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A systematic review and meta-analysis on the prevalence of amphistome infection in domestic ruminants in the sub-Saharan Africa region

Published online by Cambridge University Press:  11 December 2024

I. Nyagura Open the ORCID record for I. Nyagura [Opens in a new window] ,
M.P. Malatji ,
P.I. Ngcamphalala  and
S. Mukaratirwa
I. Nyagura*
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban 4001, South Africa
M.P. Malatji
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban 4001, South Africa
P.I. Ngcamphalala
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban 4001, South Africa
S. Mukaratirwa
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban 4001, South Africa One Health Centre for Zoonoses and Tropical Veterinary Medicine, Ross University School of Veterinary Medicine, Basseterre, St Kitts and Nevis, West Indies
*
Corresponding author: I. Nyagura; Email: nyaguraigy@gmail.com/221119814@stu.ukzn.ac.za
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Abstract

Systematic review and meta-analysis were conducted to provide comprehensive information on the prevalence of amphistome infections in domestic ruminants in sub-Saharan Africa. A systematic search of peer-reviewed articles published between 2002 and 2023 was conducted. Prevalence estimates and meta-analysis were based on 76 peer-reviewed articles which met the inclusion criteria. Of the 55,122 domestic ruminants screened, 12,858 were infected, and the overall pooled prevalence was 22% (95% confidence interval [CI], 10-37). The highest prevalence was recorded in southern Africa 25% (95% CI, 0-62), and central Africa 16% (95% CI, 0-61) the lowest. Cattle were the most frequently sampled hosts (76.56%, n = 42,202) and sheep (8.78%, n = 4838) the lowest, and cattle recorded the highest pooled prevalence of 28% (95% CI, 12-47), and goats the lowest at 5% (95% CI, 0-14). Prevalence rate was the high in males 32% (95% CI, 21-44), adult ruminants 37% (95% CI, 15-62) and animals with poor body condition 47% (95% CI, 34-60), and during the wet season 36% (95% CI, 0-94). The highest pooled prevalence was recorded at postmortem 23% (95% CI, 8-43) compared to coprology 20% (95% CI, 6-39) studies. The meta-regression model demonstrated that the body condition score, host, and period, and the interactions of different factors significantly influenced the prevalence. The lowest prevalence rate was noted for the period between 2013 and 2023. This is the first systematic review and meta-analysis in sub-Saharan Africa that provides a comprehensive review of the prevalence of amphistome infections in domestic ruminants in the past 20 years.

Keywords

prevalenceamphistomesdomestic ruminantssub-Saharan Africacattlesheepgoats
Type
Review Article
Information
Journal of Helminthology , Volume 98 , 2024 , e80
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Introduction

Livestock farming is critical to the socioeconomic development of sub-Saharan Africa because it provides food security, income production, and livelihood support to millions of people, particularly in resource-poor livestock farming communities (Erdaw, Reference Erdaw2023). Parasitic infections, on the other hand, pose a severe threat to cattle health and productivity, resulting in huge economic losses for the region (Phiri et al., Reference Phiri, Chota and Phiri2007, Zvinorova et al., Reference Zvinorova, Halimani, Muchadeyi, Matika, Riggio and Dzama2016; Chongmobmi & Panda, Reference Chongmobmi and Panda2018). Amphistomes commonly known as “conical flukes” have emerged as a major source of concern globally, affecting a variety of domesticated ruminant species such as cattle, sheep, and goats (Horak, Reference Horak1971; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018). Hence, they have been recognised for their major threats to sub-Saharan Africa’s livestock industry, causing significant economic losses due to stunted growth including death in young animals, low food conversion rates, poor milk, meat, and wool production, and poor hide and skin quality (Pfukenyi et al., Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005; Bunza et al., Reference Bunza, Ahmad and Fana2008). Despite these negative impacts, amphistomosis is still a neglected tropical disease of ruminant livestock (Hotessa & Kanko, Reference Hotessa and Kanko2020).

Amphistomes are digenetic trematodes from the subfamily Paramphistomoidea Fischoeder, 1901 (Lotfy et al., Reference Lotfy, Brant, Ashmawy, Devkota, Mkoji and Loker2010; Mitchell et al., Reference Mitchell, Zadoks and Skuce2021). They have a heteroxenous life cycle, with aquatic snails serving as obligatory intermediate hosts and ruminants as definitive hosts. More than 70 amphistome species have been recorded globally (Ghatani et al., Reference Ghatani, Shylla, Tandon, Chatterjee and Roy2012) and in sub-Saharan Africa, 36 species have been documented in wild ruminants (Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024); the majority of these species is shared between both domestic and wild ruminants (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018; Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024). Adult amphistomes inhabit the digestive system of ruminants specifically in the rumen and reticulum (Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024), and immature stages cause intestinal amphistomosis, also known as amphistomiasis (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018). Adult amphistomes cause localised loss of rumen papillae, whereas immature flukes penetrate the mucosa of the duodenum and upper ileum to plug feed, causing necrosis and haemorrhagic duodenitis, resulting in severe pathological changes (Mavenyengwa et al., Reference Mavenyengwa, Mukaratirwa, Obwolo and Monrad2005; Opara et al., Reference Opara, Chikezie, Udoidung, Yaro, Onwumerobi and Afia2017). The immature amphistomes may cause significant mortality rates in domesticated ruminants, reaching up to 80% to 90% (O’Shaughnessy et al., Reference O’Shaughnessy, Garcia-Campos, McAloon, Fagan, de Waal, McElroy, Casey, Good, Mulcahy, Fagan and Murphy2018; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018).

This disease has a global distribution; however, the prevalence and intensity of infection differ by country and location (Ghatani et al., Reference Ghatani, Shylla, Tandon, Chatterjee and Roy2012; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018; Nyagura et al., Reference Nyagura, Malatji and Mukaratirwa2024). Climate and local environmental variables, such as humidity, temperature, rainfall, and vegetation, have an impact on the prevalence and intensity of infection in pasture (Hajipour et al., Reference Hajipour, Mirshekar, Hajibemani and Ghorani2021; Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024). The epidemiological pattern of amphistome infection in domestic animals is impacted by production management systems, grazing behaviour of animals, and the presence of infected definitive hosts (Horak, Reference Horak1971) and the intermediate host species (Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024). The prevalence of infection may differ based on the age, sex, and physiological state of an animal, animal species, and between seasons (Horak, Reference Horak1971; Kanyari et al., Reference Kanyari, Kagira and Mhoma2010; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018).

Although several field-based studies have been conducted to determine the prevalence of amphistome infections in livestock in sub-Saharan Africa, the prevalence estimate for the region is not known. A complete synthesis of current data on amphistome prevalence in domestic ruminants across sub-Saharan Africa through a systematic review and meta-analysis is critical as it can offer a more accurate estimation of the disease burden, identify high-risk locations, and assist in the design of evidence-based interventions for prevention and control.

Materials and methods

Search strategy

Four electronic databases, Google Scholar, PubMed, Science Direct, and Web of Science, were used to conduct a systematic literature search for peer-reviewed publications from 2002 to 2023, following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Boolean operators (AND, OR) were used in conjunction with the following selected key terms; amphistome infection OR amphistomosis OR paramphistome infections OR paramphistomosis, rumen flukes OR conical flukes AND domestic ruminants OR livestock OR cattle OR sheep OR goats, AND prevalence in sub-Saharan Africa. Related studies were retrieved based on a preliminary screening of the titles and abstracts. Additional studies were searched manually through cross-referencing of the eligible studies. The literature search was limited to English. All full-text articles selected were imported and managed in the EndNote reference manager version X8 (Clarivate Analytics, Philadelphia, PA, USA).

Inclusion and exclusion criteria

The inclusion criteria were: (1) the study was carried out in sub-Saharan Africa, (2) the host animal (domestic ruminant) was indicated, (3) the sample size and number of positive cases clearly stated, (4) the prevalence was based on natural infections, and (5) diagnostic/identification method was clearly stated.

