‐related rate of Fasciola spp. recorded in rainy and dry seasons at the abattoir in Bamenda and Bafoussam.

Season	Age group (years)	Multivariate analysis	
	Bamenda	Bafoussam					95% C.I.	
N	Number infected (%)	N	Number infected (%)	Total infected (%)	Significant difference	Odd ratio	Sig.	Lower	Upper	
Rainy Season	2–4 years	148	12 (8.1)	158	15 (9.5)	27 (8.8)	χ 2 = 27.00, p = 0.40	Reference	
5–7 years	279	72 (25.8)	224	32 (14.3)	104 (20.7)	χ 2 = 94.61, p = 0.60	2.613	0.000	1.652	4.13	
8−10 years	116	78 (67.2)	161	46 (28.6)	124 (44.8)	χ 2 = 104.71, p = 0.72	10.031	0.000	5.740	17.52	
Sig. difference		χ 2 = 324.0, p = 0.458		χ 2 = 186.00, p = 0.445	χ 2 = 452.36, p = 0.460						
Dry season	2–4 years	78	6 (7.7)	88	7 (8.0)	13 (7.8)	χ 2 = 26.00, p = 0.41	Reference	
5–7 years	291	25 (8.6)	275	13 (4.7)	38 (6.7)	χ 2 = 91.43, p = 0.32	1.924	0.144	0.800	4.62	
8−10 years	172	71 (41.3)	177	51 (28.8)	122 (49.0)	χ 2 = 101.42, p = 0.51	8.840	0.000	3.543	22.05	
Sig. difference		χ 2 = 313.00, p = 0.041		χ 2 = 144.00, p = 0.041	χ 2 = 438.12, p = 0.040						
Note: Dry season: November to February; rainy season: May to August; N: number examined. p values in bold are significantly different. Probability significant level defined at p < 0.05.

John Wiley & Sons, Ltd.

During the dry season, the results showed a significant difference in the prevalence of fascioliasis among the different age groups (χ 2 = 438.12; p = 0.040). The prevalence of fascioliasis with respect to the different age groups showed a significant difference in the abattoirs in Bamenda (χ 2 = 313.00; p = 0.041) as well as in Bafoussam (χ 2 = 144.00, p = 0.041). In both Bamenda and Bafoussam, cattle of 8–10 years had a higher prevalence of fascioliasis (41.3%; 71/172) and (28.8%; 51/177), respectively. It was observed that cattle that were 8–10 years old had a significantly higher risk of infection compared to cattle of 2–4 years (OR: 8.84; p = 0.000).

3.7 Condemned liver in dry and rainy season

Out of the 543 cattle livers examined in Bamenda during the rainy season, 162 (29.83%) were infected with Fasciola spp. adult worms compared to 93 (17.12%) out of 543 carcasses in Bafoussam. During the dry, 541 carcasses were examined in Bamenda, and 102 (18.8%) were positive for Fasciola spp, whereas, in Bafoussam, 510 carcasses were examined and 71 (13.92) were infected. During the rainy season, 157.6 kg of livers were condemned in Bamenda and 99.8 kg in Bafoussam giving a total of 257.4 kg, whereas during the dry season, a total of 175.7 kg of livers were condemned with 98.1 kg in Bamenda and 77.6 kg in Bafoussam. Overall, the study showed a total of 433.1 kg of liver condemned and incinerated due to the presence of Fasciola spp (Table 8).

TABLE 8 Number of infected animals and the quantity of liver condemned and incinerated in abattoirs in Bamenda and Bafoussam.

	Bamenda	Bafoussam	Total weight of liver condemned (kg)	
Month	a	b (%)	c	a	b (%)	c	
Total	1084	264 (24.35)	255.7	1053	164 (15.57)	177.4	433.1	
Rainy season								
May	135	42 (31.11)	20.2	122	18 (14.75)	19.8	40	
June	151	41 (27.15)	35	135	24 (17.77)	26.7	61.7	
July	120	33 (27.5)	43.3	136	24 (17.64)	26	69.3	
August	137	46 (33.57)	59.1	150	27 (18.00)	27.3	86.4	
Total	543	162 (29.8)	157.6	543	93 (17.12)	99.8	257.4	
Dry season								
November	135	35 (25.29)	25.5	136	22 (16.17)	36.7	62.2	
December	136	28 (20.58)	19.5	134	19 (14.17)	25	44.5	
January	135	20 (14.81)	27.1	120	18 (15.00)	4.7	31.8	
February	135	19 (14.07)	26	120	12 (10.00)	11.2	37.2	
Total	541	102 (18.8)	98.1	510	71 (13.92)	77.6	175.7	
Note: a = number of carcasses examined; b = number of carcasses with Fasciola spp in liver; c = weight of liver condemned (kg).

