Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in the Middle East and North Africa

Background The zoonotic parasite Taenia saginata utilizes bovines as an intermediate host (causing cysticercosis) and humans as the definitive host (causing taeniosis). The public health burden of T. saginata is assumed to be low, but the economic burden is large, due to the resources utilized in the detection and condemnation of infected carcasses and carcass parts. As part of a collaborative effort to synthesize worldwide epidemiological data on this parasite, we present here the results of a systematic review on the distribution of T. saginata taeniosis and bovine cysticercosis in the Middle East and North Africa (MENA). Methods Information on the occurrence and prevalence of T. saginata taeniosis and cysticercosis in the MENA region was obtained through a systematic review of published and grey literature, including OIE reports, published between January 1st, 1990 and December 31st, 2017. Results A total of 63 publications were retrieved across the 21 MENA countries. Taenia saginata taeniosis was reported in 11 of these countries, whereas unspecified taeniosis was reported for a further seven. Microscopy-based prevalence values ranged between 0.02–8.6%. Bovine cysticercosis prevalence estimates based on meat inspection were only reported for Egypt and Israel, with prevalence data ranging between 0.2–20% and 0.1–9.1% for cattle and buffaloes, respectively. The presence of bovine cysticercosis could be confirmed for 10 additional countries through OIE reports. Conclusions Human taeniosis occurrence was confirmed for 86% (18/21) of the countries in the MENA region, although in several of these countries the species responsible was not specified. Religious prohibitions on the consumption of pork and the limited extent of pig farming across much of this region, however, suggest that many reported taeniosis cases are likely to be attributable to T. saginata rather than Taenia solium or Taenia asiatica. There was a paucity of data regarding both the prevalence and economic impact of bovine cysticercosis. More detailed epidemiological data on both T. saginata taeniosis and bovine cysticercosis could be obtained by adopting an integrated “One Health” approach, considering the characteristics (e.g. ecosystem related and sociopolitical aspects) of the MENA region. Compared with more conventional approaches, this could lead to an enhanced performance and cost-effectiveness of surveillance systems. Electronic supplementary material The online version of this article (10.1186/s13071-019-3339-5) contains supplementary material, which is available to authorized users.


Background
The Middle East and North Africa (MENA) is situated at the natural crossroads of three continents and has significantly contributed to the development of flourishing civilizations, the expansion of maritime empires, and the spread of three of the major religions of the world [1]. Early animal domestication in the area, which, based on Neolithic fossils, dates back to 6000 B.C., led to an early close relationship between people and domestic animals, providing an ideal interface for the development of zoonoses [2]. Indeed, paleoparasitological studies in the area have confirmed that zoonoses (e.g. taeniosis) were established here in ancient times [3][4][5]. In addition, in recent decades numerous zoonoses have emerged or reemerged in this part of the world [6][7][8][9], which to some extent can be explained by socioeconomic changes, conflicts, and political instability, all of which have resulted in fragile healthcare systems (limited laboratory and clinical capacities), increased human and animal mobility (travel, displacement, and lack of stringent animal import regulations), gaps in the knowledge of risk factors for transmission of emerging infections, and surveillance systems being unable to address early detection and rapid response. Furthermore, climate change-driven ecosystem fragility (arid regions, desertification, water scarcity) further impacts the situation [10]. Additionally, some of the petroleum-rich countries in the Arabian Peninsula represent attractive migratory destinations for tens of millions of economic migrants from neighboring regions such as South Asia or East Africa [11].
Taenia saginata, the beef tapeworm, is an important cyclo-zoonotic cestode with a worldwide distribution. The hermaphrodite adult tapeworm develops in the human intestine and produces tens of thousands of eggs that are either excreted free or within intact, motile, proglottids in the faeces [12]. The eggs are able to survive for several months in the environment [13]. Bovids, typically cattle and buffaloes, which are of particular importance in the MENA region, are the natural intermediate hosts of the parasite, and are infected by ingestion of eggs. The oncosphere migrates via the bloodstream to striated muscles, where the metacestode larval stage (cysticercus) develops. The success and widespread distribution of this parasite can be associated with a range of factors including dietary habits (consumption of raw or undercooked cysticerci-infected meat), leisure activities in close proximity to grazing areas, free access of cattle to surface water, and sanitary education level of the farm workers, as well as inadequate treatment and disposal of sewage [14][15][16][17].
Although T. saginata taeniosis is characterized by mild, or absence of clinical symptoms, rare complications such as gangrenous cholecystitis, cholangitis, abdominal discomfort and acute appendicitis have been described (reviewed in [18]). Thus, the major burden of this parasite is upon the meat industry, where considerable economic losses occur due to the cost of meat inspection, carcass condemnation in cases of heavy infections, and obligatory freezing, heating, or irradiation in cases of light infections, along with additional transport or even insurance costs in some countries [19,20]. The bovine population of the MENA region is huge, with Sudan, Egypt, Algeria, Yemen, and Syria, sorted by population rank in descending order based on 2016 data, counting among the top-producing countries in the region with an approximate population reaching almost 45 million head (including buffaloes, which are of relevance for Egypt), more than 66% of which are kept in Sudan [21]. Both traditional and modernized bovine production systems are found in the MENA region. The traditional systems mainly cater for nomadic producers (extensive production system/mainly meat oriented) or producers who have settled in close vicinity to cities/irrigated agricultural areas and rely on crop residues. Modernized systems largely serve intensively reared dairy cattle of both local and imported breeds [22].
This review provides a systematic overview of the epidemiology of T. saginata and bovine cysticercosis in the MENA region. To the best of our knowledge, an article addressing this cestode in the MENA region has not previously been published.