Excluded from this review were articles that reported on amphistome infections in non-ruminants, amphistome infections in wildlife, and studies conducted outside sub-Saharan Africa. Furthermore, articles published in other languages besides English, or outside the period of study, duplicate studies, studies without full-texts, reviews, unpublished reports, conference abstracts, and dissertations were also excluded.

Data extraction

To eliminate bias in the literature search, the retrieved studies were thoroughly checked independently by two reviewers (I.N. and M.P.M.). Thereafter, articles not fulfilling the inclusion criteria, duplicate, and low-quality assessed articles were excluded from meta-analysis. For meta-analysis, data extracted from text, tables, and figures were computed and processed in MS Excel with the authors’ names, published year, location, animal species, diagnostic/identification method, the number of animals examined, case positives, and prevalence rate.

Quality assessment

The quality of each study for meta-analysis was evaluated independently following the Grading of Recommendations Assessment, Development, and Evaluation methods criteria by Guyatt et al. (Reference Guyatt, Oxman, Vist, Kunz, Falck-Ytter, Alonso-Coello and Schünemann2008). Studies that met the inclusion criteria outlined were assigned a score of 1 point if complete information was provided and 1 point for each subsequent inclusion criterion that was met. Thus, all the studies were given a score between 0 and 5 points. Publications with a total score of 5 points were deemed good quality, 4 moderate quality, and ≤3 as low quality and were excluded. The standardized quality index score (between 0 and 1) based on quality was then computed (supplementary table 1).

Meta-analysis and meta-regression

Prevalence data were transformed using the double arcsine method to avoid overestimating the weight of individual studies (Barendregt et al., Reference Barendregt, Doi, Lee, Norman and Vos2013). The MetaXL add-in for Microsoft Excel (www.epigear.com) was used to assess the quality effects model to account for the heterogeneity. Heterogeneity between estimates was evaluated using the inverse variance statistic (I 2 index), and its significance was tested using Cochrane’s Q test. Following Higgins et al. (Reference Higgins, Thompson, Deeks and Altman2003) protocol, the I 2 score of 25%, 50%, or 75% was interpreted as low, moderate, or high heterogeneity, respectively. Forest plots were used to graphically demonstrate the estimated prevalence and the 95% confidence interval (CI) of amphistome among hosts. To evaluate the prevalence estimates for the major subgroups, meta-analysis was computed for geography (region), animal host, detection method, age (young and adult), sex (male and female), body condition score (BCS), seasonality (wet and dry), and years. Funnel plots were used to evaluate the publication bias. IBM SPSS Statistics 28.0 was used for all subsequent statistical analyses. To identify the sources of heterogeneity, univariate meta-regression was performed with region, host, sex, age, body condition factor, study type and study period fixed as independent factors. The meta regression was treated as linear model on the logit transformed prevalence data. The linear regression analysis was conducted to evaluate publication bias using Egger’s test. The Trim and Fill approach was employed after the Egger’s test to evaluate the possible influence of publication bias on the total effect size.

Results

Search results and characteristics of eligible studies

A literature search on Google Scholar, PubMed, Science Direct, and Web of Science generated 1571 records (Fig. 1). Snowballing resulted in an additional five articles. Four hundred and forty-seven duplicates were removed, and the titles and abstracts of the remaining 1129 articles were reviewed for eligibility, with 1014 articles ruled invalid and excluded. One hundred and fifteen full-text papers were evaluated using the predefined inclusion criteria and 39 articles did not fulfil the criteria and were excluded from the review. Thus, 76 articles met the inclusion criteria.

Figure 1. PRISMA flow diagram.

The 76 publications were distributed across 12 of the 50 countries in the sub-Saharan African region, of which 50% (n = 38) came from Eastern Africa, 36.84% (n = 28) from Western Africa, 10.53% (n = 8) from Southern Africa, and 2.6% (n = 2) from Central Africa (Fig. S1). Supplementary file 1 (Table S1) summarizes the key characteristics of the reviewed research articles. The findings revealed that 30.47% (12,858 of 42,202) cattle, 7.46% (603 of 8082) goats, and 13.81% (668 of 4838) sheep were infected with amphistomes (Table 1).

Table 1. Pooled prevalence of amphistome infections in domestic ruminants in sub-Saharan Africa based on different risk factors

Meta-analysis

The overall prevalence of amphistomes in domestic ruminants was 22% (95% CI, 10-37) (Fig. 2). The quality effects model revealed a significantly high heterogeneity in the studies included in the meta-analysis, (I² = 99%, P < 0.01), with Q=13862.01. This high heterogeneity confirms that the studies under this meta-analysis are from different populations. Publication bias analysis revealed asymmetric funnel plots (Supplementary file 2: Fig. S2) which indicated publication bias in the appraised studies. The results of the Egger’s test revealed a significant publication bias (P = 0.023), which is in line with the findings of the funnel plot. The imputed and observed effect sizes were found to be comparable by the Trim and Fill analysis results, and no studies were excluded from the study.

Figure 2. Forest plot for the prevalence of amphistome infections in domestic ruminants in sub-Saharan Africa.

Prevalence by region

The prevalence estimates from different regions are shown in Fig. 3a-d. The results of the study established that the southern region of Africa had the highest pooled prevalence of 25% (95% CI, 0-62) (Fig. 3c), followed by eastern and western Africa with 21% (95% CI, 14-29) and 21% (95% CI, 11-33), respectively (Fig. 3b, d). The least pooled prevalence of 16% (95% CI, 0-61) (Fig. 3a) was noted from central Africa. Results from the quality effects model revealed a high degree of heterogeneity between studies from all the regions with (I² =99%, P < 0.01) from eastern and western Africa; (I² =100%, P < 0.01) from southern Africa and (I² =98%, P < 0.01) from central Africa.

Figure 3. Forest plots of prevalence of amphistome in domestic ruminants from (A) central Africa, (B) eastern Africa, (C) western Africa, and (D) southern Africa recorded from 2002 to 2023.

Prevalence by host

The pooled prevalence of amphistome in cattle, goats, and sheep is shown in Fig. 4a-c. The highest prevalence was estimated in cattle 28% (95% CI, 12-47) followed by sheep 11% (95% CI, 4-20) and substantially lower for goats 5% (95% CI, 0-14). The quality effects model revealed a substantially high degree of heterogeneity between studies on different hosts, for cattle (I² =99%, P < 0.01) and for goats and sheep (I² =98%, P < 0.01).

Figure 4. Forest plots of prevalence of amphistome in (A) cattle, (B) goat, (C) sheep from 2002 to 2023.

Risk factors for infection

The sub-group on risk factors for infections in domestic ruminants is presented in Table 1. The quality effects model revealed a high degree of heterogeneity between studies from all sub-groups on risk factors infections in ruminants with I² >95% (P < 0.01) except for I² =89% (P < 0.01) on the medium body condition. The pooled prevalence for males at 32% (95% CI, 21-44) was higher than that of the females at 23% (95% CI, 13-36). Adult animals had a higher prevalence estimate at 37% (95% CI, 15-62) compared to young animals at 23% (95% CI, 5-52). The highest prevalence was estimated in the wet season at 36% (95% CI, 0-94) compared to the dry season at 21% (95% CI, 1-54). Animals with poor BCS had the highest prevalence estimate of 47% (95% CI, 34-60), followed by those with moderate BCS at 26% (95% CI, 13-42) and the lowest prevalence estimate was on animals with good BCS at 10% (95% CI, 1-25). The pooled prevalence measured by coprology 20% (95% CI, 6-39) was lower than the one measured at postmortem 23% (95% CI, 8-43). The years between 2002 and 2012 had a higher pooled prevalence of 29% (95% CI, 6-59) compared to 14% (95% CI, 10-19) noted between 2013 and 2023.