John Wiley & Sons, Ltd.

3.8 Financial loss due to the condemned liver

As shown in Table 9, during the rainy season (May—August) and dry season (November—February), the total weight of liver condemned was 433.1 kg resulting in a total direct financial loss of 1221,550 Francs CFA (2049.64 USD) based on the price of 2800 francs CFA/kg of liver in Bamenda and 2850 francs CFA/kg in Bafoussam. The annual economic loss due to the condemned liver at the abattoir in Bamenda and Bafoussam was estimated to be 1814,775 FCFA (3045.01 USD).

TABLE 9 Fasciola spp. infection‐related financial losses recorded in slaughtered cattle during the rainy and dry seasons.

Location	Rainy season	Dry season	Total weight of livers	Total financial (FCFA)	
A	B	A	B	
Bamenda	157.6	441,280	98.1	274,680	255.7	715,960	
Bafoussam	99.8	284,430	77.6	221,160	177.4	505,590	
TOTAL	257	725,710	175.7	495,840	433.1	1221,550	
Direct financial loss in FCFA (in USD)	725,710 (1217.67)	495,840 (831.97)		1221,550 (2049.64)	
Annual financial loss in FCFA (in USD)	2151,992 (3610.83)	1474,965 (2474.84)		1814,775 (3045.01)	
Note: A: estimated weight of liver condemned (kg); B: direct financial loss through liver condemnation; 1 USD = 595.98 FCFA.

John Wiley & Sons, Ltd.

4 DISCUSSION

An overall prevalence of 19.75% was observed in cattle slaughtered in Bamenda and Bafoussam abattoirs. This prevalence is relatively higher than that recorded by Takang et al. (2020) at the abattoir in Yaoundé, and lower than the findings of Ntonifor and Ndaleh (2012) at the Douala abattoir. This difference may be justified by the difference in ecological zones as well as due to the origin of animals slaughtered in each abattoir. However, this prevalence is relatively higher than what Ntonifor et al. (2013) recorded in Jakiri and Atanga et al. (2019) in Bamenda in the same ecological zone. This high prevalence may be due to low sanitary control. In fact, as the outbreak of the socio‐political crises in the North West and South West Regions, most of the veterinary health delivery officers in the North West Region have abandoned their work stations in the cattle production basins to seek refuge in Bamenda. This has disrupted the deworming schedules that they used to have with the cattle grazers. Farmers’ poor knowledge, access to adequate veterinary services and improper use of anthelmintics may alter the dynamics of Fasciola spp. in endemic areas and further promote the prevalence of fascioliasis. The Western Highlands have a temperature range between 15 and 32°C, annual rainfall of 1500–2400 mm and relative humidity of 65%. These factors may provide conductive environment for breeding and survival of the snail intermediate host of fascioliasis (Nyirenda et al., 2019).

The results of this study equally revealed a lower prevalence of fascioliasis during the dry season than the rainy season with some animals having only the Fasciola spp. without eggs in cattle slaughtered in the study area. This could be due to the existence of positive relationship between the prevalence of fasciolosis and rainfall, humidity and temperature. Furthermore, usually, cattle acquire Fasciola at the onset of the rainy season through ingestion of infective metacercaria while grazing, when snail intermediate hosts (Lymnea species) come out of their hibernation and release large numbers of metacercaria. At this point, cattle come in contact with vegetation infected with metacercaria. The environmental and climatic conditions of the study area during the rainy season favouring the survival of the intermediate snail hosts could also be an additional reason justifying this high prevalence during the rainy season. In dry season, prevalence gradually decreased from November to February. This variation in Fasciola infection may be related to seasonal activities of the intermediate host snails. During the dry season, breeding of the snails and development of the larval flukes slow down or stop completely and the snails undergo a state of aestivation. Although a decreasing trend was observed along with the advancement of the dry season, relatively high infection rates were recorded throughout the study. This may be attributed to infection acquired during the previous peak snail activity season. In addition, the existence of permanent suitable ecological conditions in areas like lake borders, slow flowing rivers and low‐lying marshy plains of Ndop, Gayama, Mbaw, Noun Valley as well as Bamendjing dam may contribute to persistent but low‐grade infection during the dry season. High cattle population often concentrate at these sites to graze as these areas usually remain green during the dry season and constitute transhumance grazing foci.

