Skip to main content

A systematic review and meta-analysis on prevalence and distribution of Taenia and Echinococcus infections in Ethiopia

Abstract

Background

Tapeworm infections are among the tropical neglected parasitic diseases endemically occurring in Ethiopia. This systematic review and meta-analysis aims at estimating the pooled prevalence and distribution of Taenia and Echinococcus infections in humans and animals from reports from Ethiopia.

Methods

The systematic search was conducted in four bibliographic databases (PubMed, Google Scholar, Africa Journal Online and Science Direct). Additional data were retrieved from grey literature. Studies that met the inclusion criteria were considered for the systematic review and meta-analysis. The meta-analysis was conducted using MetaXL add-in for Microsoft Excel. Heterogeneity and inconsistency were evaluated using Cochran’s Q and I2 statistics, respectively.

Results

The study provides a country-based database of Taenia and Echinococcus infections consisting of 311 datasets from 201 publications which were mostly abattoir surveys; of these, 251 datasets were subjected to meta-analysis. Most of the studies were from Oromia (32.8%) followed by Amhara (22.9%) regional states. The pooled prevalence of cystic echinococcosis in intermediate and accidental hosts was calculated as 22% (95% CI 18–26%) and high study variability (Q = 24,420.65, I2 = 100%, P = 0.000). Moreover, a pooled prevalence of Echinococcus infections in final hosts was calculated as 33% (95% CI 20–48%) and low study variability (Q = 17.24, I2 = 65%, P = 0.001). Similarly, study subjects (human, cattle, sheep, goat and wolf) were infected by Taenia spp. with pooled prevalence of 3% (95% CI 2–4%) and moderate study variability (Q = 279.07, I2 = 89, P = 0.000). Meanwhile, the pooled prevalence of Taenia hydatigena, T. ovis and T. multiceps infections in intermediate hosts were calculated as 38%, 14% and 5%, respectively. The random effect meta-analysis of bovine cysticercosis showed a pooled prevalence of 7% (95% CI 5–9%) and high study variability was of (Q = 4458.76; I2 = 99%, P = 0.000). Significant differences in prevalence of Taenia and Echinococcus infections between study sites or different livestock origins have been reported.

Conclusion

The study evidenced a comprehensive dataset on the prevalence and distribution of Taenia and Echinococcus infections at different interfaces by regions and hosts and hence can aid in the design of more effective control strategies.

Graphical Abstract

Background

Parasitic diseases are highly prevalent in resource-poor Sub-Saharan African (SSA) countries and not only cause severe economic losses but also adversely affect public health [1]. Ethiopia is a SSA country with a population of 112,078,730 [2]. It is also host to about 60.39 million cattle, 31.3 million sheep, 32.74 million goats, 2.01 million horses, 8.85 million donkeys, 0.46 million mules and about 1.42 million camels [3]. The livestock production system in the country is characterized by mixed agriculture (animal and crop production) where there is high livestock-dog contact that can enhance the spread of parasites [4]. In Ethiopia about 80% of households have direct contact with domestic animals, creating an opportunity for zoonotic disease transmission [5,6,7]. Tapeworm infections are among the tropical neglected parasitic diseases endemic in Ethiopia [8, 9].

Tapeworms (or cestodes) characterized by body differentiation with scolex, neck and strobili are an important group of flatworms that parasitize humans, livestock and other susceptible animals [10, 11]. Taenia and Echinococcus species are tapeworms classified under phylum Platyhelminthes, subclass Eucestoda, order Cyclophyllidea and family Taeniidae. Regarding the general morphology of these parasites, the scolex possesses a rostellum usually armed with double rows of hooks and unpaired genitalia in each proglottid with irregularly alternating marginal genital pores. The eggs have a radially striated hardened ‘shell’ (embryophore) [12]. They have an indirect life cycle where adults occupy the small intestine of carnivores and humans while the larva stages occur in various organs of different mammals (including humans) that serve as intermediate hosts. The complex life cycle of tapeworms starts with a larval stage and usually involves several hosts [13]. The metacestode of Echinococcus shows a low degree of host specificity and has a much greater reproductive potential compared to the Taenia species [12].

Taenia solium, T. saginata and T. asiatica are cestodes that cause taeniasis in humans and cysticercosis in intermediate host animals (cows and pigs) [14]. Beef is a source of T. saginata infection, while pork and pig viscera are responsible for T. solium and T. asiatica infections [15]. T. asiatica is a sister species of T. saginata [16] that is commonly found in Asian countries [17, 18]. Taenia hydatigena (Cysticercus tenuicollis) and T. ovis (C. ovis) are species occurring mainly in small ruminants [19, 20]. The larval stage of Taenia multiceps (Coenurus/Cysticercus cerebralis) causes coenurosis (gid or sturdy) in small ruminants. The larvae develop in the brain and spinal cord of sheep, goats and sometimes cattle. The larval development in the brain has also been reported in humans and horses with cerebral manifestation [21, 22]. In general, the transmission of many important cestodes in livestock, such as Taenia spp. and Echinococcus spp., usually involves ‘predator-prey’ relationships between carnivores (final hosts) or omnivores and herbivores (intermediate hosts) and humans as accidental hosts in the case of echinococcosis [23].

Cystic echinococcosis (CE), the most common form of echinococcosis in human and domesticated animals, is caused by E. granulosus sensu lato. It is the least severe and most treatable form of echinococcosis since the larvae usually develop as isolated single cysts. In contrast, alveolar echinococcosis (AE), caused by E. multilocularis, is less common but more fatal and difficult to treat. The larvae of this organism grow as multiple budding cysts, and the involvement of wildlife in the lifecycle makes it difficult to prevent [24,25,26].

Metacestodes of both Taenia and Echinococcus are responsible for downgrading and lowering the quantity and quality of animal commodities [4, 19]. The economic burden of CE on the global livestock industry alone has been estimated to be > $2 billion per annum due to the condemnation of edible carcasses and offal such as liver, lung and heart [27]. In Ethiopia, significant degrees of financial losses were estimated at various levels in different locations. For example, reports estimate annual losses ranging from $2807.89 in Tigray [28] to $131,737.19 in Hawassa, South Nation and Nationality of People (SNNP) [29] based on abattoir surveys due to CE and bovine cysticercosis. Furthermore, average annual losses of 4,937,583.21 Ethiopian birr (ETB) or $225,036.97 due to taenicidal drugs for human treatment were estimated in Ethiopia [30].

Globally, echinococcosis presents a serious health concern especially in endemic countries with increasing infection rate resulting from an increase in the population of definitive hosts [31, 32]. The long-standing tradition of eating raw meat (beef) in Ethiopia has led to a craving for raw beef in most of the people. The close relationship among dogs, sheep and humans maintains the infection by completing the parasite's life cycle. Absence of rigorous meat inspection procedures, predominant home slaughtering of animals, the habit of feeding domesticated dogs with condemned offal and the subsequent contamination of pasture and grazing fields facilitate the maintenance of the life cycle and play an important role in the transmission of these zoonotic parasites.

Although several reports are available on various aspects of taeniasis and echinococcosis in Ethiopia, data on prevalence and distribution are affected by the type of study population, sample size, study design and other epidemiological factors such as host, pathogen and/or environmental factors. Thus, it is important to attain a comprehensive and larger scale overview and identify possible forecasters of the parasitic infection dynamics in the population of interest to provide national strategies for the control of taeniasis and echinococcosis. This systematic review and meta-analysis aims at estimating the pooled prevalence and distribution of taeniasis and echinococcosis in human and animal from reports from different parts of the country.

Materials and methods

Study area

Ethiopia is a rugged and landlocked country in the Horn of Africa, crossed by the Great Rift Valley, and borders Eritrea to the north, Djibouti and Somalia to the east, Sudan and South Sudan to the west, and Kenya to the south. The country covers an area of 1,126,829 km2 and is located between 9.1450°N and 40.4897°E. There are nine regions and two chartered cities [33]. In Africa, Ethiopia is the second most populated country after Nigeria and is known for its huge livestock population [2, 3].

Study protocol

A protocol addressing the review questions was developed by defining outcomes of interest and inclusion/exclusion criteria. Studies related to the occurrence, incidence and prevalence of taeniasis (due to Taenia solium, T. saginata, T. hydatigina, T. ovis and T. multiceps) and echinococcosis in humans and domesticated animals were analysed.

Inclusion criteria including manuscripts written in English which were either published or grey literature, time/period (1990–2020), geographical location (Ethiopia), study subject (human and/or domesticated animal such as cattle, sheep, goat, pig, camel and dog) and design (cross-sectional study, case report and short communication), dissertations and theses were also included.

Exclusion criteria included unrelated data, duplicated, wrong pathogen/agent of interest, case control study design, experimental study (development of diagnostics, drug efficacy, ethnobotanical study), KAP (knowledge, attitude and practice) questionnaire based study, book chapters, absence of original data, books, review articles without original data, editorials or letters to the editor without original data, all data before 1990, and unavailable full text or abstract only papers.

Article selection was carried out using a three-step process: first, duplicate articles were removed, then titles and/or abstracts were screened for relevance to the topic, and finally full texts were screened for eligibility. The quality standard of each manuscript was assessed independently by two authors. Disagreements or uncertainties were resolved through discussion with other reviewers. The study approach ensured compliance with methodological recommendations of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) guideline for review processes [34] and a PRISMA check list is provided as Additional file 1: Table S1.

Searching strategy

Searching was done systematically in four bibliographic databases including PubMed, Google Scholar, Africa Journal Online and Science Direct with search terms and key elements using Boolean operators: tapeworm OR taenia/taeniasis/taeniosis/cysticercosis/coenurosis* OR echinococc/hydatid cyst/hydatidosis* AND Ethiopia. The keywords/strings were rearranged to phrases close to outcome of interest. To increase the chance of recovering additional data, articles were retrieved from the reference section and citation lists of the full texts such as original research articles and reviews. Different combinations were tailored for each electronic database to narrow the amount of results retrieved but at the same time maximizing the number of relevant studies. The last search was conducted on June 30, 2020.

Data extraction

Data were extracted by two independent researchers and any disagreements were resolved by consensus among the researchers using the standardized extraction forms to guarantee consistency and accuracy. Data were extracted from eligible studies using standardized Microsoft Excel tables (Microsoft Office 2010). The data extracted included paper identification, brief study description (study area, year of study, species, sex, age), study design, diagnostic method (parasitological, ultrasound, surgery, molecular identification and serology), total sample size, number of infected/positive, prevalence and respective 95% confidence interval, and parasitic category. All patient medical data analysed in this study were anonymised and extracted from publications in which they were reported in an aggregated form as case or population counts. Approval from an ethical committee or institutional review board was not necessary for this study.

Statistical analysis

The extracted data on Excel sheets were analysed qualitatively and quantitatively. The prevalence data were analysed using the total sample size and number of positives. Studies with known sample size and number of positive samples were minimum requirements for further meta-analysis. However, data sources from retrospective studies were not included in the meta-analysis because such data might not indicate the true nature (exact value) of the infections in the study area.

The meta-analysis procedure was performed for each potential risk factor [host, pathogen, environment (region)] and visualised using forest plots as described by [35]. Briefly, we estimated the pooled prevalences with 95% confidence intervals (CI) for Taenia and Echinococcus infections in intermediate and final hosts, which were further analysed by regions. The meta-analysis was conducted using MetaXL add-in for Microsoft Excel (EpiGear International, Queensland, Australia), and results were presented as a forest plot diagram, which shows estimates of pooled prevalence and their respective CIs of individual studies with the summary measure. The results of the analyses are presented with their P-values. The threshold for statistical significance was set at P < 0.05. It was calculated using the random-effects model, which uses the inverse of the sampling variance and a constant variable across the population effects to weight each study [36, 37]. Cochran’s Q and I2 statistics were used for evaluation of heterogeneity and inconsistency, respectively. If the P-value of the Q test was < 0.05 and I2 was > 50%, heterogeneity was inferred [38]. Finally, publication bias was assessed by the Luis Furuya-Kanamori (LFK) index and funnel plot [39]. An LFK index within the range of ± 1, ± 2 and outside ± 2 was inferred as symmetrical, slightly/minor asymmetrical and significantly/major asymmetrical, respectively, where symmetrical index indicates the absence of publication bias [40].