Heterogeneity and publication bias

The univariate meta-regression findings for the overall and subgroups for individual variables are displayed in Supplementary Table 2. Univariate meta-regression models identified three sources of variability in the prevalence of amphistome in domestic ruminants (P < 0.05). Condition factor had the greatest influence on heterogeneity, accounting for 60.1% of the variation. The heterogeneity of domestic amphistomosis was also explained by the differences in host and period in which studies occurred (P < 0.001), accounting for 15.6% and 14.8%, respectively. The analysis revealed that the period in which the studies were conducted significantly (P < 0.05) explains 21.6% and 27.7% of the variation in prevalence in the eastern and western regions, respectively. Furthermore, the two identified sources of heterogeneity for cattle, were study type and period (P < 0.001), which contributed 54.7% and 22.5% of the variation, respectively.

The combined variables had a substantial impact (P < 0.001) on the overall prevalence outcome accounting for 33.4% of the variation, with host and period (P < 0.001) as the major sources of heterogeneity (Supplementary Table 3). A combined meta-regression shows that all model predictors may significantly (P < 0.05) account for approximately 30.3% of the variability in the result in the eastern region and 27.9% in the western region. The only predictor variable that showed a statistically significant link with a P value less than 0.05 for both the eastern and western regions was the period as a factor. The combined variables in southern Africa accounted for 63.8% of the variability in the prevalence outcome, with a significant difference (P = 0.036). However, only the study type variable was statistically significant (P < .05). The prevalence of amphistome in cattle was significantly influenced by study type and period (P < .05) and all predictors together contributed 45.9% of the variation. However, for sheep and goats, the combined predictor factors had no significant effect on the prevalence outcome (P > .05). The combined factors significantly accounted for 34% and 30.6% of the variation in the prevalence outcome for age and sex, respectively. For the years 2002 through 2012 and 2013 through 2023, respectively, the combined variables explained 13.4% and 68.5% of the variation in the prevalence outcome.

Discussion

Despite the importance of amphistomes in livestock production, information on their prevalence in cattle, sheep, and goats is sporadic and limited in most sub-Saharan African countries, with data available from only 12 of the region’s 50 countries. Results demonstrated that more studies were conducted in the eastern region and western regions, which could be attributed to large number of livestock farmer practising extensive farming in these regions, and thus exposing animals to infection (FAO, 2017; Abera et al., Reference Abera, Kebede, Haile and Bekuma2023). The study found that the overall prevalence of amphistome in ruminants was lower in the most recent years (2013-2023). The decrease in the prevalence of amphistome infections can be attributed to farmers’ increased awareness of the risks associated with these parasites, improvements in the quality of veterinary services and management approaches, and improved hygiene and sanitation standards as proposed by Nyagura et al. (Reference Nyagura, Malatji and Mukaratirwa2024). Furthermore, differences in sample size, sampling processes, and diagnostic criteria can all have a significant impact on the results and contribute to the high heterogeneity. The considerable heterogeneity in the host subgroup may also be attributed to the various animal breeds examined (Kanyari et al., Reference Kanyari, Kagira and Mhoma2010; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018).

The estimated prevalence varies by region in sub-Saharan Africa with the Southern African region recording the highest pooled prevalence of amphistome infections, followed by the east and west, and central Africa with the lowest. The findings of this study are similar to those reported by Sibula et al. (Reference Sibula, Nyagura, Malatji and Mukaratirwa2024), who also recorded the highest prevalence rates of amphistome infections in wild ruminants from southern African countries. Pfukenyi & Mukaratirwa (Reference Pfukenyi and Mukaratirwa2018) proposed that the geographical distribution and prevalence of amphistome infections are influenced by the availability and abundance of susceptible definitive hosts. This may explain high amphistome infection rates in the east and west, where livestock populations are higher (FAO, 2017; Abera et al., Reference Abera, Kebede, Haile and Bekuma2023). However, Eduardo (Reference Eduardo1987) argued that the establishment of an amphistome species in a given region may be more dependent on the intermediate host than the final host. The variations in estimated prevalence between regions could be attributed to different climatic conditions (Gonzalez-Warleta et al., Reference Gonzalez-Warleta, Lladosa, Castro-Hermida, Martínez-Ibeas, Conesa, Munoz, López-Quílez, Manga-González and Mezo2013; Hajipour et al., Reference Hajipour, Mirshekar, Hajibemani and Ghorani2021), environmental conditions, ecology, host-parasite interaction, and collection season and management systems (Phiri et al., Reference Phiri, Chota, Muma, Munyeme and Sikasunge2011; Hajipour et al., Reference Hajipour, Mirshekar, Hajibemani and Ghorani2021; Tookhy et al., Reference Tookhy, Mahiza, Mansor, Yasmin, Ahmad, Hamzah and Idris2022). The regional variation in the prevalence rate of amphistome noted may also be influenced by the number of research undertaken in different regions. The prevalence of amphistome in domestic ruminants in central Africa may have been underestimated and cannot be relied on due to a paucity of studies conducted in the region.

The highest pooled prevalence was recorded in cattle, followed by sheep, whereas goats had the lowest. This was consistent with the findings by Rolfe (Reference Rolfe, Boray, Nichols and Collins1991), who reported that trematode infections were more frequent in cattle but less so in small ruminants. This could be explained by the varied feeding behavior of the animals (Mohammed et al., Reference Mohammed, Animut, Urge and Assefa2020), as cattle and sheep are grazers close to the ground, using their tongues to pull grass into their mouths or their lips and teeth to selectively consume vegetation close to the ground which subsequently makes them more susceptible to trematode infective stages (Yohanna et al., Reference Yohanna, Dung, Adejoh and Pam2019). Although the nibling tendencies of sheep (Mohammed et al., Reference Mohammed, Animut, Urge and Assefa2020) may decrease their exposure to aquatic vegetation contaminated with metacercariae, which play a crucial role in trematode life cycles. However, if the grazing environment contains infective trematode stages, such as metacercariae on the vegetation, sheep can still become infected (Kanyari et al., Reference Kanyari, Kagira and Mhoma2009). As observed in our results, Yusuf et al. (Reference Yusuf, Jima and Aseffa2024) also reported higher prevalence in sheep than goats and attributed the differences in grazing patterns between sheep and goats, which predisposed sheep more to the infective larval stages compared to goats. Goats are recognised for their browsing habits (Mohammed et al., Reference Mohammed, Animut, Urge and Assefa2020) which limit their exposure to infective stages of trematodes present near the ground (Tsotetsi et al., Reference Tsotetsi, Njiro, Katsande, Moyo, Baloyi and Mpofu2013). Dube et al. (Reference Dube, Masanganise and Dube2010) showed the same trend of sheep being better hosts than goats but indicated that goats develop better immunity than sheep which might also account for the differences in the parasite loads between them.

Several researchers have suggested that gender appears to have no bearing on infection allowances and propose that both males and females are equally prone to and vulnerable to infection (Keyyu et al., Reference Keyyu, Monrad, Kyvsgaard and Kassuku2005, Reference Keyyu, Kassuku, Msalilwa, Monrad and Kyvsgaard2006; Kanyari et al., Reference Kanyari, Kagira and Mhoma2009, Reference Kanyari, Kagira and Mhoma2010). Reviewed studies showed that males had greater pooled prevalence estimates than female hosts. This report contradicted other researchers who recorded significantly higher prevalence in females than males, which they attributed to the females’ immunological conditions during gestation and lactation, when they may be more susceptible to infection (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018; Zewde et al., Reference Zewde, Bayu and Wondimu2019). This was corroborated by Pfukenyi et al. (Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005), who reported a much higher prevalence in pregnant and lactating animals. However, the discrepancies observed in the reviewed studies could be attributed to differences in sample size, with more females being examined than male hosts.