Search strategy
This systematic review was conducted according to the PRISMA guidelines (Additional file 1) and focused on the region of Middle East and North Africa [23], specifically the countries: Algeria, Cyprus, Egypt, Iraq, Israel, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Palestine, Qatar, Saudi Arabia, South Sudan, Sudan, Syria, Tunisia, United Arab Emirates (UAE), Western Sahara and Yemen. It utilized records relating to the occurrence, prevalence, and geographical distribution of human taeniosis due to T. saginata and bovine cysticercosis for the period between the 1st of January 1990 and 31st of December 2017. A specific combination of Keywords: Beef tapeworm, Bovine cysticercosis, Cestode, Foodborne parasites, Middle East, MENA, North Africa, Taenia saginata, Taeniosis search words was used to search both for published papers and grey literature (MSc/PhD theses, reports etc.) in two international bibliographic databases (Pub-Med and opengrey.eu). The search term was as follows: (cysticerc* OR cisticerc* OR "C. bovis" OR taenia* OR tenia* OR saginata OR taeniosis OR teniosis OR taeniasis OR ténia OR taeniid OR cysticerque) AND (above-mentioned countries separated by the operator "OR"). In addition, WHO IRIS (http://apps.who.int/ iris/) and Index Medicus for the Eastern Mediterranean Region (IMEMR) (http://www.emro.who.int/infor matio n-resou rces/imemr -datab ase/) were searched by using a combination of three search words (i.e. Taenia and saginata or cysticercus), which cannot be further extended due to the limitation in the number of search words to be used by those databases. A late stage search was also conducted using the Google search engine and aimed specifically at trying to identify documents for countries for which the previous approaches had provided no or only very few records. Finally, data on both occurrence and number of bovine cysticercosis cases, whenever available, were also retrieved from OIE interfaces HANDISTATUS II (http://web.oie.int/hs2/repor t.asp?lang=en), and WAHIS (http://www.oie.int/wahis _2/publi c/wahid .php/Disea seinf ormat ion/statu sdeta il), which provide data for the periods between 1994-2004 and 2005 until the end of the study period, respectively.

Selection criteria, data extraction
Retrieved records were first screened to exclude duplicates. Subsequently, titles and abstracts of all unique records were screened for their relevance to the scope of the review. This was done based on the following list of exclusion criteria (Additional file 2): (i) publication date before 1990 or after 2017; (ii) studies concerning a parasite other than T. saginata; (iii) studies reporting data from countries other than those listed in the MENA region; (iv) studies providing information other than the scope of the review question (occurrence, prevalence, and geographical distribution of T. saginata taeniosis and bovine cysticercosis).
If it was not possible to determine the eligibility of a document from the abstract and title only, the full text was screened. Full texts, including relevant citations therein, were then retrieved where possible and evaluated by the same criteria as above. Data were extracted into tables that are presented in Tables 1-4. Prevalence data were only extracted if both the numerator and the denominator were provided, and 95% confidence intervals were calculated based on the Clopper and Pearson method.

Search results
Literature search of all four databases for the 21 MENA countries returned 823 results, of which 21 were duplicates (Fig. 1). Subsequent screening of titles and abstracts limited the number of records to 55 in line with the selection criteria. For two of these, full texts could not be retrieved. However, data in the abstracts of these articles were sufficient for prevalence calculation. Eight records were additionally retrieved through citations in the above papers (4 records) and the late stage search (4 records), resulting in a total number of 63 records to be screened. A total of 58 records reported on taeniosis presence/ prevalence and 8 on bovine cysticercosis prevalence, with 3 of them reporting on both. However, data regarding human taeniosis in one of the above three records were inconsistent and could not be considered. Most studies were from Egypt (n = 19), followed by Sudan (n = 7), Lebanon (n = 6), and Saudi Arabia (n = 5).