Results

Qualitative analysis

The online literature search yielded 15,581 potentially relevant references. After the first screening by title and/or abstract, the full texts of 558 remaining publications were further examined. A total of 86 duplicate articles were excluded while a further 271 articles were excluded during the second selection process. Unrelated title, study area and purpose/method of study were the three most common reasons for exclusion. A total of 201 publications resulting in 311 datasets were found eligible for inclusion in this systematic review, of which 251 datasets were subjected to meta-analysis to determine associations between Taenia and/or Echinococcus infection and potential risks. The review process for selecting the articles is shown in the flow diagram (Fig. 1).

Fig. 1
figure1

Study flowchart for the prevalence and distribution of Taenia and Echinococcus infections in Ethiopia

Taenia and/or Echinococcus infections were reported in seven regional states and two chartered cities. However, we could not find reports on Taenia and/or Echinococcus infections in two regions, namely Gambela and Benishangul-Gumuz regional states. Regarding the regional distribution of reviewed studies, most (32.8%, 66/201) included in this review were from Oromia followed by Amhara (22.9%, 46/201) regional states as indicated in Fig. 2. Furthermore, the number of reports focusing on Echinococcus and Taenia infections is also shown on the Ethiopian map (Fig. 3); most of the reports are from Oromia regional state. However, the map does not show those reports that were not described by region.

Fig. 2
figure2

Overall distributions of reports for the prevalence and distribution of Taenia and Echinococcus infections in Ethiopia. AA Addis Ababa, Oro Oromia, Tig Tigray, SNNP Southern Nation and Nationality of People, Amh Amhara, Har Harar, DD, Dire Dawa, Som Somali

Fig. 3
figure3

Map of Ethiopia showing regions with study distributions/concentration a Echinococcus infection, b Taenia infection. Shapefiles for Ethiopia were retrieved from https://africaopendata.org/dataset/ethiopia-shapefiles and the program ArcMap 10.1 of ArcGIS was used to create the distribution map

Human Taenia/Echinococcus infections

Of the studies included in the systematic review, 58 reported human taeniasis and/or cystic echinococcosis (Table 1). Comparatively, many reports (30.5%) were reviewed from Addis Ababa, the capital of the country. Most data were separately extracted from cross-sectional studies containing active hospital/health facilities reports (n = 24) followed by case reports (n = 23). Regarding the diagnostic methods used, most (59.3%) of the reports were based on parasitological examination (faecal examination for taeniasis; postmortem examination for CE) followed by imaging (30.5%) for CE. Of the total, cases were reported as taeniasis (n = 35) with prevalence range of 0.05–12.2% and CE (n = 24) with prevalence range of 0.066–0.7%. Some papers reported taeniasis together with other parasites. The total sample size throughout the study years was 400,450 study subjects in which 1938 were found positive for Taenia and/or Echinococcus infection (Additional file 2: Table S2).

Table 1 Distribution of data sets by human taeniasis and CE, Ethiopia

Most human CEs were reported as case reports with a total sample size of 514. These reports focused on unusual presentations and complications of cystic echinococcosis, such as tibial, hepatic, breast, neck, thigh, intra-abdominal, chest wall, cerebral, ovarian, pulmonary, interventricular septum, vertebral, pelvic, and epidural and paraspinal thoracic cyst disease related to Echinococcus. There were limited studies focusing on population-based assessments of human CE in Ethiopia. During the study period, only one article showed a prevalence of 0.7% (7/990, 95% CI 0.02–1.20) in a human CE population-based active survey in SNNP, Ethiopia (Additional file 2: Table S2).

Animal intermediate hosts of Taenia/Echinococcus infections

A total of 144 data set reports were eligible for the final systematic review focusing on cattle, sheep, goats, camels and pigs. The maximum number of reports by region was conducted in Oromia followed by Amhara regional states. Moreover, a single report may include one or more study regions/city administration. Abattoir-based postmortem examination was frequently used for the detection of these parasite infections; molecular and coprology techniques were also used (Additional file 3: Table S3).

The total sample size throughout the study years was 1,658,057 animals, and 179,722 of them were found positive for Taenia and/or Echinococcus infections. The most extensive study regarding sample size employed was 1,083,575 animals (goats) while the smallest study included was only 25 animals (camels). The studies reported on bovine, ovine, caprine, camel and swine CE with prevalence range of 2.6–65.15%, 1.1–68%, 0–65%, 12–61.6% and 9.96%, respectively (Additional file 4: Table S4, Additional file 5: Table S5, Additional file 6: Table S6, Additional file 7: Table S7, Additional file 8: Table S8).

Similarly, the studies also reported on bovine cysticercosis with prevalence range of 0.78–30.7%. However, there were only limited reports focusing on the prevalence of Taenia and Echinococcus infections in some animals. For instance, only one study reported the prevalence of 0.4% (1/257, 95% CI 0.01–2.15) of taeniasis in cattle based on coprological examination; however, the results did not indicate the species level (Additional file 4: Table S4).

The prevalence of T. hydatigena, T. ovis and T. multiceps in sheep across the studies showed prevalence range of 5.73–79%, 2.86–26% and 2.6–19.09%, respectively (Additional file 5: Table S5). Furthermore, the prevalence of T. hydatigena, T. ovis and T. multiceps in goats across the studies showed prevalence range of 8.07–72.38%, 2.1–22% and 0.52–11.7%, respectively (Additional file 6: Table S6).

Direct financial losses associated with organ condemnation reported for some of the parasites were substantial. Some surveys focused on organ condemnation to investigate the financial losses due to infection and other factors that makes calculation of the prevalence difficult. Overall, about 65 studies reported financial losses that range from 4380 ETB or $200 [98] to 34,927,200 ETB or $1,591,216.40 [99] per abattoir survey. The losses were due to the condemnation of edible carcasses and offal such as liver, lung, heart, kidney, spleen, tongue and head. Such reports highlighted the importance of these parasitic infections to the livestock sector.

However, only a few molecular studies (n = 7) aimed at identifying and genotyping Echinococcus genotypes/species responsible for CE and Taenia species were reported (Table 2), which made determining the prevalence of Echinococcus species that occur in Ethiopia difficult. At least one molecular study was conducted in all regions except the Amhara, Afar, Benshangul-Gumuz and Gambella regions.

Table 2 Molecular studies included in the systematic review and meta-analysis, Ethiopia

Animal final hosts of Taenia/Echinococcus infections

Of the studies included in the systematic review, 12 reports discussed the role of prevalence and distribution of Taenia and Echinococcus infections across the country. As described in Table 3, most (81.8%) reports employed parasitological (faecal and postmortem) examination as diagnostic method and 45.5% investigated adult Echinococcus species. The results demonstrated limited employment of molecular techniques for the diagnosis of these parasitic infections in the final hosts. The total sample size throughout the study years was 796 final hosts (dogs, wolf, hyena), and 39.07% were positive either for Taenia or Echinococcus species.

Table 3 Distribution of data sets by animal final hosts’ taeniasis and CE, Ethiopia

In contrast, according to the available data from three regional states, namely Amhara, SNNP and Tigray, average prevalence of taeniasis in dogs was found to be 45.01% with 95% CI as low as 2.1% and as high as 97.3% reporting adult Taenia species namely Taenia hydatigena, T. multiceps and T. ovis. In particular, postmortem findings of 51 dogs revealed 56.86% prevalence of taeniasis. The available evidence also indicated a prevalence range of 16.7–88.9% for canine echinococcosis (Additional file 9: Table S9).

Meta-analysis

The results of the meta-analysis (forest plots, DOi plot and pooled prevalence with their respective 95% CI) and potential publication bias (funnel plots) were separately recorded.

Overall prevalence of Taenia and Echinococcus infections

From the quantitative analysis, a total of 29,163 intermediate and final hosts were infected by Taenia and/or Echinococcus [115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173]. Dataset results, pooled effect and heterogeneity are summarized in Table 4. Of the total, 17,971 intermediate hosts were infected by CE with pooled prevalence of 22% (95% CI 18–26%) and high study variability (Q = 24,420.65, I2 = 100%, P = 0.000). Moreover, a total of 49 final hosts were infected by echinococcosis with pooled prevalence of 33% (95% CI 20–48%) and between-study variability was low (Q = 17.24, I2 = 65%, P = 0.001). Similarly, of the total, 350 study subjects including humans, cattle, sheep, goats and wolves with Taenia infection showed a pooled prevalence of 3% (95% CI 2–4%) and between-study variability of (Q = 279.07, I2 = 89, P = 0.000). Meanwhile, 3764, 443 and 151 of intermediate hosts were infected by larval stages of T. hydatigena, T. ovis and T. multiceps with pooled prevalence of 38%, 14% and 5%, respectively. The overall prevalence of these parasitic infections is illustrated by forest plots (Figs. 4, 5, 6, Additional file 10: Figure S1).

Table 4 Overall pooled prevalence of Taenia and Echinococcus infections in intermediate and final hosts, Ethiopia
Fig. 4
figure4

Overall prevalence evidenced by forest plot: a dog echinococcosis; b taeniasis. Prev prevalence, CI confidence intervals; *same study

Fig. 5
figure5

Overall prevalence of Taenia hydatigena evidenced by forest plot. Prev prevalence, CI confidence interval; *same study

Fig. 6
figure6

Overall prevalence evidenced by forest plot: a Taenia ovis; b Taenia multiceps. Prev prevalence, CI confidence interval; *same study

Furthermore, the pooled prevalence of these cestode infections is presented separately by host in Table 4. Regarding CE, high pooled prevalence of 47.7% (95% CI 20.4–75.7%) in camels followed by 25.5% (95% CI 22.2–28.9%) in cattle, 18.8% (95% CI 13.0–25.4%) in sheep and 13.2% (95% CI 6.3–21.9%) in goats was recorded. For the case of taeniasis, high pooled prevalence of 51.3% (95% CI 0.00–100%) was recorded in wolf followed by goat 3.1% (95% CI 0.00–17.7%).

The random effect meta-analysis of T. saginata (bovine cysticercosis) showed that individual study prevalence estimates ranged from 0.78 to 30.7% with an overall pooled prevalence of 7% (95% CI 5–9%). Studies’ weights ranged from 1.8 to 2.0%. Between-study variability was high of (Q = 4458.76; I2 = 99% with a P-value of 0.000) (Fig. 7).

Fig. 7
figure7

Overall prevalence of Taenia saginata (Cysticercus bovis) evidenced by forest plot. Prev prevalence, CI confidence interval; *same study

However, high prevalences of 38.9% (95% CI 25.6–53.0%), 14.6% (95% CI 6.8–24.6%) and 5.9% (95% CI 1.5–12.5%) of T. hydatigena, T. ovis and T. multiceps, respectively, were reported in sheep (Additional file 5: Table S5).