The results of the present study showed a high prevalence of Fasciola spp. in Bamenda compared to Bafoussam. This can be attributed to the fact that though Bamenda and Bafoussam are both found in the Western Highlands, the cattle slaughtered in Bamenda come from areas whose ecological factors are more favourable for the development and transmission of Fasciola. It is worth noting that most cattle slaughtered in Bamenda are produced in the cattle producing basins of the region and transported to the city for slaughter (DREPIA North West, MINEPIA, 2013). The high prevalence in Bamenda is probably as a result of little intervention conducted by the Veterinary and Public Health officers through educational awareness campaigns due to the socio‐political crises in the North West and South West Regions for the last 7 years.

The results indicated that Fasciola infection rate was higher in females than in their male counterparts. This may be explained on the basis that cattle owners keep cows in their farms for longer periods because they are used for reproduction as well as produce milk unlike the bulls. This longer stay makes them more exposed to parasitic diseases like fascioliasis (Oladele‐Bukola & Adetokun, 2014). The least numbers of infected cattle were observed in the age group of <2 years, whereas highest prevalence was recorded in the age group of 8–10 years. This observation may be attributed to the lower chances of acquiring infection due to short exposure compared to older animals. The association of age found in the present study is in agreement with the results of Keyyu et al. (2005) who observed that fewer animals less than 2 years were infected as compared to older cattle. Similar observations were reported by Oladele‐Bukola and Adetokun (2014). The number of males that were presented at slaughter was higher because males generate higher income for cattle sellers than the female animals. These findings are in agreement with other works reported by Phiri et al. (2005) and Keyyu et al. (2005).

In the current study, the economic loss due bovine fascioliasis associated with liver condemnation estimated from the total number of cattle slaughtered per year was estimated to 1814,775 (3045.01 USD) in the Western Highlands of Cameroon. However, this amount may not represent actual losses, and it can be considered high for a middle income country like Cameroon. This financial loss, which is only due to liver condemnation, demonstrates that fascioliasis is still one of the causes of losses of the economy in the highlands of Cameroon. Additionally to the losses due to the quality carcass, reduction in growth rate and reduction of milk demonstrates fascioliasis remain one of causes of poverty of the population in Cameroon. This may result in important decreases of the household incomes of small‐scale farmers, as reported elsewhere (Nyirenda et al., 2019).

A total of 257 kg of liver, valued at 725,710 FCFA ($1217.67), was condemned during the rainy season; this value was significantly high compared to the dry seasons. This difference might be as a result of the influence of high prevalence of bovine fasciolosis observed during this season.

The fact that more livers were condemned during the rainy season may result from the fact that cattle may acquire the infective stage of Fasciola while grazing at river banks and around water bodies during the dry season when animals were taken in the valley. The development of lesion may occur during the dry season. Therefore, at rainy season, gross pathological lesion may become more obvious with a corresponding increase in the number of livers condemned. Economic losses from bovine fasciolosis have been reported in other parts of the world. In Ethiopia, for example, a yearly direct financial losses financial loss of 47,945.24 USD was attributed to condemnation of liver due to bovine fascioliasis (Mathewos et al., 2023).

5 CONCLUSION

The results of this study demonstrated that bovine fasciolosis is endemic in cattle slaughtered in Bamenda and Bafoussam abattoirs, with a significantly high prevalence during the rainy season in the Western Highlands of Cameroon. Condemnation of livers due to the detection of gross pathology caused by fasciolosis in cattle slaughtered accounts for huge financial losses which occur more during the season.

Following that, it can recommend that control measures for the disease (regular examination and deworming) should be reinforced in order to reduce these losses. Veterinary services in the area should take a compulsory deworming programme. In all abattoirs of the area, meat inspection should be intensified and slaughter slabs to monitor and improve on the health of the animals and human beings. Moreover, it is important to educate the public about the significance of this snail‐borne disease in the Western Highlands of the country. It is also important to determine the extent of the infection in humans in the study area.