Human taeniosis occurrence
Of the 58 records reporting the presence/prevalence of taeniosis, 5 were case reports, whereas 53 reported infection prevalence in particular study groups, such as schoolchildren, immigrants, refugees, housemaids, food handlers, or groups presenting a certain health condition (e.g. abdominal pain, diarrhea, appendicitis) and its relation to parasitism. The age of participants ranged between 1-90 years. Diagnosis was based mainly on microscopy of stool samples (e.g. wet smears, concentration and/or flotation methods) and/or microscopy-based proglottid identification. However, it was not always apparent from the articles if and how species identification was performed. In a single record from Egypt, T. saginata was confirmed using molecular methods [24].
Individual case reports confirmed the presence of T. saginata taeniosis in Lebanon, Morocco and Sudan, and an unspecified taeniosis case was described from Syria ( Table 1). The remaining population-based prevalence studies confirmed the occurrence of unspecified taeniosis in seven countries, namely Iraq, Israel, Kuwait, Oman, South Sudan, Syria and UAE (Table 2). Taenia saginata taeniosis was reported from the following countries (11 in total): Algeria, Egypt, Jordan, Lebanon, Libya, Morocco, Palestine, Saudi Arabia, Sudan, Tunisia and Yemen (Table 2). Taenia spp. infections were not detected in two studies from Qatar with sample sizes of 1737 and 9208 respectively, whereas in the Republic of Cyprus, T. saginata is considered to be eliminated [25]. For Western Sahara, relevant data could not be retrieved from the databases. Thus, evidence for the presence of human Taenia spp. infections could be found for 18 out of 21 MENA countries for the study period between 1990 and 2017, with 11 of them specifically indicating T. saginata infections (Fig. 2). Microscopy-based prevalence values ranged between 0.02-8.6%.

Bovine cysticercosis
Prevalence data from Egypt (7 records) and Israel (1 record) were found upon database screening or elsewhere (Table 3). Data from Egypt derived from six different governorates situated along the Nile and a large-scale study included data from all official abattoirs (6,160,982 slaughtered cattle and buffaloes from 1994 to 1997). An additional large-scale study from an abattoir in the south of Israel provided prevalence data over a considerable study period  and number of slaughtered cattle, i.e. 629,549 animals. For the remaining 19 MENA countries, data on the prevalence of bovine cysticercosis could not be obtained, even from Sudan that has one of the highest cattle populations globally. However, as previously mentioned, the parasite has apparently been eradicated from the Republic of Cyprus [25].
Although meat inspection-based prevalence data are provided in the eight published studies on bovine cysticercosis, in two of the studies from Egypt, antibody-ELISA (infection prevalence of 29.3%) and molecular identification of tissue cysts by PCR, sequencing and phylogenetic analysis were also performed. Bovine cysticercosis prevalence was determined for both cattle and buffaloes in five studies from Egypt, only for cattle in one study from Egypt and one from Israel, and one study from Egypt solely focused on buffaloes. Bovine cysticercosis prevalence for cattle based on meat inspection ranged between 0.2-20%. For buffaloes, lower prevalence values, ranging between 0.1-9.1% were observed. Interestingly, three studies [26][27][28] reported considerably higher infection rates in imported than native cattle. In Israel this was connected to extensive import of cattle from Australia after 1998 (more than 500,000 imported cattle between 1998 and 2007, 95% of which originated from Australia), which seems to have contributed to cysticercosis outbreaks, whereas in a study from Egypt all imported animals were of Sudanese origin. In addition, two studies reported higher infection rates in older animals, particularly females [27,29].
In addition to Egypt and Israel, bovine cysticercosis presence could be further confirmed based on OIE reports for the following countries: Algeria, Jordan, Lebanon, Morocco, Palestine, Saudi Arabia, Sudan/ South Sudan (data after South Sudan became independent in 2011 were not available), Tunisia and UAE (Table 4). Therefore, bovine cysticercosis presence could be confirmed for 12 out of the 21 MENA countries (Fig. 3).
For Iraq, Kuwait, Libya, Oman, Syria and Yemen, although unspecified Taenia spp. or T. saginata infections in humans were reported, OIE data do not indicate the presence of cysticercosis, although for some of those countries there is a considerable degree of underreporting. Neither T. saginata/Taenia spp. nor bovine cysticercosis records were found for Qatar and Western Sahara.