Prevalence of Taenia and Echinococcus infections by region

Significant differences in prevalence of Taenia and Echinococcus infections between study regions or livestock type have been reported (Additional file 11: Table S10). Region-based group analysis showed 30.1% pooled prevalence of bovine CE at Oromia (95% CI 22.5–38.3%) and 28.4% at Addis Ababa (95% CI 18.5–39.4%). Similarly, high pooled prevalences of 16.6% (95% CI 9.3–25.5%) and 7.4% (95% CI 2.4–14.5%) of ovine and caprine CE, respectively, were recorded in Oromia regional state. Moreover, a pooled prevalence of 37.1% (95% CI 22.4–53.0%) dog echinococcosis was also recorded from the same region. The reports within each of the subgroup of the study animals were highly heterogeneous for CE (I2 > 96%) except for bovine and ovine CE in Dire Dawa and Amahara, respectively. There was also less heterogeiniety in reports of dog echinococcosis in Amhara, Oromia and Tigray regional states (I2 < 90%).

Based on coprological results, comparatively high pooled prevalence of human taeniasis was recorded in Addis Ababa (4.0%, 95% CI 1.1–8.3%) followed by Oromia (3.9%, 95% CI 2.4–5.6%). Meanwhile, two research papers with pooled prevalence of 51.3% (95% CI 0.00–100%) of taeniasis in wolves (Canis simensis) were documented from Oromia regional state.

Most cattle were found to be infected by T. saginata in SNNP with a pooled prevalence of 10.5% (95% CI 4.0–19.4%) followed by 7.9% (95% CI 5.7–10.4%) in Oromia regional state. Regarding T. hydatigena, high prevalence was reported from Dire Dawa with a pooled prevalence of 52.8% (95% CI 0.00–100%) and 40.7% (95% CI 10.5–74.6%) in sheep and goat, respectively. Likewise, a pooled prevalence ranging from 3.6 to 8.3% of T. ovis and T. multiceps from both sheep and goat was reported from Oromia regional state. Additional file 11: Table S10 presents the summary of key findings reported in this review.

Publication bias

The existence of publication bias was assessed in some study groups but not for some because of the nature of the article (case report) or not enough publication data to discuss the possible impact on infection prevalence (camel, pig, dog, wolf and hyena). Possible publication bias was demonstrated by visualization of asymmetry in funnel plots with their respective LFK values. Accordingly, there was no asymmetry for echinococcosis (LFK index = 0.23), taeniasis (LFK index = 0.93), T. hydatigena (LFK index = 0.61) and T. multiceps (LFK index = 0.58) infection. There was minor asymmetry for hydatidosis (LFK index = 1.59). In contrast, there was major asymmetry for T. ovis (LFK index = 2.59) and T. saginata (LFK index = 3.07), which indicates the presence of publication bias as indicated in the funnel plots presented (Additional file 12: Figure S2, Additional file 13: Figure S3, Additional file 14: Figure S4, Additional file 15: Figure S5, Additional file 16: Figure S6, Additional file 17: Figure S7, Additional file 18: Figure S8).

Discussion

This SR and meta-analysis summarized the current evidence on the prevalence and distribution of Taenia and Echinococcus infections in Ethiopia. More than 15,500 potentially relevant references were assessed, a fact that emphasizes the broad relevance of the topic.

At least one report was documented from each region and chartered cities except for Gambela and Benishangul-Gumuz. The absence of data, however, does not exclude the existence of cestode infection in these regions. Moreover, poor diagnosis and reporting, particularly in rural areas, indicate that the data accrued are likely to underestimate occurrence.

Abattoir-, hospital-, household- and field-based studies conducted across the country were used as source of data. Most of the studies were conducted in Oromia and Amhara followed by Addis Ababa and SNNP regional states. The geographical distribution of Taenia and Echinococcus infection within the country was uneven and might affect the generalization of the findings. Spatial variation in the infection prevalence in livestock was previously reported by Jobre et al. [174] and Kebede et al. [175]. The distribution may also be influenced by temperature and humidity [176].

Most human CE was reported as case reports focused on unusual presentations and complications of cystic echinococcosis, such as tibial, hepatic, breast, neck, thigh, intra-abdominal, chest wall, cerebral, ovarian, pulmonary, interventricular septum, vertebral, pelvic, and epidural and paraspinal thoracic cysts, which makes them non-representative of the epidemiology of cystic echinococcosis in the affected area [177]. Evidence from hospital-based case reports from other parts of the world indicates that the condition of patients with cerebral Echinococcus cysts depends on the size and location of the cysts. However, the lack of advanced imaging techniques in most rural health facilities in sub-Saharan Africa where the disease is endemic could, in part, contribute to the lack of reported cases of cystic echinococcosis [178]. Similarly, population-based active surveys have not been well documented and explored at the country level. This may be attributed to the fact that it is a neglected disease [179]. In addition, the diagnosis requires advanced techniques for confirmation particularly in humans [180]. Furthermore, five studies were included in this study where the diagnosis was made in Ethiopian immigrants outside the country. This indicates the chronic nature of the disease [181, 182].

The high prevalence of taeniasis in most developing countries including Ethiopia is due to the habit of consuming raw or undercooked beef [183, 184]. In the current study, high prevalence of taeniasis based on microscopy was found in Addis Ababa followed by Oromia region. However, coprological techniques have fairly low sensitivities associated with intermittent egg excretion and depend on the technique used [185, 186].

Most studies in animal intermediate hosts were conducted in Oromia and Amhara regions because of their infrastructure advantages (both municipal and private abattoirs). Similarly, most of the hosts investigated were ruminants (cattle, sheep and goat) because of the high meat demand of the people inhabiting these regions. This will have a direct impact on the life cycle of Taenia and Echinococcus spp. [187]. The life cycle is completed when the final host, such as dogs, ingests Echinococcus cysts containing protoscolices [188] where there is enough access to visceral organs from the slaughtered animals.

In the current study available evidence suggests limited application of molecular tools. This is because little funding is given for research and management of neglected tropical diseases in sub-Saharan Africa [189, 190]. Another reason could be the lack of well-equipped laboratories and trained personnel.

Though the life cycle of taeniasis and echinococcosis involves canids, limited studies have been conducted at different interfaces. For instance, there are > 55 protected areas (including 21 national parks) in the country [191] where potential intermediate and final hosts are present, but the status of the infections is not well reported. However, the interaction between wildlife and livestock transmitted forms is likely to have an impact on human and animal health in the vicinity of the national parks [102].

Regarding livestock, several cystic echinococcosis investigations in cattle from several parts of Ethiopia have found regional differences in prevalence. Similar studies in Kenya, a neighboring country, demonstrated that cystic echinococcosis occurs in most parts of the country but available data are mostly from Turkana communities in the northwest and from Maasai communities in the south [177]. The current study also showed similar variation in the prevalence of CE among the different regions of the country. Similarly, Omer and her colleagues [192] also documented similar findings in Sudan. From central Sudan, prevalence ranged from 20% (cattle) to 55.6% (camels). In western Sudan, prevalence is highest among camels (61.4% of 565) followed by sheep (11.9% of 9272). In southern Sudan, varying prevalences in cattle (7.1% of 325), sheep (2.7% of 295) and goats (7.1% of 42) have also been reported.

In Africa, though differing by country and also region, CE is reported most commonly in cattle [193,194,195]. Meanwhile, CE is the major cause of organ condemnation in most Ethiopian abattoirs and leads to huge economic losses [196, 197]. In the present review higher pooled prevalence of CE was recorded in camels and cattle than sheep and goats. Variation among the intermediate hosts could be ascribed to the age factor. For instance, cattle and camels are generally slaughtered at older age than sheep and goats and consequently are exposed to infection over a longer period of time [198]. Ibrahim [199], Cabrera et al. [200] and Guorino et al. [201] also reported an increase in prevalence of the disease with increase in age.

The low prevalence of Echinococcus cyst infection in pigs in Ethiopia could be mainly attributed to the absence of extensive swine farms in the country [198]. Furthermore, pork is not consumed by most of people in Ethiopia. In general, information on echinococcosis in pigs in sub-Saharan Africa is scarce [177] but high prevalence (56%) is reported from West Africa in the region the Niger Delta [202]. In the current review, though reports are limited, the findings showed the significance of dog echinococcosis. Globally, echinococcosis presents a serious health concern especially in endemic countries [31, 32] where transmission of the disease is affected by the prevalence of the parasite in domestic dogs, behaviors of humans towards dogs and other related factors [203].

There are considerable variations in the prevalence and distribution of T. saginata (bovine cysticercosis) in different areas that are not easily explained by the existing information. The overall pooled prevalence was lower than in reports from Nigeria, 29% [204], but higher than in reports from Kenya, 2.56% [205], whereas the prevalence ranged from 0.2 to 20% in Egypt [206]. Results showed a widespread occurrence of metacestodes in sheep and goats in Ethiopia where T. hydatigena (C. tenuicollis) was the most common cestode (metacestode) reported, in line with the report of Asmare et al. [207].

Studies to determine the prevalence of coenurosis (T. multiceps) in small ruminants show low variation in their results. In contrast, this result is much lower than the findings of Desouky et al. [208] and Miran et al. [209] in Tanzania who reported a T. multiceps prevalence of 44.4% in small ruminants (45.6% in sheep and 43.3% in goats). This could be due to factors that play an important role in the epidemiology of T. multiceps [210].

Most taeniids of dogs are globally distributed. In the current study, only two studies described the status of Taenia infection with average prevalence of 45% of T. hydatigena, T. multiceps and T. ovis. This finding is supported by Mulinge et al. [211] who found T hydatigena and T. multiceps were the most frequent taeniids of dogs in some parts of Kenya. Such findings demonstrate the involvement of dogs in the transmission cycles of the diseases. However, the limited number of studies (only two reports) from most of the regions affected the reflection of the real situation of these parasites in the country.

Molecular studies during the survey period covered most of the regions, though the numbers of studies are unbalanced, which made determining the prevalence of Echinococcus species that occur in Ethiopia difficult; they ranged from one to five reports per region, except for Afar, Amhara, Benishangul-Gumuz and Gambela regional states where molecular data were absent. These reports showed the presence of different genotypes, E. ortleppi (genotype 5), E. granulosus s.s., E. canadensis and E. intermedius (genotype 6). This shows cattle may have an important role in the life cycle of this disease and indicates the existence of potential transmission to human and other susceptible hosts [212,213,214]. Moreover, genotype 6 has been identified in human CE in Argentina, Nepal and Iran [215,216,217] cited by [181].

Study limitation

We observed study limitations such as the scantiness of data in some regions, publication bias, heterogeneity between studies and the uneven prevalence distribution among study regions. Few reports had results showing tapeworm infection (broad classification) that were not identified at the species level and some studies reported taeniasis together with other parasites. Moreover, only few studies reported at genotype level, which made determining the prevalence of Echinococcus spp. that occur in Ethiopia difficult. Lastly, when the meta-analysis included only a small number of studies, it was not possible to assess publication bias using funnel plots.

Conclusion

In the current study, we provided comprehensive information on the prevalence and distribution of Taenia and Echinococcus infections in Ethiopia. The results showed the status of these cestode infections in different regions, but studies were mainly carried out around central Ethiopia, particularly Oromia and Addis Ababa, because of the presence of relatively more infrastructure. The meta-analysis confirmed a high degree of variability in pooled prevalence of these parasitic infections. However, there are still many data gaps with respect to the research coverage and agro-ecological factors contributing to the parasite prevalence and distribution across the country, which urges further studies. Therefore, annual surveillance of infection rates in dogs, livestock and humans is critical for determining a pre-intervention baseline and evaluating the effectiveness of control programmes.

Availability of data and materials

All data generated or analysed in this paper are provided as Additional files.

Abbreviations

AE:

Alveolar echinococcosis

CE:

Cystic echinococcosis

CI:

Confidence interval

ETB:

Ethiopian Birr

LFK:

Luis Furuya-Kanamori

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analysis

SNNP:

South Nation and Nationality of People

SSA:

Sub-Saharan African

References

  1. 1.