The findings indicated that young animals were less likely to be infected than older animals. Similar observations were made where older animals were more susceptible to infection, and implying that age has a significant impact on the prevalence of trematodes (Aragaw et al., 2012; Zewde et al., Reference Zewde, Bayu and Wondimu2019). Pfukenyi & Mukaratirwa (Reference Pfukenyi and Mukaratirwa2018) attributed this to prolonged exposure in adults, which resulted in tolerance to the pathogenic effects of immature amphistomes while mature ones maintained their high egg production capacity. Furthermore, Zewde et al. (Reference Zewde, Bayu and Wondimu2019) noted that older animals are allowed to graze on pasture for longer periods, potentially contributing to a higher infection rate than young animals. Meguini et al. (Reference Meguini, Righi, Boucheikhchoukh, Sedraoui and Benakhla2021) hypothesized that amphistomiosis is more common in older cattle due to their reduced immune systems. Results showed that poor conditioned cattle had the highest overall prevalence which aligned with Kanyari et al. (Reference Kanyari, Kagira and Mhoma2010) report which found a link between low body condition and high amphistome prevalence in cattle based on coprology. Heavy infections are thought to cause weakness, repeated ruminal tympany, ruminal atony, weight loss, anaemia, and production losses (Anuracpreeda et al., Reference Anuracpreeda, Wanichanon and Sobhon2008; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018). Furthermore, Mpofu et al. (Reference Mpofu, Slayi, Mutero, Mlahlwa and Jaja2023) also indicated that parasitic infections can affect nutrient absorption and utilisation, potentially impacting overall growth. Analysis indicated that the host, period, and condition factors all significantly contributed to the heterogeneity in the prevalence. However, the variability became much more common when different factors are combined, indicating that understanding the interactions between these factors is crucial to understanding the complexity of epidemiological outcomes. The findings of this study support the notion that the epidemiology of amphistome parasites is usually caused by a confluence of factors that interact considerably rather than by a single determinant (Hajipour et al., Reference Hajipour, Mirshekar, Hajibemani and Ghorani2021). However, there was no observed relationship between body condition and amphistome infections in small ruminants because there was no data for meta-analysis.

The wet season was associated with higher pooled prevalence of amphistome infection in cattle compared to the dry season. Pfukenyi et al. (Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005) suggested that a high faecal egg counts during the wet season may be due to mature infections acquired during the preceding dry season. This observation contradicted other authors who noted the highest degree of parasite contamination in pasture occurs during the dry season (Chingwena et al., Reference Chingwena, Mukaratirwa, Kristensen and Chimbari2002; Phiri et al., Reference Phiri, Phiri, Chota and Monrad2007b). Pfukenyi et al. (Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005) further reported that only light infections are likely to occur since snail habitats and pastures are frequently inundated, flushing snails and free-living parasite stages out and disseminating them across a vast area. Mia et al. (Reference Mia, Hasan and Chowdhury2021) added that the extreme temperatures hinder the pathogenic phases of the parasite during the summer.

Meta analysis could not be performed at a species level, and this may be attributed to lack of prevalence statistics at the species level due to technical challenges in specific identification (Phiri et al., Reference Phiri, Phiri and Monrad2006). This was also consistent with Pfukenyi et al. (Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005), who asserted that specific species prevalence data are limited due to the difficulties in identifying amphistome to species level. The pooled prevalence in domestic ruminants measured by coprology was lower than the postmortem. This may be attributed to low sensitivity of coprological method as it only detects the presence of adult rumen fluke infection and infection with immature stages may have gone undetected (Malrait et al., Reference Malrait, Verschave, Skuce, Van Loo, Vercruysse and Charlier2015; Sargison et al., Reference Sargison, Francis, Davison, Barend, Handel and Mazeri2016). According to Horak (Reference Horak1971), one drawback of coprology diagnostic method is the high probability of finding few to no eggs in acute infections as they are usually associated with massive infection with immature flukes. Furthermore, Sargison et al. (Reference Sargison, Francis, Davison, Barend, Handel and Mazeri2016) also highlighted that although coprological technique/faecal egg count is the only practical test that is validated for diagnosis and identification of rumen fluke infections in live animals; it also has the potential to underestimate infections as it can only diagnose patent infections. Reviewed studies also showed a wider use of sedimentation technique to detect eggs in faecal samples. Although this technique has showed a huge success in large populations (Ibarra et al., Reference Ibarra, Montenegro, Vera, Boulard, Quiroz, Flores and Ochoa1998; Munguía-Xóchihua et al., Reference Munguía-Xóchihua, Ibarra-Velarde, Ducoing-Watty, Montenegro-Cristino and Quiroz-Romero2007), its lack of sensitivity in detecting low-intensity infections (Bosco et al., Reference Bosco, Ciuca, Maurelli, Vitiello, Cringoli, Prada and Rinaldi2023) often leads to misrepresenting the true prevalence. Bosco et al. (Reference Bosco, Ciuca, Maurelli, Vitiello, Cringoli, Prada and Rinaldi2023) proved that other techniques such as Mini-Flotac and Fluke Finder techniques should be used as they have shown to be more efficient, and sensitive compared to sedimentation.

For postmortem cases, histology and flattening were used to identify between species. However, these techniques need an expert skilled in identification of amphistome species identification of which they are scarce in the region (Lotfy et al., Reference Lotfy, Brant, Ashmawy, Devkota, Mkoji and Loker2010). Furthermore, determining the amphitsome species based only on morphology is difficult since the disease-causing flukes are mostly sexually immature (Chaoudhary et al., Reference Chaoudhary, Hasnani, Khyalia, Pandey, Chauhan, Pandya and Patel2015; Ikeuchi et al., Reference Ikeuchi, Kondoh, Halajian and Ichikawa-Seki2022). Thus, several researchers relied on the biased procedure of identifying a few adult worms that may be present in the rumen of animals (Horak, Reference Horak1971). Many errors could have been made in specific identification because the histology and flattening methods used are unreliable, according to Pfukenyi and Mukaratirwa et al. (Reference Pfukenyi and Mukaratirwa2018). Furthermore, Mitchell et al. (Reference Mitchell, Zadoks and Skuce2021) also highlighted that the morphologically plasticity of amphistomes result in numerous cases of misdiagnosis. As a result, polymerase chain reaction-based techniques providing rDNA Internal Transcriber Spacer (ITS-2) sequences have proven to be reliable tools to identify amphistome species and to determine their phylogenetic relationships (Itagaki et al., Reference Itagaki, Tsumagari, Tsutsumi and Chinone2003; Rinaldi et al., Reference Rinaldi, Perugini, Capuano, Fenizia, Musella, Veneziano and Cringoli2005).

Limitations of the study

Publication bias raised concerns regarding the reliability of the results and increases the risk of making poorly informed decisions about amphistomosis, even when the effect size remains unchanged when bias is considered. Therefore, it is critical that veterinary or departments monthly or yearly abattoir reports on amphistomosis in domestic ruminants are readily and easily accessible, and these should be incorporated in future research to improve our understanding of prevalence of amphistome in domestic ruminants.

Conclusion

The outcomes of this review and meta-analysis revealed that most sub-Saharan African countries have little to no information on the prevalence of amphistome in cattle, sheep, and goats, despite it being a substantial limiting factor in cattle and small ruminant production. Furthermore, the available data on amphistome infections in the region are often scattered across different studies and locations, making it challenging to obtain a clear picture of the overall status. This study highlighted that cattle were the most susceptible domestic ruminant. However, more epidemiological research on amphistomes is required in all sub-Saharan African countries to determine the true prevalence estimate in the region. The widely used coproscopic examination cannot be used for the early diagnosis of clinical amphistomosis which is vital for prompt treatment before considerable damages and economic losses are incurred. Developing diagnostic techniques capable of detecting prepatent infections in the final host will allow for a more accurate portrayal of the total prevalence of amphistome in African domestic ruminants. The findings of such research would provide vital information to aid in disease prevention, optimizing production efficiency to satisfy Africa’s rising population. Furthermore, additional research is needed to establish the economic significance of amphistomosis in domestic ruminants, as well as the efficacy of various anthelmintics. The high variation observed across and within subgroups emphasizes the need of using precise sample criteria to adequately integrate and quantify epidemiological data.

Supplementary material

The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X24000725.

Declaration

The authors declare that there is no conflict of interest.

Author contribution

I.N. conceptualized the study under the guidance of S.M. and M.P.M. I.N. and P.I.N. developed the concept note, conducted the search, selected studies, and wrote the first draft of the manuscript under M.P.M.’s guidance. All authors contributed to the article, agreed on the final draft, and approved the submitted version.

