Advertisement

Parasites & Vectors

, 12:113 | Cite as

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

  • Anastasios SaratsisEmail author
  • Smaragda Sotiraki
  • Uffe C. Braae
  • Brecht Devleesschauwer
  • Veronique Dermauw
  • Ramon M. Eichenberger
  • Lian F. Thomas
  • Branko Bobić
  • Pierre Dorny
  • Sarah Gabriël
  • Lucy J. Robertson
Open Access
Review
Part of the following topical collections:
  1. Global distribution of Taenia saginata

Abstract

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.

Keywords

Beef tapeworm Bovine cysticercosis Cestode Foodborne parasites Middle East MENA North Africa Taenia saginata Taeniosis 

Abbreviations

B.C.

Before Christ

CI

Confidence interval

IMEMR

Index Medicus for the Eastern Mediterranean Region

MENA

Middle East and North Africa

GOOSE

World Organization for Animal Health/Office International des Epizooties

UAE

United Arab Emirates

WHO

World Health Organization

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 re-emerged 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.

Methods

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 search words was used to search both for published papers and grey literature (MSc/PhD theses, reports etc.) in two international bibliographic databases (PubMed 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/information-resources/imemr-database/) 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/report.asp?lang=en), and WAHIS (http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/statusdetail), 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 14. 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.

Results

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%.
Table 1

Taenia saginata or Taenia spp. taeniosis case reports

Country (city)

No. of cases

Age

Species

Diagnosis

Reference

Lebanon (Tripoli)

1

69

T. saginata

Proglottid identification of the part of tapeworm found in the peritoneal exudate after jejunal perforation

[61]

Morocco (Rabat)

1

63

T. saginata

Tapeworm detection during capsule endoscopy. Proglottid identification after post-treatment elimination

[62]

Sudan (Khartoum)

1

50

T. saginata

Part of a tapeworm found in jejunostomy leak after esophagectomy

[63]

Sudan (flame)

1

43

T. saginata

Proglottid identification of vomited part of a tapeworm

[64]

Syria (Allepo)

1

70

Taenia spp.

Tapeworm detection during esophagogastroduodenoscopy

[65]

Table 2

Prevalence of taeniosis in humans based on cross-sectional or retrospective studies

Country

Timeframe

Location of study

Age range tested

No. positive/total no. of people tested

Prevalence (%)

(95% CI)

Species

Technical diagnosis

Ref

Algeria

12/2010–11/2011

Oran

1–80

1/1042

0.1

(<0.01–0.5)

T. saginata

Microscopy

[66]

Egypt

on

Sohag (Sohag Governorate)

12–90

5/150

3.2

(1.0–7.3)

Taenia spp.

Microscopy

[67]

Egypt

09/2013–08/2014

Sohag (Sohag Governorate)

1–14

1/100

1.0

(0.03–5.5)

Taenia spp.

Microscopy

[68]

Egypt

01/2009–12/2009

Qalyubia, Dakahlia and Damietta Governorates

1– >40

2/105

1.9

(0.2–6.7)

Taenia spp.

Microscopy

[69]

Egypt

12/2005–12/2006

Mansoura (Dakahlia Governorate)

on

37/3180

1.1

(0.8–1.6)

T. saginata

Microscopy

[70]

Egypt

01/2005–01/2006

Mansoura and Gogar (Dakahlia Governorate)

20–40

2/2000

0.1

(<0.01–0.4)

T. saginata

Microscopy (including proglottid identification)

[71]

Egypt

on

Qalyub (Qalyubia Governorate)

6–12

2/486

0.4

(0.05–1.5)

T. saginata

Microscopy

[72]

Egypt

on

Sennores (El-Fayum Governorate)

6–12

3/252

1.2

(0.3–3.4)

T. saginata

Microscopy (including proglottid identification)

[73]

Egypt

on

Ashmoun, Tala, Berket El Sabaa Shebeen El Koom, Menouf (Menoufia Governorate)

<10– >50

2/565

0.4

(0.05–1.4)

Taenia spp.

Microscopy

[74]

Egypt

05/2006–06/2007

El-Eman, El-Matieea, El-Ezeia (Assiut Governorate)

on

2/325

0.6

(0.07–2.2)

T. saginata

Microscopy

[29]

Egypt

01/2001–12/2008

Alexandria, Ismailia (Alexandria and Ismailia Governorates)

1–17

8/1500

0.5

(0.2–1.0)

T. saginata

on

[75]

Egypt

on

El-Ghanayem (Assiut Governorate)

6–11

1/400

0.3

(<0.01–1.4)

T. saginata

on

[76]

Egypt

01/2014–12/2014

Benha (Qalyubia Governorate)

20–55

6/100

6.0

(2.2–12.6)

T. saginata

Microscopy (including proglottid identification) and molecular confirmation

[24]

Iraq

04/1988–03/1989

Kirkuk area (Al-Tameem/Kirkuk Governorate)

6–12

9/1681

0.5

(0.25–1.0)

Taenia spp.

Microscopy

[77]

Israel

on

on

on

3/93

3.2 of a

(0.7-9.1)

Taenia spp.

on

[78]

Israel

2007–2011

Beer Sheva (Negev region)

0–19

8/45,978

0.02b

(0.008-0.03)

Taenia spp.

Microscopy

[79]

Jordan

2009–2013

Irbid, Jerash and Ajlun

All age groups

48/21,906

0.2

(0.2–0.3)

Taenia spp.