    Roberts LS, Janovy J, Schmidt GD. Gerald D. Schmidt & Larry S. Roberts’ Foundations of Parasitology. Boston: McGraw-Hill; 2009.

    Google Scholar 

  2. 2.

    Worldometer. Worldometers.info/world-population/Ethiopia-population; 2019. Accessed 25 July 2020.

  3. 3.

    CSA. Federal Democratic Republic of Ethiopia agricultural sample survey 2017/2018 (2010 E.C.), Volume II, Report on livestock and livestock characteristics, Central Statistical Agency, Addis Ababa. Addis Ababa; 2018.

  4. 4.

    Hiko A, Ibrahim H, Agga GE. Abattoir based survey of bovine cystic echinococcosis in selected commercial abattoir in Ethiopia. J Vet Sci Technol. 2018;9:1–5.

    Article  Google Scholar 

  5. 5.

    Lindahl JF, Grace D. The consequences of human actions on risks for infectious diseases: a review. Inf Ecol Epidemiol. 2015;5:30048.

    Google Scholar 

  6. 6.

    McDermott J, Grace D. Agriculture-associated diseases: adapting agriculture to improve human health. In: Fan S, Pandya-Lorch R, editors. Reshaping agriculture for nutrition and health. Washington, DC: International Food Policy Research Institute; 2012.

    Google Scholar 

  7. 7.

    Greger M. The human/animal interface: emergence and resurgence of zoonotic infectious diseases. Crit Rev Microbiol. 2007;33:243–99.

    PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    WHO. Investing to overcome the global impact of neglected tropical diseases: third WHO report on neglected tropical diseases. Geneva: World Health Organization; 2015.

    Google Scholar 

  9. 9.

    FDRE-MoH. Second edition of national neglected tropical diseases (NTDs) master plan (2015/16–2019/20). Addis Ababa, Ethiopia: Ministry of health, federal democratic republic of Ethiopia. 2016.

  10. 10.

    Diop G, Yanagida T, Hailemariam Z, Menkir S, Nakao M, Sako Y, et al. Genetic characterization of Moniezia species in Senegal and Ethiopia. Parasitol Int. 2015;64:256–60.

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Egger B. Making heads or tails of tapeworms. Trends parasitol. 2016;32:511–2.

    PubMed  Article  Google Scholar 

  12. 12.

    Thompson R. Biology and systematics of Echinococcus. Adv Parasitol. 2017;95:65–109.

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Tyler S, Hooge M. Comparative morphology of the body wall in flatworms (Platyhelminthes). Can J Zool. 2004;82:194–210.

    Article  Google Scholar 

  14. 14.

    Eom KS, Rim HJ. Morphologic descriptions of Taenia asiatica sp. n. Korean J Parasitol. 1993;31(1):1–6.

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Hoberg EP. Phylogeny of Taenia: species definitions and origins of human parasites. Parasitol Int. 2006;55:S23–30.

    PubMed  Article  Google Scholar 

  16. 16.

    Jeon HK, Eom KS. Taenia asiatica and Taenia saginata: genetic divergence estimated from their mitochondrial genomes. Exp Parasitol. 2006;113(1):58–61.

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Anantaphruti MT, Yamasaki H, Nakao M, Waikagul J, Watthanakulpanich D, Nuamtanong S, et al. Sympatric occurrence of Taenia solium, T. saginata, and T. asiatica, Thailand. Emerg Infect Dis. 2007;13(9):1413.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Li T, Craig PS, Ito A, Chen X, Qiu D, Qiu J, et al. Taeniasis/cysticercosis in a Tibetan population in Sichuan province. China Acta Trop. 2006;100(3):223–31.

    PubMed  Article  Google Scholar 

  19. 19.

    Jibat T, Ejeta G, Asfaw Y, Wudie A. Causes of abattoir condemnation in apparently healthy slaughtered sheep and goats at HELMEX abattoir, Debre Zeit, Ethiopia. Rev Méd Vét. 2008;159(5):305.

    Google Scholar 

  20. 20.

    Regassa A, Moje N, Megersa B, Beyene D, Sheferaw D, Debela E, et al. Major causes of organs and carcass condemnation in small ruminants slaughtered at Luna export abattoir, Oromia Regional State, Ethiopia. Prev Vet Med. 2013;110(2):139–48.

    PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Achenef M, Markos T, Feseha G, Hibret A, Tembely S. Coenurus cerebralis infection in Ethiopian highland sheep: incidence and observations on pathogenesis and clinical signs. Trop Anim Health Prod. 1999;31(1):15–24.

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    Radostits OM, Gay CC, Blood DC, Hinchcliff KW. Disease of the alimentary tract. In: A textbook of disease of cattle, sheep, pigs, goats and horses. 10th ed. Oxford: Saunders Publication Co.; 2010.

    Google Scholar 

  23. 23.

    Chappell L. Encyclopedic reference of parasitology Vol. 1 Biology, structure, function; Vol. 2 Disease, treatment, therapy. (ed. H. Mehlhorn,). Springer-Verlag, Berlin. ISBN 3-540-66239-1. Parasitology. 2001;123(5):531–5.

    Article  Google Scholar 

  24. 24.

    Abushhewa MH, Abushhiwa MH, Nolan MJ, Jex AR, Campbell BE, Jabbar A, et al. Genetic classification of Echinococcus granulosus cysts from humans, cattle and camels in Libya using mutation scanning-based analysis of mitochondrial loci. Mol Cell Probes. 2010;24(6):346–51.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Brunetti E, Kern P, Vuitton DA. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114(1):1–16.

    PubMed  Article  Google Scholar 

  26. 26.

    Dakkak A. Echinococcosis/hydatidosis: a severe threat in Mediterranean countries. Vet Parasitol. 2010;174(1–2):2–11.

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Scala A, Garippa G, Varcasia A, Tranquillo VM, Genchi C. Cystic echinococcosis in slaughtered sheep in Sardinia (Italy). Vet Parasitol. 2006;135(1):33–8.

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Kebede W, Hagos A, Girma Z, Lobago F. Echinococcosis/hydatidosis: its prevalence, economic and public health significance in Tigray region, North Ethiopia. Trop Anim Health Prod. 2009;41(6):865–71.

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Regassa F, Molla A, Bekele J. Study on the prevalence of cystic hydatidosis and its economic significance in cattle slaughtered at Hawassa municipal abattoir, Ethiopia. Tropl Anim Health Prod. 2010;42(5):977–84.

    Article  Google Scholar 

  30. 30.

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

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Deplazes P, Rinaldi L, Rojas C, Torgerson P, Harandi M, Romig T, et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol. 2017;95:315–493.

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Schweiger A, Ammann RW, Candinas D, Clavien PA, Eckert J, Gottstein B, et al. Human alveolar echinococcosis after fox population increase, Switzerland. Emerg Infect Dis. 2007;13(6):878–82.

    PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    CSA, ICF. Ethiopia demographic and health survey. Addis Ababa, Ethiopia and Calverton, Maryland, USA: Central Statistical Agency [Ethiopia] and ICF International. 2011.

  34. 34.

    Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.

    PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Conraths FJ, Probst C, Possenti A, Boufana B, Saulle R, La Torre G, et al. Potential risk factors associated with human alveolar echinococcosis: systematic review and meta-analysis. PLoS Negl Trop Dis. 2017;11(7):e0005801.

    PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Hedges LV, Vevea JL. Fixed-and random-effects models in meta-analysis. Psychol Methods. 1998;3(4):486–504.

    Article  Google Scholar 

  37. 37.

    DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trial. 2007;28(2):105–14.

    Article  Google Scholar 

  38. 38.

    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.

    PubMed  Article  Google Scholar 

  39. 39.

    Barendregt JJ, Doi SA. MetaXL user guide version 5.3. EpiGear International Pty Ltd. 2016.

  40. 40.

    Ohiolei JA, Li L, Ebhodaghe F, Yan HB, Isaac C, Bo XW, et al. Prevalence and distribution of Echinococcus spp. in wild and domestic animals across Africa: a systematic review and meta-analysis. Transbound Emerg Dis. 2020;67(6):2345–64.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. 41.

    Kassa BG, Yeshi MM, Abraha AH, Gebremariam TT. Tibial hydatidosis: a case report. BMC Res Notes. 2014;7(1):1–4.

    Article  Google Scholar 

  42. 42.

    Mardu F, Yohannes M, Tadesse D. Prevalence of intestinal parasites and associated risk factors among inmates of Mekelle prison, Tigrai Region, Northern Ethiopia. BMC Infect Dis. 2019;19(1):1–8.

    Article  Google Scholar 

  43. 43.

    Yemane M, Kumar A. Retrospective study on prevalence of human taeniasis in Mekelle, Tigray, Ethiopia. Momona Ethiop J Sci. 2018;10(2):290–7.

    Article  Google Scholar 

  44. 44.

    Chala B. Prevalence of intestinal parasitic infections in Mojo health center, Eastern Ethiopia: a 6-year (2005–2010) retrospective study. Epidemiol. 2013;3(119):2161–1165.

    Google Scholar 

  45. 45.

    Fontanet AL, Sahlu T, Rinkede Wit T, Messele T, Masho W, Woldemichael T, et al. Epidemiology of infections with intestinal parasites and human immunodeficiency virus (HIV) among sugar-estate residents in Ethiopia. Ann Trop Med Parasitol. 2000;94(3):269–78.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Geinoro T, Bedore B. Prevalence of Cysticercus bovis in cattle slaughtered at Bishoftu municipal abattoir; public health significance and community perception about zoonotic importance of taeniosis in Bishoftu. Int J Adv Res Biol Sci. 2019;6(4):52–61.

    Google Scholar 

  47. 47.

    Hailemariam G, Kassu A, Abebe G, Abate E, Damte D, Mekonnen E, et al. Intestinal parasitic infections in HIV/AIDS and HIV seronegative individuals in a teaching hospital, Ethiopia. Jpn J Infect Dis. 2004;57(2):41–3.

    PubMed  Google Scholar 

  48. 48.

    Nyantekyi L, Legesse M, Medhin G, Animut A, Tadesse K, Macias C, et al. Community awareness of intestinal parasites and the prevalence of infection among community members of rural Abaye Deneba area, Ethiopia. Asian Pac J Trop Biomed. 2014;4:S152–7.

    PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Mhatebu WT, Nuru HB, Kerse SM, Tigre W. Community’s knowledge, attitude and practices on hydatidosis and its public health implication in Asella and Adama areas central Ethiopia. Food Sci Qual Mgt. 2017;62:1–9.

    Google Scholar 

  50. 50.

    Worku E. Major metacestodes of cattle, sheep and goats slaughtered at Bishoftu ELFORA export abattoir, community perception and public health significance of zoonotic cestodes, MVSc. Thesis, Addis Ababa University, College of Veterinary Medicine and Agriculture; 2017.

  51. 51.

    Yeshanew S, Tadesse T. Prevalence of intestinal parasites among HIV seropositive individuals at Mettu Karl hospital, Southwest Ethiopia (preliminary study). Int J Health Sci Res. 2017;7(2):275–80.

    Google Scholar 

  52. 52.

    Abera B, Biadegelgen F, Bezabih B. Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar town, Northwest Ethiopia. Ethiop J Health Dev. 2010. https://doi.org/10.4314/ejhd.v24i1.62944.

    Article  Google Scholar 

  53. 53.

    Bekele A, Firew A. A rare case of hydatid cyst disease of the breast: a case report and review of literature. Ethiop Med J. 2016;54(1):37–40.

    PubMed  PubMed Central  Google Scholar 

  54. 54.