Funding

No financial assistance was received for this study.

References

Abass, CG, Abdoulmoumini, M, Koumai, P, Hervé, AS, Marie, W and Mbida, M (2020) Hepatic and rumenal worms infestations of cattle in Vina Division (Adamawa–Cameroon). International Journal of Forest, Animal and Fisheries Research 4, 14–28.CrossRefGoogle Scholar
Abebe, F, Behablom, M and Berhanu, M (2011) Major trematode infections of cattle slaughtered at Jimma Municipality Abattoir and the occurrence of the intermediate hosts in selected water bodies of the zone. Journal of Animal and Veterinary Advances 10, 1592–1597.Google Scholar
Abera, D, Kebede, Y, Haile, N and Bekuma, F (2023) Incidence of gastrointestinal helminth parasite of cattle in Ambo District, West Shoa, Ethiopia. International Journal of Advanced Multidisciplinary Research & Studies 3, 948–953.Google Scholar
Adedipe, OD, Uwalaka, EC, Akinseye, VO, Adediran, OA and Cadmus, SIB (2014) Gastrointestinal helminths in slaughtered cattle in Ibadan, South‐Western Nigeria. Journal of Veterinary Medicine 2014, 923561.CrossRefGoogle ScholarPubMed
Anuracpreeda, P, Wanichanon, C and Sobhon, (2008). Paramphistomum cervi: antigenic profile of adults as recognized by infected cattle sera. Experimental Parasitology 118, 203–207.CrossRefGoogle ScholarPubMed
Aragaw, K and Tilahun, H (2019) Coprological study of trematode infections and associated host risk factors in cattle during the dry season in and around Bahir Dar, northwest Ethiopia. Veterinary and Animal Science 7, 100041.CrossRefGoogle ScholarPubMed
Arowoloa, OB, Mohammeda, BR and Opara, МN (2020) Prevalence of Paramphistomum species in cattle slaughtered at Gwagwalada abattoir, Abuja, Nigeria. Parasitology 54, 514–521.Google Scholar
Attindéhou, S, Salifou, S, Daga, DF, Gbangboché, AB, Gbati, OB and Pangui, LJ (2012) Stomach fluke infection in sahelian and West African dwarf small ruminants in Benin. International Multidisciplinary Research Journal 2(8), 1–3.Google Scholar
Ayalew, G, Tilahun, A, Aylate, A, Teshale, A and Getachew, A (2016) A study on prevalence of Paramphistomum in cattle slaughtered in Gondar Elfora Abattoir, Ethiopia. Journal of Veterinary Medicine and Animal Health 8, 107–111.Google Scholar
Barendregt, JJ, Doi, SA, Lee, YY, Norman, RE and Vos, T (2013) Meta-analysis of prevalence. Journal of Epidemiology and Community Health 67(11), 974–978.CrossRefGoogle ScholarPubMed
Bedasa, C, Getachow, M, Duguma, A and Abera, S (2016) Status of helminthes parasites of cattle in dairy farms of Holleta agricultural research center, central Ethiopia. Journal of Veterinary Science &Technology 7, 2.Google Scholar
Beyene, B (2016) Study on gastrointestinal parasite of cattle at Horoguduru Animal Production and Research Center of Wollega University, Oromia, Ethiopia. Science, Technology and Arts Research Journal 5, 46–50.CrossRefGoogle Scholar
Biu, AA and Oluwafunmilayo, A (2004) Identification of some paramphistomes infecting sheep in Maiduguri, Nigeria. Young 9, 22.Google Scholar
Bosco, A, Ciuca, L, Maurelli, MP, Vitiello, P, Cringoli, G, Prada, JM and Rinaldi, L (2023) Comparison of Mini-FLOTAC, Flukefinder® and sedimentation techniques for detection and quantification of Fasciola hepatica and Calicophoron daubneyi eggs using spiked and naturally infected bovine faecal samples. Parasites & Vectors 16, 260.CrossRefGoogle ScholarPubMed
Bunza, MDA, Ahmad, A and Fana, SA (2008) Prevalence and of paramphistomiasis in ruminants slaughtered at Sokoto Central Abattoir, Sokoto. Nigerian Journal of Basic and Applied Sciences 16, 287–292.Google Scholar
Chaoudhary, V, Hasnani, JJ, Khyalia, MK, Pandey, S, Chauhan, VD, Pandya, SS and Patel, PV (2015) Morphological and histological identification of Paramphistomum cervi (Trematoda: Paramiphistoma) in the rumen of infected sheep. Veterinary World 8, 125.CrossRefGoogle ScholarPubMed
Chingwena, G, Mukaratirwa, S, Kristensen, TK and Chimbari, M (2002) Larval trematode infections in freshwater snails from the highveld and lowveld areas of Zimbabwe. Journal of Helminthology 76, 283–293.CrossRefGoogle ScholarPubMed
Chongmobmi, M and Panda, SM (2018) Bovine gastrointestinal trematodosis in Nigeria: a review. IOSR Journal of Agriculture and Veterinary Science 11, 8–19.Google Scholar
Dabasa, G, Shanko, T, Zewdei, W, Jilo, K, Gurmesa, G and Abdela, N (2017) Prevalence of small ruminant gastrointestinal parasites infections and associated risk factors in selected districts of Bale zone, south-eastern Ethiopia. Journal of Parasitology and Vector Biology 9, 81–88.Google Scholar
Daniel, A, Deneke, Y and Ibrahim, N (2014) Gastrointestinal parasites in sheep in Gemechis and Boke Districts, West Harerghe Zone, Ethiopia. Acta Parasitologica Globalis 5, 120–124.Google Scholar
Degefu, H, Abera, C, Yohannes, M and Tolosa, T (2011) Gastrointestinal helminth infections in small-scale dairy cattle farms of Jimma town, Ethiopia. Ethiopian Journal of Applied Science and Technology 2, 31–37.Google Scholar
Dogo, AG, Karaye, GP, Patrobas, MG, Galadima, M and Gosomji, IJ (2017) Prevalence of gastrointestinal parasites and their impact in domestic animals in Vom, Nigeria. Saudi Journal of Medical and Pharmaceutical Sciences 3, 211–216.Google Scholar
Dube, S, Masanganise, KE and Dube, C (2010) Studies on paramphistomes infecting goats and sheep from Gwanda District in Zimbabwe. Zimbabwe Journal of Science & Technology 5, 55–64.Google Scholar
Dube, S, Siwela, AH, Masanganise, KE and Dube, C (2002) Prevalence of paramphistomes in Mashonaland West, Central and East, and Midlands Provinces, Zimbabwe. Acta Zoologica Taiwanica 13, 39–52.Google Scholar
Dube, S and Aisien, MSO (2005) Descriptive studies of the genus Paramphistomum Fischoeder, 1901 in some Nigerian Cattle. Discovery and Innovation 17, 186–192.Google Scholar
Dube, S and Aisien, MSO (2010) Descriptive studies on Paramphistomes of small domestic ruminants in Southern Nigeria. Zimbabwe Journal of Science and Technology 5, 12–21.Google Scholar
Eduardo, SL (1987) Zoogeographical affinities of paramphistomids of ruminants. Transactions of the National Academy of Science & Technology (Phils.) 9, 229–242.Google Scholar
Elele, K, Owhoeli, O and Gboeloh, L (2013) Prevalence of species of helminth parasites in cattle slaughtered in selected abattoirs in Port Harcourt, south-south, Nigeria. International Journal of Research in Medical Sciences 1, 10–7.Google Scholar
Elele, K, Owhoeli, O and Gboeloh, LB (2021) Research article prevalence of gastrointestinal helminths in exotic and indigenous goats slaughtered in selected abattoirs in Port Harcourt, South-South, Nigeria. Chinese Journal of Biology 1(2014), 435913.Google Scholar
Elelu, N, Ambali, A, Coles, GC and Eisler, MC (2016) Cross-sectional study of Fasciola gigantica and other trematode infections of cattle in Edu Local Government Area, Kwara State, north-central Nigeria. Parasites & Vectors 9, 1–11.CrossRefGoogle ScholarPubMed