Discussion
The sparsity of data on T. saginata taeniosis and bovine cysticercosis in the MENA region prompted us to summarize existing knowledge. Based on data gathered through this systematic review, T. saginata taeniosis is definitely present across the MENA region, being reported in just over 50% (11/21) of the countries studied. Furthermore, human infections with unspecified Taenia spp. were found for an additional seven countries; thus, taeniosis occurs in most (86%; 18/21) of the countries of the MENA region. Because both pig farming and pork consumption are uncommon in many of the MENA countries (over 90% of the local population were registered as Muslim or Jewish in 2010 [30]), it is likely that unspecified taeniosis cases are mainly due to T. saginata, as was noted in some of the publications. However, recent data from the Arabian Peninsula indicate the presence of autochthonous Taenia solium transmission [31], potentially resulting in human neurocysticercosis. In addition, porcine cysticercosis due to T. solium has        been detected by meat inspection in 0.09% of slaughtered pigs in Egypt [26]. Some countries of the Arabian Peninsula are attractive destinations for millions of economic immigrants, some of whom come from T. solium-and/or Taenia asiatica-endemic countries, such as from south-/ southeast Asia and sub-Saharan Africa [11,[32][33][34][35]; thus, T. solium or T. asiatica taeniosis cannot be entirely excluded. As the results presented herein relied almost  exclusively on microscopy for monitoring parasitic infections in general, it is important to note that species differentiation by the application of appropriate methods, such as multiplex real-time PCR, would be essential in case of a history of pork consumption, given the morphological similarity between Taenia spp. eggs [36,37]. Diagnosis of intestinal parasites typically relies on the microscopic detection of transmission stages in human faecal samples which was also the result of our search, despite the enormous inter-and intra-country disparities (e.g. rural vs urban areas) in terms of healthcare infrastructure. Such data often result, especially to what taeniosis infections concerns, in prevalence underestimation because of the poor sensitivity of microscopy (e.g. due to the intermittent excretion of eggs) and the asymptomatic nature of infection (many infected individuals never get tested) [38]. The observed prevalence range (0.02-8.6%) based on microscopy studies conducted in the MENA region is comparable to that reported for southern/eastern Africa and the Americas, but the prevalence values were higher than those for the Russian Federation, western and eastern Europe [39][40][41][42][43]. However, comparison between studies is challenging due to their variability in design (variable factors including, for example, duration of study, inclusion of only certain target/age groups, different diagnostic methods used, randomization of participants, geographical coverage). The adoption of a consensus protocol for taeniosis surveillance purposes by clinical investigators such that bias is minimized is therefore highly recommended, as previously suggested [40].
The present review clearly demonstrates the lack of bovine cysticercosis-related epidemiological data and data on its possible economic impact for the MENA region. Meat inspection-based prevalence studies were available only for Egypt and Israel, confirming considerable infection rates, especially in imported cattle, but also native cattle and buffaloes. Moreover, bovine cysticercosis could be confirmed for a further 10 countries in the MENA region based on OIE data, thus demonstrating the presence of this infection in just over 50% of the countries considered, despite the widespread distribution of taeniosis in the region. Apart from a possible underestimation in the reported prevalence values for both Egypt and Israel due to the low sensitivity of visual meat inspection [44,45], lack of data and underreporting to OIE for the remaining countries strongly reflect the actual inconsistency in reporting systems. This might be attributed to the fact that bovine cysticercosis is not notifiable in many of those countries and to OIE.
The MENA region covers a wide diversity of environments, from wet coastal regions to high mountain plateaus and arid steppes and deserts in the interior. Around 2% of the region is considered to consist of humid areas and over 6% of the population live in these areas, while most of the region (85%) is considered to be arid or semiarid and approximately 23% of the population live in these areas [46]. The remaining population lives in both urban centers and intensively irrigated agricultural areas of the arid and semi-arid parts of the MENA region, where bovine rearing might also take place. Large-scale irrigated systems are primarily situated in Morocco and Libya, and along the Nile (South Sudan, Sudan, Egypt), Euphrates and Tigris rivers (Syria, Iraq). In addition, water scarcity in the region (only 1% of global freshwater resources are available in the MENA region) may be addressed by extensive wastewater reuse [46]. Such wastewater may not always be treated sufficiently so that all pathogens are efficiently eliminated; on average 43% of wastewater is treated in the MENA region [47]. For instance, a study from Morocco demonstrated Taenia spp. infections in children from areas where untreated wastewater irrigation was