    Dagnew M, Tiruneh M, Moges F, Tekeste Z. Survey of nasal carriage of Staphylococcus aureus and intestinal parasites among food handlers working at Gondar university, Northwest Ethiopia. BMC Public Health. 2012;12(1):1–7.

    Article  Google Scholar 

  55. 55.

    Asnakech D. Intestinal parasitic infections among patients visiting Gorebella health center, North-Central Ethiopia, MSc. Thesis, Addis Ababa University; 2016.

  56. 56.

    Kebede N, Mitiku A, Tilahun G. Retrospective survey of human hydatidosis in Bahir Dar, north-western Ethiopia. East Mediterr Health J. 2010;16(9):937–41.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. 57.

    Mamo H. Intestinal parasitic infections among prison inmates and tobacco farm workers in Shewa Robit, north-central Ethiopia. PLoS ONE. 2014;9(6):e99559.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  58. 58.

    Chanyalew MD, Gurara MK. Malaria and intestinal parasite infections and co-infections in Tach Gayint district, South Gondar zone, Amhara Regional State. Sci J Public Health. 2014;296:546–53.

    Google Scholar 

  59. 59.

    Yimam NE. Individual, household and environmental variables in relation to some neglected tropical diseases. In: Hara health center, South Wollo, Northeast Ethiopia, MSc. Thesis, Addis Ababa University; 2016.

  60. 60.

    Yimer A, Gebrmedehan BM. Bovine cysticercosis and hospital based retrospective survey of human taeniasis in and around Debre Brihan city, central Ethiopia. Biol Med. 2019;11(2):455.

    Google Scholar 

  61. 61.

    Alemu M, Anley A, Tedla K. Magnitude of intestinal parasitosis and associated factors in rural school children, Northwest Ethiopia. Ethiop J Health Sci. 2019. https://doi.org/10.4314/ejhs.v29i1.14.

    Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Dessie S. Intestinal parasitic infections among patients of Aykel health center, Northwest Ethiopia, MSc. Thesis, Addis Ababa University, Ethiopia; 2017.

  63. 63.

    Alemayehu B, Tomass Z, Wadilo F, Leja D, Liang S, Erko B. Epidemiology of intestinal helminthiasis among school children with emphasis on Schistosoma mansoni infection in Wolaita zone, Southern Ethiopia. BMC Public Health. 2017;17(1):1–10.

    Article  Google Scholar 

  64. 64.

    Alemu G, Mama M. Intestinal helminth co-infection and associated factors among tuberculosis patients in Arba Minch, Ethiopia. BMC Infect Dis. 2017;17(1):1–9.

    Article  Google Scholar 

  65. 65.

    Alemu M, Hailu A, Bugssa G. Prevalence of intestinal schistosomiasis and soil-transmitted helminthiasis among primary schoolchildren in Umolante district, South Ethiopia. Clin Med Res. 2014;3(6):174–80.

    Article  Google Scholar 

  66. 66.

    Birmeka M, Urga K, Petros B. Intestinal parasitic infection and nutritional status of elementary schoolchildren aged 7–14 in Enemorena-Ener district, Gurage zone, Ethiopia. EC Nutri. 2017;9(3):129–41.

    Google Scholar 

  67. 67.

    Fekadu S, Taye K, Teshome W, Asnake S. Prevalence of parasitic infections in HIV-positive patients in southern Ethiopia: a cross-sectional study. J Infect Dev Ctries. 2013;7(11):868–72.

    PubMed  Article  PubMed Central  Google Scholar 

  68. 68.

    Merid Y, Hegazy M, Mekete G, Teklemariam S. Intestinal helminthic infection among children at lake Awassa area, South Ethiopia. Ethiop J Health Dev. 2001;15(1).

  69. 69.

    Mulugeta Y, Yohannes M, Wolde D, Aklilu M, Ashenefe B, Gebree D, et al. Intestinal parasites in dogs and humans, environmental egg contamination and risk of human infection with zoonotic helminth parasites from dog in Hosanna town. Int J Biomed Mater Res. 2019;7(1):24–36.

    Google Scholar 

  70. 70.

    Klungsoyr P, Courtright P, Hendrikson TH. Hydatid disease in the Hamar of Ethiopia: a public health problem for women. Trans R Soc Trop Med Hyg. 1993;87(3):254–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. 71.

    Terefe A, Shimelis T, Mengistu M, Hailu A, Erko B. Schistosomiasis mansoni and soil-transmitted helminthiasis in Bushulo village, southern Ethiopia. Ethiop J Health Dev. 2011;25(1):46–50.

    Article  Google Scholar 

  72. 72.

    Wassermann M, Woldeyes D, Gerbi BM, Ebi D, Zeyhle E, Mackenstedt U, et al. A novel zoonotic genotype related to Echinococcus granulosus sensu stricto from southern Ethiopia. Int J Parasitol. 2016;46(10):663–8.

    PubMed  Article  PubMed Central  Google Scholar 

  73. 73.

    Weldesenbet H, Worku A, Shumbej T. Prevalence, infection intensity and associated factors of soil transmitted helminths among primary school children in Gurage zone, South central Ethiopia: a cross-sectional study design. BMC Res Notes. 2019;12(1):1–6.

    Article  Google Scholar 

  74. 74.

    Wegayehu T, Tsalla T, Seifu B, Teklu T. Prevalence of intestinal parasitic infections among highland and lowland dwellers in Gamo area, South Ethiopia. BMC Public Health. 2013;13(1):1–7.

    Article  Google Scholar 

  75. 75.

    Abebe E, Tsehay A. Hydatid cyst disease in the left lateral neck: an uncommon presentation. Ethiop Med J. 2016;54(3):145–7.

    PubMed  PubMed Central  Google Scholar 

  76. 76.

    Abebe A. Hydatid cyst of the left thigh: a case report. East Cent Afr J Surg. 2010;15(1):139–40.

    Google Scholar 

  77. 77.

    Abebe E, Kassa T, Bekele M, Tsehay A. Intra-abdominal hydatid cyst: sociodemographics, clinical profiles, and outcomes of patients operated on at a tertiary hospital in Addis Ababa, Ethiopia. J Parasitol Res. 2017. https://doi.org/10.1155/2017/4837234.

    Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Aklilu A, Kahase D, Dessalegn M, Tarekegn N, Gebremichael S, Zenebe S, et al. Prevalence of intestinal parasites, salmonella and shigella among apparently health food handlers of Addis Ababa University student’s cafeteria, Addis Ababa, Ethiopia. BMC Res Notes. 2015;8(1):1–6.

    Article  Google Scholar 

  79. 79.

    Ali A, Biluts H, Gulilat D. Experience of surgical therapy in 72 patients with thoracic hydatidosis over a 10-year period. Ethiop Med J. 2005;43(1):1–8.

    PubMed  PubMed Central  Google Scholar 

  80. 80.

    Argaw F, Abebe E, Tsehay A. Primary chest wall hydatid cyst, case report & review of literature. Ann Clin Case Rep. 2017;2:1245.

    Google Scholar 

  81. 81.

    Assefa G, Biluts H, Abebe M, Birahanu MH. Cerebral hydatidosis, a rare clinical entity in Ethiopian teaching hospitals: case series and literature review. East Cent Afr J Surg. 2011;16(2):123–9.

    Google Scholar 

  82. 82.

    Assefa H, Mulate B, Nazir S, Alemayehu A. Cystic echinococcosis amongst small ruminants and humans in central Ethiopia. Onderstepoort J Vet Res. 2015;82(1):01–7.

    Article  CAS  Google Scholar 

  83. 83.

    Biluts H, Minas M, Bekele A. Hydatid disease of the liver: a 12 year experience of surgical management. East Cent Afr J Surg. 2006;11(2):54–60.

    Google Scholar 

  84. 84.

    Deressa A, Yohannes M, Alemayehu M, Degefu H, Tolosa T, Pal M. Human taeniasis in health centers and bovine cysticercosis in selected abattoirs in Addis Ababa and Modjo, Ethiopia. Int J Livest Health. 2012;2:217–26.

    Google Scholar 

  85. 85.

    Gaym A, Abebe D, Degefe DA. Hydatid cyst an unusual cause of ovarian enlargement. Ethiop Med J. 2002;40(3):283–91.

    PubMed  PubMed Central  Google Scholar 

  86. 86.

    Minas M, Biluts H, Bekele A, Alemie M. Surgical management of 234 patients with hydatid disease: the Tikur Anbessa hospital experience. Ethiop Med J. 2007;45(3):257–65.

    PubMed  PubMed Central  Google Scholar 

  87. 87.

    Sisay S, Amezene T, Tadesse H, Zewdneh D, Gorfu Y, Wakjira E, et al. Imaging findings and management of paediatric pulmonary hydatidiosis in an Ethiopian referral hospital. East Cent Afr J Surg. 2015;20(3):73–80.

    Google Scholar 

  88. 88.

    Tefera E, Knapp J, Teodori M. Hydatid cyst of the interventricular septum. Glob Cardiol Sci Pract. 2017;9:1–5.

    Google Scholar 

  89. 89.

    Tessema A, Yitayew B, Kebede T. Intestinal parasitic infections at Tikur Anbessa university hospital, Ethiopia: a 5-year retrospective study. Int J Infect Dis Ther. 2016;1(1):22–6.

    Google Scholar 

  90. 90.

    Sahlu A, Mesfin B, Tirsit A, Knut W. Spinal cord compression secondary to vertebral echinococcosis. J Neurosci Rural Pract. 2016;7(1):143–6.

    PubMed  PubMed Central  Article  Google Scholar 

  91. 91.

    Aderaye G. Pulmonary hydatid cyst as a cause of recurrent haemoptysis and responding to treatment with albendazole. Ethiop Med J. 1998;36(3):193–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Assefa G, Abebe M, Belete A, Schnider J. Epidural and para spinal thoracic hydatidosis presenting with progressive paraparesis and paraplegia: a case report. Ethiop Med J. 2014;52(1):49–51.

    PubMed  PubMed Central  Google Scholar 

  93. 93.

    Abdullah A, Alsafi R, Iqbal J, Rotimi V. Unusual case of pelvic hydatid cyst of broad ligament mimicking an ovarian tumour. JMM Case Rep. 2016;3(4):e005057.

    PubMed  PubMed Central  Article  Google Scholar 

  94. 94.

    Ajmera RK, Simon GL. Appendicitis associated with Taenia species: cause or coincidental? Vector Borne Zoonotic Dis. 2010;10(3):321–2.

    PubMed  Article  PubMed Central  Google Scholar 

  95. 95.

    Almazeedi S, Ali Y, Diba FA, Rajgopal V, Kehinde EO. Bladder outlet and rectal obstruction secondary to a large pelvic hydatic cyst. J Clin Urol. 2014;7(6):418–20.

    Article  Google Scholar 

  96. 96.

    Noss MR, Gilmore K, Wittich AC. A case of taeniasis diagnosed postpartum. Mil Med. 2013;178(4):e516–9.

    PubMed  Article  PubMed Central  Google Scholar 

  97. 97.

    Heaton J. Intestinal helminths infestation in pregnancy: a case report and literature review. Mil Med. 2002;167(11):954–5.

    PubMed  Article  Google Scholar 

  98. 98.

    Birhanu T. Prevalence, financial loss and public health significance of ovine hydatidosis in adama municipal abattoir, Ethiopia. Nat Sci. 2014;12(10):176–82.

    Google Scholar 

  99. 99.

    Birhanu T, Abda S. Prevalence, economic impact and public perception of hydatid cyst and cysticercus bovis on cattle slaughtered at Adama municipal abattoir, south-eastern Ethiopia. Am Euras J Sci Res. 2014;9:87–97.

    Google Scholar 

  100. 100.