Elemo, KK and Geresu, MA (2017) Prevalence and risk factors of gastrointestinal parasites of small ruminants in Sinana and Dinsho districts of Bale zone, south-eastern Ethiopia. European Journal of Biological Sciences 9, 1–8.Google Scholar
Erdaw, MM (2023) Contribution, prospects and trends of livestock production in sub-Saharan Africa: a review. International Journal of Agricultural Sustainability 21, 2247776.CrossRefGoogle Scholar
FAO (2017) The future of food and agriculture. Food Agric. Organ. United Nations 1–52.Google Scholar
Ferede, Y, Mola, L and Asmare, Z (2018) Prevalence and species composition of major internal and external parasites of calves in selected dairy farms of Bahir Dar milk-shade. Ethiopian Veterinary Journal 22, 128–142.CrossRefGoogle Scholar
Getahun, TK, Siyoum, T, Yohannes, A and Eshete, M (2017) Prevalence of gastrointestinal parasites in dry season on dairy cattle at Holeta Agricultural Research Center Dairy Farm, Ethiopia. Journal of Veterinary Medicine and Animal Health 9, 356–360.Google Scholar
Ghatani, S, Shylla, JA, Tandon, V, Chatterjee, A and Roy, B (2012) Molecular characterization of pouched amphistome parasites (Trematoda: Gastrothylacidae) using ribosomal ITS2 sequence and secondary structures. Journal of Helminthology 86, 117–124.CrossRefGoogle ScholarPubMed
Gonzalez-Warleta, M, Lladosa, S, Castro-Hermida, JA, Martínez-Ibeas, AM, Conesa, D, Munoz, F, López-Quílez, A, Manga-González, Y and Mezo, M (2013) Bovine paramphistomosis in Galicia (Spain): prevalence, intensity, aetiology and geospatial distribution of the infection. Veterinary Parasitology 191, 252–263. https://doi.org/10.1016/j.vetpar.2012.09.006.CrossRefGoogle ScholarPubMed
Guyatt, GH, Oxman, AD, Vist, GE, Kunz, R, Falck-Ytter, Y, Alonso-Coello, P and Schünemann, HJ (2008). GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. British Medical Journal 336, 924–926.CrossRefGoogle ScholarPubMed
Hajipour, N, Mirshekar, F, Hajibemani, A and Ghorani, M (2021) Prevalence and risk factors associated with amphistome parasites in cattle in Iran. Veterinary Medicine & Science 7, 105–111.CrossRefGoogle ScholarPubMed
Hayider, N, Mekuria, S and Mekibib, B (2018) Major trematodes of cattle slaughtered at Hirna municipal Abattoir: prevalence, associated risk factors and test agreement of sedimentation technique in Ethiopia. Journal of Parasitology & Vector Biology 10, 51–57.Google Scholar
Higgins, JP, Thompson, SG, Deeks, JJ and Altman, DG (2003) Measuring inconsistency in meta-analyses. British Medical Journal 327, 557–60.CrossRefGoogle ScholarPubMed
Horak, IG (1971) Paramphistomiasis of domestic ruminants. Advances in Parasitology 9, 33–72. https://doi.org/10.1016/s0065-308x(08)60159-1.CrossRefGoogle ScholarPubMed
Hotessa, AS and Kanko, DK (2020) Review on paramphistomosis. Advances in Biological Research 14, 184–192.Google Scholar
Ibarra, F, Montenegro, N, Vera, Y, Boulard, C, Quiroz, H, Flores, J and Ochoa, P (1998) Comparison of three ELISA tests for seroepidemiology of bovine fascioliosis. Veterinary Parasitology 77, 229–36.Google ScholarPubMed
Ibrahim, N, Tefera, M, Bekele, M and Alemu, S (2014) Prevalence of gastrointestinal parasites of small ruminants in and around Jimma Town Western Ethiopia. Acta Parasitologica Globalis 5, 12–18.Google Scholar
Ibrahim, S, Auta, T and Orpin, JB (2022) Occurrence of gastrointestinal parasites in cattle slaughtered at Central Abattoir in Katsina Metropolis, Katsina State, Nigeria. Research Journal of Veterinary Sciences 15, 65–71.CrossRefGoogle Scholar
Ikeuchi, A, Kondoh, D, Halajian, A and Ichikawa-Seki, M (2022) Morphological and molecular characterization of Calicophoron raja (N¨asmark, 1937) collected from wild Bovidae in South Africa. International Journal for Parasitology: Parasites & Wildlife 19, 38–43.Google ScholarPubMed
Itagaki, T, Tsumagari, N, Tsutsumi, K and Chinone, S (2003) Discrimination of three amphistome species by PCR-RFLP based on rDNA ITS2 markers. Journal of Veterinary Medical Science 65, 931–933.CrossRefGoogle ScholarPubMed
Kalule, F, Vudriko, P, Nanteza, A, Ekiri, AB, Alafiatayo, R, Betts, J, Betson, M, Mijten, E, Varga, G and Cook, A (2023) Prevalence of gastrointestinal parasites and molecular identification of beta-tubulin mutations associated with benzimidazole resistance in Haemonchus contortus in goats from selected districts of Uganda. Veterinary Parasitology: Regional Studies and Reports 42, 100889.Google ScholarPubMed
Kanyari, PWN, Kagira, JM and Mhoma, JRL (2009) Prevalence and intensity of endoparasites in small ruminants kept by farmers in Kisumu Municipality, Kenya. Livestock Research & Rural Development 21, 11.Google Scholar
Kanyari, PWN, Kagira, JM and Mhoma, JRL (2010) Prevalence and intensity of endoparasites in cattle within urban and peri-urban areas of Lake Victoria Basin, Kenya with special reference to zoonotic potential. Scientia Parasitologica 11, 171–178.Google Scholar
Kebede, IA, Beriso, TE, Mengistu, TS and Gebremeskel, HF (2023) Study on cattle trematodiasis and related risk factors in Damot Sore District, Wolaita Zone, Southern Ethiopia. Journal of Parasitology Research 2023(1), 6687665.CrossRefGoogle Scholar
Kemal, J and Terefe, Y (2013) Prevalence of gastrointestinal parasitism of cattle in Gedebano Gutazer Wolene district, Ethiopia. Journal of Veterinary Medicine & Animal Health 5, 365–370.Google Scholar
Keno, L, Abera, B, Lemma, D, Eticha, E and Assefa, G (2017) Study on the prevalence of endoparasites in small holder dairy rarm in and around Harar Town, Oromia Regional State, Eastern Ethiopia. Journal of Veterinary Science & Technology 8, 2.CrossRefGoogle Scholar
Keyyu, JD, Kassuku, AA, Msalilwa, LP, Monrad, J and Kyvsgaard, NC (2006) Cross-sectional prevalence of helminth infections in cattle on traditional, small-scale and large-scale dairy farms in Iringa District, Tanzania. Veterinary Research Communications 30, 45–55.CrossRefGoogle ScholarPubMed
Keyyu, JD, Monrad, J, Kyvsgaard, NC and Kassuku, AA (2005) Epidemiology of Fasciola gigantica and amphistomes in cattle on traditional, small-scale dairy and large-scale dairy farms in southern highlands of Kenya. Tropical Animal Health & Production 37, 303–314.CrossRefGoogle Scholar
Kifleyohannes, T, Kebede, E, Hagos, Y, Weldu, K and Michael, MG (2015) Prevalence of paramphistomosis in ruminants in Ashenge, Tigray Ethiopia. Acta Parasitologica Globalis 6, 83–86.Google Scholar
Lotfy, WM, Brant, SV, Ashmawy, KI, Devkota, R, Mkoji, GM and Loker, ES (2010) A molecular approach for identification of paramphistomes from Africa and Asia. Veterinary Parasitology 174, 234–240.CrossRefGoogle ScholarPubMed