practiced, but this was not the case in control areas [48]. In some territories, such as in Palestine, sewage channels are often open, and thus prone to flooding [49,50]. This may increase the risk of animals coming into contact with pathogens in human sewage, such as Taenia eggs, and cattle or buffaloes contracting bovine cysticercosis [49]. Even in cases (e.g. in Tunisia) where sewage/wastewater is treated, Taenia spp. eggs could not be efficiently eliminated [51], whereas in some cases Taenia spp. eggs were even found in drinking water, such as in Iraq [52]. Considering both the significant cattle and buffalo population, as well as the specific geographic, environmental and demographic characteristics of the area, efforts should be directed towards obtaining more detailed prevalence-based data by considering relevant aspects on the human, animal and ecosystem interface from a One-Health perspective. This would constitute the basis for the development of models predicting possible spatiotemporal transmission clusters and high-risk areas.
Globalization poses an increased threat for the spread of, among others, foodborne pathogens, including the agents of cysticercosis/taeniosis via the international movement of people, animals, and their products, and potentially contaminated produce or other fomites from endemic regions. This was also evident for the MENA region, where the import of live cattle from Australia to Israel after 1998 seems to have contributed to cysticercosis outbreaks in this country [28]. Additionally, the prevalence of cysticercosis infection was higher in imported cattle than native cattle in two studies from Egypt [26,27]. Sudan and Brazil were the biggest suppliers of live cattle to Egypt during 2017 (approximately 250,000 head, mainly intended for immediate slaughter), whereas exports of chilled beef from the USA to Lebanon reached a value of $3.2 million in 2015 [53,54]. Given that the cysticercosis infection rates in Brazilian cattle range from very low levels to 18.8% [40], import of such high numbers implies that some infected cattle will be imported. The role of mass religious gatherings, such as the annual Hajj pilgrimage to Mecca in Saudi Arabia, where thousands of live animals, including cattle, are imported from various neighboring countries, slaughtered, and prepared for consumption, poses both a real zoonotic risk and a considerable challenge for local veterinary and medical authorities [6,55]. The role of such socio-cultural events in the epidemiology of taeniosis should not be underestimated and deserves further attention. It was, for instance, previously demonstrated that the Eid al-Adha (the second of two great Muslim festivals, the other being Eid al-Fitr) celebration in Kosovo might contribute to an increased annual incidence of canine echinococcosis [56]. Certain culinary habits from the MENA region, potentially promoting T. saginata infection, include the consumption of raw, smoked, salted or dried beef products, with the most characteristic representative of the Lebanese and Levantine (Levant is an approximate historical geographical term, referring to a large area in the Eastern Mediterranean) cuisine being "Kibbeh nayyeh", which is prepared using minced raw beef [57,58]. A further example of how cysticercosis epidemiology could potentially be affected by globalization is also the recent boycott against Qatar by neighboring countries. This has stimulated a massive import of cattle from various other countries in order for the country to cover its milk needs [59]. The above facts highlight the need for the development of sensitive diagnostic tests that efficiently detect infected animals or carcasses, and evaluation of their application in the international live cattle and chilled beef trades [20,44,60]. Currently, apart from meat inspection, only antigen-based ELISA tests are capable of detecting infective (live) cysticerci, and the reduced sensitivity in light infections may mean that some infections would go undetected [20,44,45]. Harmonization of the legislation scheme underlying international bovine/beef trade with regard to ensuring only the entrance of bovine cysticercosis-free chilled meat in the food chain/or live animals, would be an additional necessary act complementary to the respective national preventive, antemortem, and post mortem control measures.

Conclusions
The present review demonstrates the widespread distribution of T. saginata taeniosis in the MENA region. However, both prevalence and distribution data, as well as economic burden data, on bovine cysticercosis are largely unavailable. Therefore, complementary to the application of appropriate control measures covering the whole spectrum of "primary production-to-consumption" food chain continuum, efforts should be directed towards obtaining more detailed epidemiological data for both T. saginata taeniosis and bovine cysticercosis. This would enable identification of probable transmission routes by considering possible risk factors (such as wastewater reuse and animal trade). Taenia saginata control and elimination offers ground for an integrated "One Health" approach, thus interdisciplinary collaboration between health, agricultural, and environmental authorities of all countries in the MENA countries should be further encouraged. Epidemiological evidence to support decisions on appropriate interventions to be applied could be significantly improved by such an approach.