    Hailemariam Z, Nakao M, Menkir S, Lavikainen A, Iwaki T, Yanagida T, et al. Molecular identification of species of Taenia causing bovine cysticercosis in Ethiopia. J Helminthol. 2014;88(3):376–80.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  101. 101.

    Hailemariam Z, Nakao M, Menkir S, Lavikainen A, Yanagida T, Okamoto M, et al. Molecular identification of unilocular hydatid cysts from domestic ungulates in Ethiopia: implications for human infections. Parasitol Int. 2012;61(2):375–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  102. 102.

    Romig T, Omer RA, Zeyhle E, Hüttner M, Dinkel A, Siefert L, et al. Echinococcosis in sub-Saharan Africa: emerging complexity. Vet Parasitol. 2011;181(1):43–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  103. 103.

    Terefe Y, Addy F, Alemu S, Mackenstedt U, Romig T, Wassermann M. Genetic characterization of Echinococcus species in eastern Ethiopia. Vet Parasitol Reg Stud Rep. 2019;17:100302.

    CAS  Google Scholar 

  104. 104.

    Tigre W, Deresa B, Haile A, Gabriël S, Victor B, Van Pelt J, et al. Molecular characterization of Echinococcus granulosus sl cysts from cattle, camels, goats and pigs in Ethiopia. Vet Parasitol. 2016;215:17–21.

    CAS  PubMed  Article  Google Scholar 

  105. 105.

    Terefe Y, Hailemariam Z, Menkir S, Nakao M, Lavikainen A, Haukisalmi V, et al. Phylogenetic characterisation of Taenia tapeworms in spotted hyenas and reconsideration of the “Out of Africa” hypothesis of Taenia in humans. Int J Parasitol. 2014;44(8):533–41.

    CAS  PubMed  Article  Google Scholar 

  106. 106.

    Gugsa G, Hailu T, Kalayou S, Abebe N, Hagos Y. Prevalence and worm burdens of gastro-intestinal parasites in stray dogs of Mekelle city, Tigray, Ethiopia. Am Eurasian J Agric Environ Sci. 2015;15(1):08–15.

    Google Scholar 

  107. 107.

    Mersie A. Survey of echinococcosis in eastern Ethiopia. Vet Parasitol. 1993;47(1–2):161–3.

    CAS  PubMed  Article  Google Scholar 

  108. 108.

    Jebessa H. Some helminths of the Ethiopian wolf (Canis simensis Rüpell 1840, Canidae) and its prey in the Bale mountains national park. SINET Ethiopi J Sci. 2009;32(1):81–4.

    Google Scholar 

  109. 109.

    Van Kesteren F, Piggott KJ, Bengui T, Kubri SB, Mastin A, Sillero-Zubiri C, et al. Helminth parasites in the endangered Ethiopian wolf, Canis simensis. J Helminthol. 2015;89(4):487–95.

    PubMed  Article  PubMed Central  Google Scholar 

  110. 110.

    Degefu H, Damet T. Hydatidosis of cattle and sheep, its economic importance and Echinococcus granulosus among stray dogs in South Wollo, Ethiopia. Ethiop Vet J. 2013;17(2):101–19.

    Article  Google Scholar 

  111. 111.

    Kebede N. Prevalence of gastrointestinal parasites of dogs and community awareness about zoonotic diseases in Chagni town, northwestern Ethiopia. Ethiop Vet J. 2019;23(2):13–26.

    Article  Google Scholar 

  112. 112.

    Mulugeta Y, Yohannes M, Wolde D, Aklilu M, Ashenefe B, Gebree D, et al. Intestinal parasites in dogs and humans, environmental egg contamination and risk of human infection with zoonotic helminth parasites from dog in Hosanna town. Int J Biomed Mater Res. 2013;7(1):24–36.

    Google Scholar 

  113. 113.

    Jones O, Kebede N, Kassa T, Tilahun G, Macias C. Occurrence of bovine hydatidosis and evaluation of its risk to humans in traditional communities of Southern region of Ethiopia. Ethiop J Health Dev. 2012;26(1):43–8.

    Google Scholar 

  114. 114.

    Koskei P, Janitschke K, Feseha G. Prevalence of Echinococcus granulosus in some selected sites of Ethiopia. East Afr J Public Health. 2011;8(3):170–5.

    CAS  PubMed  Google Scholar 

  115. 115.

    Abay G, Kumar A. Cysticercosis in cattle and its public health implications in Mekelle city and surrounding areas, Ethiopia. Ethiop Vet J. 2013;17(1):31–40.

    Article  Google Scholar 

  116. 116.

    Belay S, Afera B. Prevalence of Cysticercus bovis in cattle at municipal abbatoir of Shire. J Vet Sci Technol. 2014;5(4):1–3.

    Article  Google Scholar 

  117. 117.

    Getachew T, Olani W, Sadia H. Prevalence and economic significance of bovine hydatidosis and cysticercosis in Mekelle municipality abattoir, northern Ethiopia. J Vet Sci Res. 2017;2:000135.

    Google Scholar 

  118. 118.

    Shiferaw S, Kumar A, Amssalu K. Organs condemnation and economic loss at Mekelle municipal abattoir, Ethiopia. Haryana Vet. 2009;48:17–22.

    Google Scholar 

  119. 119.

    Bayou K, Taddesse T. Prevalence of bovine cysticercosis of slaughtered cattle in Dale Wabera district municipal abattoir, western Ethiopia. Int J Anim Sci. 2018;2(1):1012s.

    Google Scholar 

  120. 120.

    Bedu H, Tafess K, Shelima B, Woldeyohannes D, Amare B, Kassu A. Bovine cysticercosis in cattle slaughtered at Zeway municipal abattoir: prevalence and its public health importance. J Vet Sci Thechnol. 2011;2(2):1–5.

    Google Scholar 

  121. 121.

    Bekele D, Berhanu B, Pal M. Studies on the prevalence, cyst viability, organ distribution and public health significance of bovine cysticercosis in Ambo municipality abattoir, western Shoa, Ethiopia. J Parasitol Vector Biol. 2017;9(5):73–80.

    Google Scholar 

  122. 122.

    Berhanu D. Studies on the prevalence, cyst viability, organ distribution and public health significance of bovine cysticercosis at cattle slaughtered in Nekemte municipality abattoir, East Wollega, Ethiopia. J Biol Agri Healthc. 2017;7(9):59–67.

    Google Scholar 

  123. 123.

    Edao A, Dima FG, Deressa FB. Prevalence of bovine cysticercosis and status of human taeniasis in and around Asella town, Tiyo woreda, south east Ethiopia. Glob J Med Res. 2016;16:18–26.

    Google Scholar 

  124. 124.

    Korso L, Edao A. Prevalence of Cysticercosis bovis in Eastern Shoa of Oromia, Ethiopia. J Biol Agric Healthc. 2019;9(7):58–64.

    Google Scholar 

  125. 125.

    Emiru L, Tadesse D, Kifleyohannes T, Sori T, Hagos Y. Prevalence and public health significance of bovine cysticercosis at ELFORA abattoir, Bishoftu, Ethiopia. J Public Health Epidemiol. 2015;7(2):34–40.

    Article  Google Scholar 

  126. 126.

    Firew F, Moges N. Prevalence of bovine cysticercosis in cattle and zoonotic significance in Jimma town, Ethiopia. Acta Parasitol Glob. 2014;5:214–22.

    Google Scholar 

  127. 127.

    Ibrahim A, editor. Bovine cysticercosis in animals slaughtered in Nekemte municipality slaughter house. In: Ethiopian veterinary association proceedings of the 14th conference, Addis Ababa, Ethiopia; 2000.

  128. 128.

    Mame M, Amante M. Major parasitic causes of organ condemnation and economic loss in cattle slaughtered at Enango municipal abattoir, Western Ethiopia. J Anim Vet Adv. 2020;19(7):92–8.

    Google Scholar 

  129. 129.

    Megersa B, Tesfaye E, Regassa A, Abebe R, Abunna F. Bovine cysticercosis in cattle slaughtered at Jimma municipal abattoir, South western Ethiopia: prevalence, cyst viability and its socio-economic importance. Vet World. 2010;3(6):257–62.

    Article  Google Scholar 

  130. 130.

    Moje N, Zewde D, Bacha B, Regassa A. Metacestodes in cattle slaughtered at Shashemene municipal abattoir, southern Ethiopia: prevalence, cyst viability, organ distribution and financial losses. Glob Vet. 2014;12:129–39.

    Google Scholar 

  131. 131.

    Regassa F, Sori T, Dhuguma R, Kiros Y. Epidemiology of gastrointestinal parasites of ruminants in Western Oromia, Ethiopia. Int J Appl Res Vet Med. 2006;4(1):51–7.

    Google Scholar 

  132. 132.

    Tadesse A, Tolossa YH, Ayana D, Terefe G. Bovine cysticercosis and human taeniosis in South-west Shoa zone of Oromia Region, Ethiopia. Ethiop Vet J. 2013;17(2):121–33.

    Article  Google Scholar 

  133. 133.

    Tesfaye H. Prevalence, public health and financial importance of bovine cysticercosis in cattle slaughtered at Debre zeit municipal abattoir, Ethiopia. J Health Med Nurs. 2016;33:1–6.

    Google Scholar 

  134. 134.

    Tolosa T, Tigre W, Teka G, Dorny P. Prevalence of bovine cysticercosis and hydatidosis in Jimma municipal abattoir, South West Ethiopia. Onderstepoort J Vet Res. 2009;76(3):323–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  135. 135.

    Tolossa YH, Taha A, Terefe G, Jibat T. Bovine cysticercosis and human taeniosis in Adama town, Oromia region, Ethiopia. J Vet Sci Technol. 2015;S10(003):1–4.

    Google Scholar 

  136. 136.

    Abede W, Esayas G. Survey of ovine and caprine gastro-intestinal helminthosis in eastern part of Ethiopia during the dry season of the year. Rev Med Vet. 2001;152(5):379–84.

    Google Scholar 

  137. 137.

    Admasu Y, Tadesse T, Reta Z. Study on prevalence of small ruminant Cysticercus tenuicollis and its monetary loss at Bishoftu ELFORA export abattoir, Oromia, Ethiopia. J Dairy Vet Sci. 2019;9(2):555759.

    Google Scholar 

  138. 138.

    Ayele M, Ayele B, Belete A. Prevalence and associated risk factors of helminth parasites of small ruminants slaughtered at HELIMEX abattoir, Ethiopia. J Biol Agric Healthc. 2016;6(19):120–5.

    Google Scholar 

  139. 139.

    Guadu T, Akalu A, Fentahun T, Chanie M. Cysticercus tenuicollis: occurrence at Hashim nur’s meat export abattoir, Debre-Zeit, Ethiopia. Adv Biol Res. 2012;6(6):221–5.

    Google Scholar 

  140. 140.

    Mandefro A, Aragaw K, Hailu B, Alemayehu G, Chala G. Major cause of organ and carcass condemnation and its financial loss at Bishoftu ELFORA Export Abattoir. Int J Nutr Food Sci. 2015;4(3):364–72.

    Article  Google Scholar 

  141. 141.

    Mengistu FD, Belina D, Eshetu A. Prevalence of Coenurus cerebralis and its economic loss in small ruminants slaughtered at Bishoftu ELFORA export abattoir Ethiopia. Eur J Biol Sci. 2017;9(2):101–5.

    Google Scholar 

  142. 142.

    Samuel W, Zewde GG. Prevalence, risk factors, and distribution of Cysticercus tenuicollis in visceral organs of slaughtered sheep and goats in central Ethiopia. Trop Anim Health Prod. 2010;42(6):1049–51.

    PubMed  Article  Google Scholar 

  143. 143.