Luka, J, Ajanusi, OJ, Chiezey, NP, Bale, JO, Tanko, JT and Kamani, J (2018) Gastrointestinal parasites of bile and faeces of slaughtered cattle and sheep from Maiduguri Municipal abattoir, North Eastern Nigeria. Nigerian Veterinary Journal 39, 368–377.CrossRefGoogle Scholar
Malrait, K, Verschave, S, Skuce, P, Van Loo, H, Vercruysse, J and Charlier, J (2015) Novel insights into the pathogenic importance, diagnosis and treatment of the rumen fluke (Calicophoron daubneyi) in cattle. Veterinary Parasitology 207, 134–139.CrossRefGoogle ScholarPubMed
Mariam, T, Mohamed, A, Ibrahim, N and Baye, D (2014) Prevalence of fasciolosis and paramphistomosis in dairy farm and household in Hawassa town. European Journal of Biological Sciences 6, 54–58.Google Scholar
Mavenyengwa, M, Mukaratirwa, S, Obwolo, M and Monrad, J (2005) A macro-and light microscopical study of the pathology of Calicophoron microbothrium infection in experimentally infected cattle. Onderstepoort Journal of Veterinary Research 72, 321–332.CrossRefGoogle ScholarPubMed
Meguini, MN, Righi, S, Boucheikhchoukh, M, Sedraoui, S and Benakhla, A (2021) Investigation of flukes (Fasciola hepatica and Paramphistomum sp.) parasites of cattle in north-eastern Algeria. Annals of Parasitology 67(3).Google ScholarPubMed
Mia, MM, Hasan, M and Chowdhury, MR (2021) A systematic review and meta-analysis on prevalence and epidemiological risk factors of zoonotic Fascioliasis infection among the ruminants in Bangladesh. Heliyon 7.CrossRefGoogle ScholarPubMed
Micheal, AO, Folakemi, A, Joy, OO, Olajumoke, AE, Ademola, AD and Adenike, AK (2020) Identification and prevalence of intestinal parasites from slaughtered cows in Saki and Ago-Are Abattoirs. World Journal of Advanced Research and Reviews 6, 83–89.CrossRefGoogle Scholar
Mitchell, G, Zadoks, RN and Skuce, PJ (2021) A universal approach to molecular identification of rumen fluke species across hosts, continents, and sample types. Frontiers in Veterinary Science 7, 605259.CrossRefGoogle ScholarPubMed
Mohammed, AS, Animut, G, Urge, M and Assefa, G (2020) Grazing behavior, dietary value and performance of sheep, goats, cattle and camels co-grazing range with mixed species of grazing and browsing plants. Veterinary & Animal Science 10, 100154.CrossRefGoogle ScholarPubMed
Mpofu, BI, Slayi, M, Mutero, G, Mlahlwa, S and Jaja, IF (2023) Assessing body condition scores, weight gain dynamics, and fecal egg counts in feedlot and non-feedlot cattle within high throughput abattoirs of the Eastern Cape Province. Frontiers in Animal Science 4, 1302320.CrossRefGoogle Scholar
Munguía-Xóchihua, JA, Ibarra-Velarde, F and Ducoing-Watty, A, Montenegro-Cristino, N and Quiroz-Romero, H (2007). Prevalence of Fasciola hepatica (ELISA and fecal analysis) in ruminants from a semi-desert area in the northwest of Mexico. Parasitology Research 101, 127–30.CrossRefGoogle ScholarPubMed
Njoku-Tony, RF and Nwoko, BEB (2011) Prevalence of paramphistomiasis among sheep slaughtered in some selected abattoirs in Imo State, Nigeria. Science World Journal 3(1), 82–86.Google Scholar
Nwigwe, JO, Njoku, OO, Odikamnoro, OO and Cosmas, UA (2013) Comparative study of intestinal helminths and protozoa of cattle and goats in Abakaliki metropolis of Ebonyi State, Nigeria. Advances in Applied Science Research 4, 223–227.Google Scholar
Nyagura, I, Malatji, MP and Mukaratirwa, S (2024) The prevalence and infection rates of amphistome species in intermediate snail hosts: a systematic review and meta-analysis. Frontiers in Veterinary Science 11, 1418979.CrossRefGoogle ScholarPubMed
Nzalawahe, J, Kassuku, AA, Stothard, RJ, Coles, CG and Eisler, MC (2014) Trematodes infection in cattle in Arumeru District, Tanzania are associated with irrigation. Parasites & Vectors 7, 107.CrossRefGoogle ScholarPubMed
Nzalawahe, J, Kassuku, AA, Stothard, RJ, Coles, CG and Eisler, MC (2015) Associations between trematode infections in cattle and freshwater snails in highland and lowland areas of Iringa Rural District, Tanzania. Parasitology 142, 1–10.CrossRefGoogle ScholarPubMed
Odeniran, PO, Jegede, HO and Adewoga, TO (2016) Prevalence and risk perception of adult-stage parasites in slaughtered food animals (cattle, sheep and goat) among local meat personnel in Ipata abattoir, Ilorin, Nigeria. Veterinary Medicine and Animal Science 4, 1.CrossRefGoogle Scholar
Ola-Fadunsin, SD, Ganiyu, IA, Rabiu, M, Hussain, K, Sanda, IM, Baba, AY, Furo, NA and Balogun, RB (2020) Helminth infections of great concern among cattle in Nigeria: insight to its prevalence, species diversity, patterns of infections and risk factors. Veterinary World 13, 338.CrossRefGoogle ScholarPubMed
Opara, KN, Chikezie, FM, Udoidung, NI, Yaro, CA, Onwumerobi, KM and Afia, UU (2017) Prevalence and intensity of paramphistomatidae fluke species in ruminants slaughtered in Uyo Local Government Area, Akwa Ibom State, Nigeria. World Journal of Applied Science and Technology 14, 789–81.Google Scholar
O’Shaughnessy, J, Garcia-Campos, A, McAloon, CG, Fagan, S, de Waal, T, McElroy, M, Casey, M, Good, B, Mulcahy, G, Fagan, J and Murphy, D (2018) Epidemiological investigation of a severe rumen fluke outbreak on an Irish dairy farm. Parasitology 145, 948–952.CrossRefGoogle Scholar
Oyewusi, IK, Takeet, MI, Olugbogi, EI, Takeet, OVA and Talabi, AO (2017) Prevalence of gastrointestinal parasites of rams brought into Abeokuta small ruminants markets in preparation for a festive season. Nigerian Journal of Animal Science 19, 101–107.Google Scholar
Paguem, A, Kamtsap, P, Manchang, TK, Yembo, J, Achukwi, MD, Streit, A and Renz, A (2023) Species identity and phylogeny of Paramphistomoidea Fischoeder, 1901 occurring in cattle and sheep in North Cameroon. Veterinary Parasitology: Regional Studies and Reports 45, 100922.Google ScholarPubMed
Paul, A, Osemeke, H, Olaolu, S, Gulek, J, Takyun, A, Yakubu, R and Weka, R (2021) Gastrointestinal parasites infection among sheep in Bokkos local government area of Plateau state, Nigeria. Nigerian Journal of Animal Science 23, 153–160.Google Scholar
Pfukenyi, DM and Mukaratirwa, S (2018) Amphistome infections in domestic and wild ruminants in East and Southern Africa: A review. Onderstepoort Journal of Veterinary Research 85, 1–3.CrossRefGoogle Scholar
Pfukenyi, DM, Mukaratirwa, S, Willingham, AL and Monrad, J (2005) Epidemiological studies of amphistome infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research 72, 67–86.CrossRefGoogle ScholarPubMed
Phiri, AM, Chota, A and Phiri, IK (2007) Seasonal pattern of bovine amphistomosis in traditionally reared cattle in the Kafue and Zambezi catchment areas of Zambia. Tropical Animal Health & Production 39, 97–102.CrossRefGoogle ScholarPubMed
Phiri, AM, Chota, A, Muma, JB, Munyeme, M and Sikasunge, CS (2011) Helminth parasites of the Kafue lechwe antelope (Kobus leche kafuensis): a potential source of infection to domestic animals in the Kafue wetlands of Zambia. Journal of Helminthology 85, 20–27.CrossRefGoogle ScholarPubMed