AUTHOR CONTRIBUTIONS

Heinendez Merrius Atanga: Conceptualization; data curation; formal analysis; funding acquisition; investigation; writing – original draft. Ngum Helen Ntonifor: Conceptualization; supervision; writing—review and editing. Oumar Mahamat: Conceptualization; formal analysis; supervision; writing—original draft; writing—review and editing.

CONFLICT OF INTEREST STATEMENT

Authors declare that there are no conflicts of interest.

FUNDING INFORMATION

Authors declare that they have not received any financial support.

ETHICS STATEMENT

This study was carried out with the collaboration of the Ministry of Livestock Fisheries and Animal Industries (MINEPIA) staff regularly on duty at the abattoir following the routine meat inspection guidelines for developing countries described by FAO (2009). Authorizations were obtained from the Ministry of Livestock Fisheries and Animal Industries (MINEPIA/DREPIA/SRAG/NW/40/86 of 31/03/2022) and the head of the abattoir (No: 026/22/AS/MINEPIA/SG/DREPIA‐O/SRAG of 13 July 2022).

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.70002.

DATA AVAILABILITY STATEMENT

Data are available from the corresponding author.
==== Refs
REFERENCES

Atanga, M. H. N. , Keambou, C. , & Kimbi, H. (2019). Bovine Fasciola infection: Prevalence and intensity among cattle slaughtered in Bamenda Abattoir. International Journal of Biomedical Research, 10 (6 ), e4981.
Cheesbrough, M. (1992). Medical laboratory manual for tropical countries (2nd ed.). Cambridge University Press.
Cheesbrough, M. (2009). Medical laboratory manual for tropical countries (Col ‐1) 2. London Great British University Press.
Diyana, J. N. A. , Lokman, I. H. , Fazila, S. H. N. , Latiffah, H. , Ibitoye, E. B. , Hazfalinda, H. N. , Chandrawathani, P. , Juriah, K. , & Mahiza, M. I. N. (2019). A retrospective study on bovine fascioliasis in veterinary regional laboratories in Peninsular Malaysia. Journal of Parasitology Research, 2019 , 7903682.31354983
Ephrem, B. , Wassie, M. , & Abadi, A. (2012). Prevalence and economic loss of bovine fascioliasis in Dessie Municipal Abattoir, Ethiopia. European Journal of Biological Science, 4 (2 ), 53–59.
Food and Agriculture Organization and World Organization for Animal Health . (2021). Bulletin: Foodborne parasitic infections‐fascioliasis . Food and Agriculture Organization and World Organization for Animal Health.
Keiser, J. , & Utzinger, J. (2009). Food‐borne trematodiases. Clinical Microbiology Revised, 22 , 466.
Keyyu, A. M. , Phiri, I. K. , Phiri, C. S. , & Sikasunge, J. (2005). Prevalence of fascioliasis in Zambian cattle observed at selected abattoirs with emphasis on age, sex and origin. Journal of Veterinary Medicine, 52 (9 ), 414–416.16283922
Lalor, R. , Cwiklinski, K. , Calvani, N. E. D. , Dorey, A. , Hamon, S. , Corrales, J. L. , Dalton, J. P. , & De Marco Verissimo, C. (2021). Pathogenicity and virulence of the liver flukes Fasciola hepatica and Fasciola gigantica that cause the zoonosis fasciolosis. Virulence, 12 (1 ), 2839–2867.34696693
Madkour, F. A. , & Al‐Amgad, Z. (2023). Histopathological investigations of the bovine fascioliosis in liver and lymph node. SVU‐International Journal of Veterinary Sciences, 6 (1 ), 116–126.
Mas‐Coma, S. , Bargues, M. D. , & Valero, M. A. (2005). Fascioliasis and other plant‐borne trematode zoonoses. International Journal of Parasitology, 35 , 1255–1278.16150452
Mathewos, M. , Endale, H. , & Kebamo, M. (2023). Coprological and postmortem assessment and economic significance of bovine fascioliasis in cattle slaughtered at Tarcha Municipal Abattoir, Southern Ethiopia. Parasite Epidemiology and Control, 22 (2023 ), e00316.37521359