    Wondimu A, Abera D, Hailu Y. A study on the prevalence, distribution and economic importance of Cysticercus tenuicollis in visceral organs of small ruminants slaughtered at an abattoir in Ethiopia. J Vet Med Anim Health. 2011;3(5):67–74.

    Google Scholar 

  144. 144.

    Mekonnen K. Study on prevalence of Cysticercus bovis in cattle at municipal abbatoir of Kofale district, West Arsi zone, Oromia Regional State Ethiopia. J Biol Agric Healthc. 2017;7(17):1–17.

    Google Scholar 

  145. 145.

    Haile G. Major metacestodes of sheep and goats slaughtered at three selected export abattoirs in central Oromia: prevalence, cyst characterization, assessment of financial losses and public pwareness about metacestodes and their risk factors, MVSc. Thesis, Addis Ababa University, College of Veterinary Medicine and Agriculture; 2019.

  146. 146.

    Adem E, Alemneh T. Epidemiological studies on Cysticercus bovis at Gondar ELFORA abattoir, North West of Ethiopia. J Vet Sci Technol. 2016;7(5):2.

    Article  Google Scholar 

  147. 147.

    Cheru H, Zerihun T. Prevalence and public health significance of Cysticercus bovis in cattle slaughtered at Gondar ELFORA abattior. Biomed Nurs. 2017;3(2):56–63.

    Google Scholar 

  148. 148.

    Endris J, Negussie H. Bovine cysticercosis: prevalence, cyst viability and distribution in cattle slaughtered at Kombolcha ELFORA meat factory, Ethiopia. Am Eurasian J Agric Environ Sci. 2011;11(2):173–6.

    Google Scholar 

  149. 149.

    Engdaw TA, Alemneh AT, Ambaw ST. Study on the prevalence of Cysticercus bovis in Kombolcha ELFORA, North-Eastern Ethiopia. Eur J Appl Sci. 2015;7(4):152–7.

    Google Scholar 

  150. 150.

    Kassaw M, Belay W, Tesfaye W. Prevalence of Cysticercus bovis in cattle slaughterd at Kombolcha ELFORA meat processing factory, northern Ethiopia. Int J Curr Res Biol Med. 2017;2:1–6.

    Google Scholar 

  151. 151.

    Kebede N. Cysticercosis of slaughtered cattle in northwestern Ethiopia. Res Vet Sci. 2008;85(3):522–6.

    PubMed  Article  PubMed Central  Google Scholar 

  152. 152.

    Kinfe G, Admassu B, Getaneh G, Haile B. Study on the prevalence of bovine cysticercosis in Gondar ELFORA abattoir, Gondar, Ethiopia. World J Biol Med Sci. 2016;3:14–23.

    Google Scholar 

  153. 153.

    Mohammed N, Hailemariam Z, Mindaye S, Dewa D. Major causes of liver condemnation and associated financial loss at Kombolcha ELFORA abattoir, South Wollo, Ethiopia. Eur J Appl Sci. 2012;4(4):140–5.

    Google Scholar 

  154. 154.

    Tamirat B, Tamirat H, Gebru M. Prevalence, financial impact and public health significance of Cysticercus bovis at Bahir Dar municipal abattoir, Ethiopia. J Vet Med Anim Health. 2018;10(1):14–20.

    Article  Google Scholar 

  155. 155.

    Tefera Y, Mesfin Z, Muleta W. Major causes and abnormalities of organ condemnation and financial loss in cattle slaughtered at Dessie municipal abattior North Eastern Ethiopia. J Vet Med Anim Health. 2016;8(7):56–63.

    Article  Google Scholar 

  156. 156.

    Tegegne A, Hiko A, Elemo KK. Bovine cysticercosis and human taeniasis: animal–human health and economic approach with treatment trends in Kombolcha town, Wollo, Ethiopia. Int J One Health. 2018;4:15–21.

    Article  Google Scholar 

  157. 157.

    Wondimagegnei K, Belete S. Prevalence and public health significance of Cysticercus bovis in and around Debreberhan city. Eur J Appl Sci. 2015;7:199–208.

    Google Scholar 

  158. 158.

    Yalew K, Tassew A, Legesse K. Major causes of organ condemnation and assessment of its financial loss in cattle slaughtered at Bahir Dar municipal abattoir, Northwestern Ehtiopia. Food Sci Qual Mgt. 2017;69:27–33.

    Google Scholar 

  159. 159.

    Yigizaw G, Tefera Y, Tintagu T. Prevalence of Cysticercus bovis at Dessie municipal abattoir, north east Ethiopia. Abyssinia J Sci Technol. 2017;2(1):25–9.

    Google Scholar 

  160. 160.

    Gessese AT, Mulate B, Nazir S, Asmare A. Major metacestodes in small ruminants slaughtered at Dessie municipal abattoir, Eastern Ethiopia: prevalence, cyst viability, organ distribution and economic implications. Comp Clin Path. 2015;24(3):659–68.

    Article  Google Scholar 

  161. 161.

    Abunna F. Prevalence, organ distribution, viability and socioeconomic implication of bovine cysticercosis/teniasis, Ethiopia. Rev Elev Med Vet Pays Trop. 2013;66:25–30.

    Article  Google Scholar 

  162. 162.

    Hirpha A, Bekele T, Melaku M. Study on bovine cysticercosis with special attention to its prevalence, economic losses and public health significance in and around Halaba Kulito town, south Ethiopia. World J Agric Sci. 2016;12(4):299–307.

    Google Scholar 

  163. 163.

    Regassa A, Abunna F, Mulugeta A, Megersa B. Major metacestodes in cattle slaughtered at Wolaita Soddo municipal abattoir, Southern Ethiopia: prevalence, cyst viability, organ distribution and socioeconomic implications. Trop Anim Health Prod. 2009;41(7):1495–502.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  164. 164.

    Tesfaye D, Sadado T, Demissie T. Public health and economic significance of bovine cysticercosis in Wolaita Soddo, southern Ethiopia. Glob Vet. 2012;9:557–63.

    Google Scholar 

  165. 165.

    Ibrahim N, Zerihun F. Prevalence of Tania saginata cysticercosis in cattle slaughtered in Addis Ababa municipal abattoir, Ethiopia. Glob Vet. 2012;8:467–71.

    Google Scholar 

  166. 166.

    Kebede N, Tilahun G, Hailu A. Current status of bovine cysticercosis of slaughtered cattle in Addis Ababa abattoir, Ethiopia. Trop Anim Health Prod. 2009;41(3):291–4.

    PubMed  Article  Google Scholar 

  167. 167.

    Kebede N, Tilahun G, Hailu A. Development and evaluation of indirect hemagglutination antibody test (IHAT) for serological diagnosis and screening of bovine cysticercosis in Ethiopia. SINET Ethiop J Sci. 2008;31(2):135–40.

    Google Scholar 

  168. 168.

    Bayu Y, Asmelash A, Zerom K, Ayalew T. Prevalence and economic importance of liver parasites: Hydatid cyst, Fasciola species and Cysticercus tenuicolis in sheep and goats slaughtered at Addis Ababa abattoir enterprise in Ethiopia. J Vet Med Anim Health. 2013;5(1):1–7.

    Google Scholar 

  169. 169.

    Terefe Y, Redwan F, Zewdu E. Bovine cysticercosis and its food safety implications in Harari People’s National Regional State, eastern Ethiopia. Onderstepoort J Vet Res. 2014;81(1):1–6.

    Article  Google Scholar 

  170. 170.

    Disassa H, Ahmednur M, Jaleta H, Zenebe T, Kebede G. Major cause s of organ condemnation and its financial losses in cattle slaughtered at Dire Dawa municipal abattoir, Eastern Ethiopia. Acad J Anim Dis. 2015;4(3):118–23.

    Google Scholar 

  171. 171.

    Mekuria E, Shimelis S, Bekele J, Sheferaw D. Sheep and goats Cysticercus tenuicollis prevalence and associated risk factors. Afr J Agric Res. 2013;8(24):3121–5.

    Google Scholar 

  172. 172.

    Biruk W. Prevalence of bovine cysticercosis at Jijiga municipal abattoir, Ethiopia. J Vet Sci Technol. 2017;8(3):1–4.

    Google Scholar 

  173. 173.

    Sissay MM, Uggla A, Waller PJ. Prevalence and seasonal incidence of larval and adult cestode infections of sheep and goats in eastern Ethiopia. Trop Anim Health Prod. 2008;40(6):387–94.

    PubMed  Article  Google Scholar 

  174. 174.

    Jobre Y, Lobago F, Tiruneh R, Abebe G, Dorchies P. Hydatidosis in three selected regions in Ethiopia: an assessment trial on its prevalence, economic and public health importance. Rev Méd Vét. 1996;147(11):797–804.

    Google Scholar 

  175. 175.

    Kebede N, Abuhay A, Tilahun G, Wossene A. Financial loss estimation, prevalence and characterization of hydatidosis of cattle slaughtered at Debre Markos municipality abattoir, Ethiopia. Trop Anim Health Prod. 2009;41(8):1787–9.

    PubMed  Article  PubMed Central  Google Scholar 

  176. 176.

    Wen H, Yang WG. Public health importance of cystic echinococcosis in China. Acta Trop. 1997;67:133–45.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  177. 177.

    Wahlers K, Menezes CN, Wong ML, Zeyhle E, Ahmed ME, Ocaido M, et al. Cystic echinococcosis in sub-Saharan Africa. Lancet Infect Dis. 2012;12:871–80.

    PubMed  Article  PubMed Central  Google Scholar 

  178. 178.

    Humphrey DM, Domenica M, Eliningaya JK, Rebecca W, Ladslaus LM, Jorg H. Epilepsy and tropical parasitic infections in sub-Saharan Africa: a review. Tanzan J Health Res. 2013;15(2):1–21.

    Google Scholar 

  179. 179.

    WHO. The control of neglected zoonotic diseases: a route to poverty alleviation: report of a joint WHO (No. WHO/SDE/FOS/2006.1). World Health Organization; 2006.

  180. 180.

    Stojkovic M, Rosenberger K, Kauczor HU, Junghanss T, Hosch W. Diagnosing and staging of cystic echinococcosis: how do CT and MRI perform in comparison to ultrasound? PLoS Negl Trop Dis. 2012;6(10):e1880.

    PubMed  PubMed Central  Article  Google Scholar 

  181. 181.

    Eckert J, Deplazes P. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 2004;17(1):107–35.

    PubMed  PubMed Central  Article  Google Scholar 

  182. 182.

    Frider B, Larrieu E, Odriozola M. Long-term outcome of asymptomatic liver hydatidosis. J Hepatol. 1999;30(2):228–31.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  183. 183.

    Abunna F, Tilahun G, Megersa B, Regassa A, Kumsa B. Bovine cysticercosis in cattle slaughtered at Awassa municipal abattoir, Ethiopia: prevalence, cyst viability, distribution and its public health implication. Zoonoses Public Health. 2008;55(2):82–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  184. 184.

    Suarez HM, Santizo RM. Epidemiology of the Taenia saginata complex and C bovis in Ciego de Avila, province of Cuba. Rev Patolog Trop. 2005;34:43–52.

    Google Scholar 

  185. 185.

    Allan J, Avila G, Brandr J, Correa D, Del Brutto OH, Dorny P, et al. Guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. WHO/FAO/OIE guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. Paris, France; 2005. p. 150–6.

  186. 186.

    Praet N, Verweij JJ, Mwape KE, Phiri IK, Muma JB, Zulu G, et al. Bayesian modelling to estimate the test characteristics of coprology, coproantigen ELISA and a novel real-time PCR for the diagnosis of taeniasis. Trop Med Int Health. 2013;18:608–14.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  187. 187.