Phiri, AM, Phiri, IK and Monrad, J (2006) Prevalence of amphistomiasis and its association with Fasciola gigantica infections in Zambian cattle from communal grazing areas. Journal of Helminthology 80, 65–68.CrossRefGoogle ScholarPubMed
Phiri, AM, Phiri, IK, Chota, A and Monrad, J (2007b) Trematode infections in freshwater snails and cattle from the Kafue wetlands of Zambia during a period of highest cattle-water contact. Journal of Helminthology 81, 85–92.CrossRefGoogle ScholarPubMed
Rinaldi, L, Perugini, AG, Capuano, F, Fenizia, D, Musella, V, Veneziano, V and Cringoli, G (2005) Characterization of the second internal transcribed spacer of ribosomal DNA of Calicophoron daubneyi from various hosts and locations in southern Italy. Veterinary Parasitology 131, 247–253.CrossRefGoogle ScholarPubMed
Rolfe, PF, Boray, JC, Nichols, P and Collins, GH (1991) Epidemiology of paramphistomosis in cattle. International Journal for Parasitology 21, 813–819.CrossRefGoogle ScholarPubMed
Sargison, N, Francis, E, Davison, C, Barend, M, Handel, I and Mazeri, S (2016) Observations on the biology, epidemiology and economic relevance of rumen flukes (Paramphistomidae) in cattle kept in a temperate environment. Veterinary Parasitology 219, 7–16.CrossRefGoogle Scholar
Sebro, E, Kebamo, M and Abebe, A (2022) Prevalence of gastrointestinal parasites of sheep and goats in an-Lemo, Hadiya zone southern Ethiopia. Indian Journal of Science and Technology 15, 1084–1090.CrossRefGoogle Scholar
Sibula, MS, Nyagura, I, Malatji, MP and Mukaratirwa, S (2024) Prevalence and geographical distribution of amphistomes of African wild ruminants, a scoping review. International Journal for Parasitology: Parasites and Wildlife 23, 100906Google ScholarPubMed
Solomon, L, Ibrahim, N and Temesgen, M (2016) Prevalence of Gastrointestinal Helminthes Parasite of Cattle in Ejere District, West Shoa, Oromiya Region, Ethiopia. World Journal of Agricultural Sciences 12, 364–371.Google Scholar
Squire, SA, Robertson, ID, Yang, R, Ayi, I and Ryan, U (2019) Prevalence and risk factors associated with gastrointestinal parasites in ruminant livestock in the Coastal Savannah zone of Ghana. Acta Tropica 199, 105126.CrossRefGoogle ScholarPubMed
Squire, SA, Yang, R, Robertson, I, Ayi, I, Squire, DS and Ryan, U (2018) Gastrointestinal helminths in farmers and their ruminant livestock from the Coastal Savannah zone of Ghana. Parasitology research 117, 3183–3194.CrossRefGoogle ScholarPubMed
Tasse, I (2024) Prevalence of Paramphistomum and its associated factors in cattle slaughtered at Boko Slaughterhouse, Fedis District, Eastern Hararghe Zone, Ethiopia. Iranian Journal of Veterinary Medicine 18, 435–40.CrossRefGoogle Scholar
Tesema, G, Tesfaye, S and Bekele, D (2023) Helminth parasites prevalence and distribution among Sheep in Gudaya Bila District, East Wallaga, Ethiopia. Journal of Parasite Research 1, 23–38.Google Scholar
Tookhy, NA, Mahiza, MIN, Mansor, R, Yasmin, AR, Ahmad, NI, Hamzah, NH and Idris, LH (2022) Rumen fluke in cattle and buffaloes in Asia: a review. Pertanika Journal of Tropical Agricultural Science 45, 781–803.CrossRefGoogle Scholar
Tsotetsi, AM, Njiro, S, Katsande, TC, Moyo, G, Baloyi, F and Mpofu, J (2013) Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in Gauteng Province, South Africa. Tropical Animal Health and Production 45, 751–761.CrossRefGoogle ScholarPubMed
Tulu, D and Lelisa, K (2016) A study on major gastro-intestinal Helminths parasites of cattle in Tulo District, West Hararghe Zone, South-Eastern Ethiopia. Austin Journal of Veterinary Science & Animal Husbandry 3, 3–6.Google Scholar
Tumusiime, M, Manishimwe, JC and Ntampaka, P (2023) Prevalence of bovine Trematodiases and associated risk factors in Nyagatare District, Rwanda. Veterinary Medicine: Research and Reports 14, 221–231.Google Scholar
Turuna, G and Adugna, B (2019) Prevalence of major bovine trematodes (Fasciola and Paramphistomum) in cattle slaughtered at Nekemte municipal abattoir, East Wollega, Oromia Regional State, Ethiopia. Prevalence 9, 1–5.Google Scholar
Uwalaka, EC, Akpabio, U and Adediran, OA (2019) Prevalence of Fascioliasis and Paramphistomiasis in cattle in Umuahia, Abia State, Nigeria. Young 112, 74–11.Google Scholar
Yabe, J, Phiri, IK, Phiri, AM, Chembensofu, M, Dorny, P. and Vercruysse, J (2008) Concurrent infections of Fasciola, Schistosoma and Amphistomum spp. in cattle from Kafue and Zambezi river basins of Zambia. Journal of Helminthology 82, 373–376.CrossRefGoogle ScholarPubMed
Yasin, H, Tsegay, T and Niraj, K (2017) Prevalence of bovine trematodes and associated risk factors at Abergelle Export Abattoir, Mekelle, Tigray, Ethiopia. Ethiopian Journal of Veterinary Science Animal Production 1, 25–34.Google Scholar
Yohanna, JA, Dung, OK, Adejoh, VA and Pam, DD (2019) Prevalence of helminth parasites of ruminants in Abattoir Market Jos, Jos South Local Government Area, Plateau State, Nigeria. International Journal of Biomedical and Health Sciences 15(2), 51–57.Google Scholar
Yohannes, M, Birasa, D, Damena, D, Tasew, S and Degefu, H (2013) Bovine trypanosomosis and gastrointestinal helminthosis in settlement villages of Bedele district, South-western Ethiopia. Ethiopian Veterinary Journal 17(1), 41–45.CrossRefGoogle Scholar
Yusuf, K, Jima, CB and Aseffa, MS (2024) Prevalence of gastrointestinal tract parasites in small ruminants in and around Jaja Town, Melka Belo Woreda of East Haraghe Zone, Oromia, Ethiopia. Journal of Research in Veterinary Sciences 2, 51–66.Google Scholar
Zewde, A, Bayu, Y and Wondimu, A (2019) Prevalence of bovine fasciolosis and its economic loss due to liver condemnation at Wolaita Sodo Municipal Abattair, Ethiopia. Veterinary Medicine International 2019(1), 9572373.CrossRefGoogle ScholarPubMed
Zvinorova, PI, Halimani, TE, Muchadeyi, FC, Matika, O, Riggio, V and Dzama, K (2016) Prevalence and risk factors of gastrointestinal parasitic infections in goats in low-input low-output farming systems in Zimbabwe. Small Ruminant Research 143, 75–83.CrossRefGoogle ScholarPubMed
Figure 0

Figure 1. PRISMA flow diagram.

Figure 1

Table 1. Pooled prevalence of amphistome infections in domestic ruminants in sub-Saharan Africa based on different risk factors

Figure 2

Figure 2. Forest plot for the prevalence of amphistome infections in domestic ruminants in sub-Saharan Africa.

Figure 3

Figure 3. Forest plots of prevalence of amphistome in domestic ruminants from (A) central Africa, (B) eastern Africa, (C) western Africa, and (D) southern Africa recorded from 2002 to 2023.

Figure 4

Figure 4. Forest plots of prevalence of amphistome in (A) cattle, (B) goat, (C) sheep from 2002 to 2023.

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