Ministry of Livestock Fisheries and Animal Industries (MINEPIA) . (2013). Annual report . Ministry of Livestock Fisheries and Animal Industries.
Ministry of Livestock Fisheries and Animal Industries (MINEPIA) . (2018). Annual report . Ministry of Livestock Fisheries and Animal Industries.
Mungube, E. , Bauni, S. , Tenhagen, B. A. , Wamae, L. , Nginyi, J. , & Mugambi, J. (2006). The prevalence and economic significance of Fasciola gigantica and Stilesia hepatica in slaughtered animals in the semi‐arid coastal Kenya. Tropical Animal Health and Production, 38 , 475–483.17243475
Mwabonimana, M. F. , Kassuku, A. A. , Ngowi, H. A. , Mellau, L. S. B. , Nonga, H. E. , & Karimuribo, E. D. (2009). Prevalence and economic significance of bovine fasciolosis in slaughtered cattle at Arusha abattoir, Tanzania. Tanzania Veterinary Journal, 26 , 68–74.
Ntonifor, H. N. , & Ndaleh, W. N. (2012). Prevalence of liver fluke infections and other gastrointestinal tract parasites in slaughtered cattle in Douala, Cameroon. Bulletin of Animal Health and Production in Africa, 4 (11 ), 288–295.
Ntonifor, H. N. , Shei, S. J. , Ndaleh, N. W. , & Mbunkur, G. N. (2013). Epidemiological studies of gastrointestinal parasitic infections in ruminants in Jakiri, Bui Division, North West Region of Cameroon. Journal of Veterinary Medicine and Animal Health, 5 (12 ), 344–352.
Nyirenda, S. S. , Sakala, M. , Lennon, M. , Edgar, K. , Paul, F. , Fredrick, B. , & Yona, S. (2019). Prevalence of bovine fascioliasis and economic impact associated with liver condemnation in abattoirs in Mongu district of Zambia. BMC Veterinary Research, 15 , 33.30665406
Oladele‐Bukola, M. O. , & Adetokun, A. I. (2014). Prevalence of bovine fascioliasis at Ibadan Municipal Abattoir. Nigeria. African Journal of Food Agriculture Nutrition and Development, 14 (4 ), 9055–9070.
Pace, J. E. , & Wakeman, D. L. (1983). Determination of the age cattle by their teeth. University of Florida: IFAS Extension. https://www.edis.ifas.ufl.edu/ANO46
Pfukenyi, D. S. , & Mukaratirwa, S. (2004). A retrospective study of the prevalence and seasonal variation of Fasciola gigantica in cattle slaughtered in the major abattoirs of Zimbabwe between 1990 and 1999. Onderstepoort Journal of Veterinary Research, 71 , 181–187.15580766
Phiri, A. M. , Phiri, I. K. , Sikasunge, C. S. , & Monrad, J. (2005). Prevalence of fascioliasis in Zambia cattle observed at selected abattoirs with emphasis on age sex and origin. Journal of Veterinary Medicine Series B, 52 (9 ), 414–416.16283922
Rahmeto, A. , Fufa, A. , Mulugeta, B. , & Mekuria, S. (2010). Fasciola: Prevalence, financial losses due liver condemnation and evaluation of simple sedimentation technique in cattle slaughtered at Hawassa Municipal abattoir, Ethiopia. Ethiopia Veterinary Journal, 14 (1 ), 39–51.
Roberts, J. A. & Suhardono . (1996). Approaches to the control of fasciolosis in ruminants. International Journal of Parasitology, 26 (8‐9 ), 971–981.8923144
Soulsby, E. J. L. (1986). Helminths, arthropods and protozoa of domesticated animals. Bailliere Tindall.
Takang, A. A. , LeBreton, M. , Ayuk, C. E. , & MacLeod, E. T. (2020). A socio‐economic study of Fasciola infections in cattle and sheep at the Etoudi slaughterhouse, Yaoundé, Cameroon. Journal of Helminthology, 94 , e92.
Thursfield, M. (2005). Veterinary epidemiology (2nd ed.). University of Edinburgh.
World Health Organization . (2006). Report of the WHO expert consultation on foodborne trematode infections and taeniasis/cysticercosis. Vientiane, Lao people's Democratic Republic, 12–16 October 2006 Geneva . WHO.