    Hajialilo E, Harandi MF, Sharbatkhori M, Mirhendi H, Rostami S. Genetic characterization of Echinococcus granulosus in camels, cattle and sheep from the south-east of Iran indicates the presence of the G3 genotype. J Helminthol. 2011;13:1–18.

    Google Scholar 

  188. 188.

    Regassa B. Review on hydatidosis in small ruminant and its economic and public health significance. J Dairy Vet Sci. 2019;11(2):1–8.

    Google Scholar 

  189. 189.

    Payne L, Fitchett JR. Bringing neglected tropical diseases into the spotlight. Trends Parasitol. 2010;26:421–64.

    PubMed  Article  PubMed Central  Google Scholar 

  190. 190.

    Hotez PJ, Kamath A. Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis. 2009;3:e412.

    PubMed  PubMed Central  Article  Google Scholar 

  191. 191.

    Temesgen F, Warkineh B. Biodiversity status and conservation challenges of protected areas of Ethiopia: Awash and Nechsar national parks in focus. J Nat Sci Res. 2018;8(5):46–61.

    Google Scholar 

  192. 192.

    Omer RA, Dinkel A, Romig T, Mackenstedt U, Elnahas AA, Aradaib E, et al. A molecular survey of cystic echinococcosis in Sudan. Vet Parasitol. 2010;169:340–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  193. 193.

    El Berbri I, Petavy AF, Umhang G, Bouslikhane M, Fassi Fihri O, Boué F, et al. Epidemiological investigations on cystic echinococcosis in North-West (Sidi Kacem Province) Morocco: infection in ruminants. Adv Epidemiol. 2015;2015:9.

    Article  Google Scholar 

  194. 194.

    Addy F, Alakonya A, Wamae N, Magambo J, Mbae C, Mulinge E, et al. Prevalence and diversity of cystic echinococcosis in livestock in Maasailand, Kenya. Parasitol Res. 2012;111(6):2289–94.

    PubMed  Article  PubMed Central  Google Scholar 

  195. 195.

    Fikire Z, Tolosa T, Nigussie Z, Kebede N. Prevalence and characterization of hydatidosis in animals slaughtered at Addis Ababa abattoir, Ethiopia. J Parasitol Vector Biol. 2012;4(1):1–6.

    Google Scholar 

  196. 196.

    Terefe D, Kebede K, Beyene D, Wondimu A. Prevalence and financial loss estimation of hydatidosis of cattle slaughtered at Addis Ababa abattoirs enterprise. J Vet Med Anim Health. 2012;4(3):42–7.

    Google Scholar 

  197. 197.

    Dawit G, Adem A, Simenew K, Tilahun Z. Prevalence, cyst characterization and economic importance of bovine hydatidosis in Mekelle municipality abattoir, Northern Ethiopia. J Vet Med Anim Health. 2013;5(3):87–93.

    Google Scholar 

  198. 198.

    Fromsa A, Jobre Y. Infection prevalence of hydatidosis (Echinococcus granulosus, Batsch, 1786) in domestic animals in Ethiopia: a synthesis report of previous surveys. Ethiop Vet J. 2011;15(2):11–33.

    Article  Google Scholar 

  199. 199.

    Ibrahim MM. Study of cystic echinococcosis in slaughtered animals in Al Baha region, Saudi Arabia: interaction between some biotic and abiotic factors. Acta Trop. 2010;113:26–33.

    PubMed  Article  PubMed Central  Google Scholar 

  200. 200.

    Cabrera PA, Irabedra P, Orlando D, Rista L, Haran G, Viñals G, et al. National prevalence of larval echinococcosis in sheep in slaughtering plants Ovis aries as an indicator in control programmes in Uruguay. Acta Trop. 2003;85:281–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  201. 201.

    Guorino ML, Cardoso DG, Clivio DF, Freire H, Gaudiano MJ, La Gamma G. Control of hydatiodosis in Uruguay. Vet Med Rev. 1981;1:47–57.

    Google Scholar 

  202. 202.

    Arene FO. Prevalence of hydatid cysts in domestic livestock in the Niger Delta. Trop Anim Health Prod. 1985;17:3–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  203. 203.

    Magambo J, Njoroge E, Zeyhle E. Epidemiology and control of echinococcosis in sub-Saharan Africa. Parasitol Int. 2006;55:S193–5.

    PubMed  Article  PubMed Central  Google Scholar 

  204. 204.

    Opara MN, Ukpong UM, Okoli IC, Anosike JC. Cysticercosis of slaughter cattle in southeastern Nigeria. Ann N Y Acad Sci. 2006;1081:339–46.

    PubMed  Article  PubMed Central  Google Scholar 

  205. 205.

    Kimari AM. Prevalence of bovine cysticercosis, taeniasis and associated zoonotic risk factors in Kajiado county, Kenya, MSc. Thesis, Egerton University; 2017.

  206. 206.

    Saratsis A, Sotiraki S, Braae UC, Devleesschauwer B, Dermauw V, Eichenberger RM, et al. Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in the Middle East and North Africa. Parasites Vectors. 2019;12(1):1–15.

    Article  Google Scholar 

  207. 207.

    Asmare K, Sibhat B, Abera M, Haile A, Degefu H, Fentie T, et al. Systematic review and meta-analysis of metacestode prevalence in small ruminants in Ethiopia. Prev Vet Med. 2016;129:99–107.

    PubMed  Article  PubMed Central  Google Scholar 

  208. 208.

    Desouky E, Badawy A, Refaat R. Survey on coenurosis in sheep and goats in Egypt. Vet Ital. 2011;47(3):333–40.

    PubMed  PubMed Central  Google Scholar 

  209. 209.

    Miran M, Nzalawahe J, Kassuku A, Swai E. Prevalence of coenurosis in sheep and goats at three slaughter slabs in Ngorongoro district, Tanzania. Trop Anim Health Prod. 2015;47(8):1591–7.

    PubMed  Article  PubMed Central  Google Scholar 

  210. 210.

    Sharma D, Chauhan P. Coenurosis status in Afro-Asian region: a review. Small Rumin Res. 2006;64(3):197–202.

    Article  Google Scholar 

  211. 211.

    Mulinge E, Odongo D, Magambo J, Njenga SM, Zeyhle E, Mbae C, et al. Diversity of Taenia and Hydatigera (Cestoda: Taeniidae) in domestic dogs in Kenya. Parasitol Res. 2020;119(9):2863–75.

    PubMed  Article  Google Scholar 

  212. 212.

    Dybicz M, Borkowski PK, Jonas M, Wasiak D, Malkowski P. First report of Echinococcus ortleppi in human cases of cystic echinococcosis in Poland. BioMed Res Int. 2019. https://doi.org/10.1155/2019/2474839.

    Article  PubMed  PubMed Central  Google Scholar 

  213. 213.

    Shi Y, Wan X, Wang Z, Li J, Jiang Z, Yang Y. First description of Echinococcus ortleppi infection in China. Parasites Vectors. 2019;12:398.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  214. 214.

    Correa F, Stoore C, Horlacher P, Jimenez M, Hidalgo C, Alvarez Rojas CA, et al. First description of Echinococcus ortleppi and cystic echinococcosis infection status in Chile. PLoS ONE. 2018;13(5):e0197620.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  215. 215.

    Rosenzvit MC, Zhang LH, Kamenetzky L, Canova SG, Guarnera EA, McManus DP. Genetic variation and epidemiology of Echinococcus granulosus in Argentina. Parasitol. 1999;118(5):523–30.

    CAS  Article  Google Scholar 

  216. 216.

    Zhang LH, Joshi DD, McManus DP. Three genotypes of Echinococcus granulosus identified in Nepal using mitochondrial DNA markers. Trans R Soc Trop Med Hyg. 2000;94(3):258–60.

    CAS  PubMed  Article  Google Scholar 

  217. 217.

    Harandi MF, Hobbs RP, Adams PJ, Mobedi I, Morgan-Ryan UM, Thompson RC. Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitology. 2002;125(04):367–73.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the scientific communities involved in those studies included in the SR.

Funding

This study was funded by the National Key Research and Development Plan (2017YFD0501301; 2018YFC1602504), Central Public-Interest Scientific Istitution Basal Research Fund (1610312017001; 1610312020016) and Cultivation of Achievements of State Key Laboratory of Veterinary Etiological Biology (SKLVEB2020CGPY01).

Author information

Affiliations

Authors

Contributions

NAS and WZJ conceived the study; NAS and JAO designed the research. NAS, JAO and MBG conducted study selection, data extraction and data analysis. WZJ, HBY and BQF supervised the study. All authors discussed and drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Wan-Zhong Jia.

Ethics declarations

Ethics approval and consent to participants

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

PRISMA 2009 checklist.

Additional file 2: Table S2.

Characteristics of studies included in the systematic review and meta-analysis (study subject: human). F, female; M, male; B = both male and female; Imm, immigrant; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 3: Table S3.

Distribution of data sets by animal intermediate hosts’ taeniasis and CE, Ethiopia. n, number of report; AA, Addis Ababa; Oro, Oromia; Tig, Tigray; SNNP, Southern Nation and Nationality of People; Amh, Amhara; Har, Harar; DD, Dire Dawa; Som, Somali; *some papers reported more than one parasite hence multiple datasets.

Additional file 4: Table S4.

Characteristics of studies included in the systematic review and meta-analysis (study subject: cattle). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 5: Table S5.

Characteristics of studies included in the systematic review and meta-analysis (study subject: sheep). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 6: Table S6.

Characteristics of studies included in the systematic review and meta-analysis (study subject: goat). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 7: Table S7.

Characteristics of studies included in the systematic review and meta-analysis (study subject: camel). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 8: Table S8.

Characteristics of studies included in the systematic review and meta-analysis (study subject: pig). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 9: Table S9.

Characteristics of studies included in the systematic review and meta-analysis (study subject: final hosts). F, female; M, male; B = both male and female; CS, cross sectional; p, prevalence; CI, confidence interval.

Additional file 10: Figure S1.

Overall prevalence of cystic echinococcosis evidenced by forest plot. Prev, prevalence; CI, confidence interval; *same study; **same name of first authors.

Additional file 11: Table S10.

Pooled prevalence of Taenia and Echinococcus infections in intermediate and final hosts by region, Ethiopia.

Additional file 12: Figure S2.

Publication bias evidenced by funnel plots for overall prevalence of cystic echinococcosis. Prev, prevalence.

Additional file 13: Figure S3.

Publication bias evidenced by funnel plots for overall prevalence of dog echinococcosis. Prev, prevalence.

Additional file 14: Figure S4.

Publication bias evidenced by funnel plots for overall prevalence of taeniasis. Prev, prevalence.

Additional file 15: Figure S5.

Publication bias evidenced by funnel plots for overall prevalence of T.saginata (C. bovis). Prev, prevalence.

Additional file 16: Figure S6.

Publication bias evidenced by funnel plots for overall prevalence of T. hydatigena. Prev, prevalence.

Additional file 17: Figure S7.

Publication bias evidenced by funnel plots for overall prevalence of T. ovis. Prev, prevalence.

Additional file 18: Figure S8.

Publication bias evidenced by funnels plots for overall prevalence of T. multiceps. Prev, prevalence.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shumuye, N.A., Ohiolei, J.A., Gebremedhin, M.B. et al. A systematic review and meta-analysis on prevalence and distribution of Taenia and Echinococcus infections in Ethiopia. Parasites Vectors 14, 447 (2021). https://doi.org/10.1186/s13071-021-04925-w

Download citation

Keywords

  • Cystic echinococcosis
  • Taeniasis
  • Cysticercosis
  • Epidemiology
  • Risk factors
  • Ethiopia