Microscopy

[80]

Jordan

07/1987–07/1988

Irbid

on

1/283

0.4

(<0.01–2.0)

T. saginata

Microscopy

[81]

Kuwait

on

Kuwait

1– >40

1/1674

0.06

(<0.01–0.3)

Taenia spp.c

Histology of appedenctomy sections

[82]

Kuwait

01/1986–12/1986

Six general hospitals (Adan, Amiri, Mubarak, Jahra, Farwaniya and Infectious Diseases)

1–69

17/6000

0.3

(0.2–0.5)

Taenia spp.

Microscopy

[83]

Lebanon

01/1997–12/1998 & 01/2007–12/2008

Beirut

on

116/14,771

0.8d

(0.7–0.9)

Taenia spp.

Microscopy

[84]

    

27/7477

0.4e

(0.2-0.5)

   

Lebanon

1997–2001

Tripoli

<5– >66

188/17,126

1.1

(1.0–1.3)

Taenia spp.

Microscopy

[85]

Lebanon

on

Tripoli, Beirut

on

2479/44,864

5.5

(5.3–5.7)

Taenia spp.

Microscopy

[86]

Lebanon

1995–1997

Beirut

14–71

on

Either 0.8 (0.5–1.3) or 0.4f

Taenia spp

Microscopy

[87]

Lebanon

05/2004–09/2004

North Lebanon (Akkar Governorate)

16–50

1/308

0.3

(<0.01–1.8)

Taenia spp.

Microscopy

[88]

Libya

03/2004–06/2004

Tripoli

5–18

1/50

2.0

(0.05–10.7)

T. saginata

Microscopy

[89]

Morocco

1996–2005

Kenitra

on

6/4285

0.14

(0.05–0.3)

T. saginata

Microscopy

[90]

Morocco

on

Me Mellal

7–14

4/740

0.5g

(0.2–1.4)

Taenia spp

Microscopy

[48]

    

0/603

0h

(0-0.6)

   

Oman

09/2004–03/2005

Dhahira Governorate

9–10

8/436

1.8i

(0.8-3.6)

Taenia spp

Microscopy

[91]

Oman

on

Dhofar Governorate (Dhalqut, Rakhyut, Salalah, Taqah, Mirbat Wilayats)

All age groups

0/5253

0

(0–0.07)

Taenia spp.

on

[92]

Palestine

01/1998–12/2007

Gaza strip (Gaza, North, Mid-Zone, Khan Younis and Rafah Governorates)

All age groups

on

<1.0j

T. saginata

Microscopy

[49]

Palestine

11/2002–04/2003

Khan Younis Governorate

6–11

0/1370

0

(0–0.3)

Taenia spp.

Microscopy

[93]

Qatar

01/2005–12/2006

Doha

15–50

0/1737

0k

Taenia spp.

Microscopy

[94]

Qatar

01/2005–12/2008

Doha

1–80

0/9208

0

Taenia spp.

Microscopy

[95]

Saudi Arabia

09/2012–12/2012

Hail

on

2/130

1.5

(0.2–5.5)

Taenia spp.

Microscopy

[96]

Saudi Arabia

01/2010–12/2010

Hofuf, Khobar, Damman and suburban areas

2–18

5/1600

0.3

(0.1–0.7)

T. saginata

on

[97]

Saudi Arabia

10/2009–01/2011

Al-Baha

on

119/2000

6.0l

(5.0-7.0)

T. saginata

Microscopy

[98]

Saudi Arabia

2012

Madinah

20–55

1/120

0.8m

(0.02-4.6)

Taenia spp.

Microscopy

[99]

Saudi Arabia

01/1990–12/1992

Abha

17–45

0/5518

0n

(0–0.07)

Taenia spp.

Microscopy

[100]

South Sudan

on

Already

4– >50

1/241

0.4

(0.01–2.3)

Taenia spp.

Microscopy

[101]

Sudan

11/2003–10/2005

Khartoum

<21– >51

4/1500

0.3o

(0.07-0.7)

T. saginata

Microscopy

[102]

Sudan

03/1990–02/1991

Khartoum

<5

5/298

1.7

(0.6–3.9)

T. saginata

Microscopy

[103]

Sudan

12/2016–04/2017

Khartoum

5–14

0/120

0

(0–3.0)

Taenia spp.

Microscopy

[104]

Sudan

01/2013–06/2013

Khartoum

1–5

6/562

1.1

(0.4–2.3)

T. saginata

Microscopy (including proglottid or scolex identification)

[105]

Sudan

on

Khartoum

Primary school children

43/500

8.6

(6.3–11.4)

T. saginata

Microscopy

[106]

Syria

03/2006–06/2006

Damascus

6–12

0/1469

0

(0–0.3)

Taenia spp.

Microscopy

[107]

Tunisia

01/1997–12/2006

Sfax

1– >60

24/30,573

0.08

(0.05–0.1)

T. saginata

Microscopy

[108]

Tunisia

01/1996–12/2012

Tunis

on

4/20,033

0.02p

(0.005–0.05)

T. saginata

Microscopy

[109]

United Arab Emirates

01/2008–12/2009

Emirate of Sharjah (5 different hospitals)

1–58

0/10,514

0q

(0-0.04)

Taenia spp.

Microscopy

[110]

United Arab Emirates

01/2013–12/2013

Sharjah city

16– >44

31/21,347

0.15

(0.1–0.2)

Taenia spp.

Microscopy

[111]

Yemen

2009

Hadhramout Governorate (rural and urban areas)

6–13

9/600

1.5

(0.7–2.8)

T. saginata

Microscopy

[112]

Yemen

on

Sahar District

7–14

1/534

0.2

(0.005–1.0)

T. saginata

Microscopy

[113]

aRefers to Thais working in Israel

bStudy refers to Jewish, Bedouine and Ethiopian children living in southern Israel. Taenia spp. infections were only detected in Ethiopian children and were most probably T. saginata infections according to the authors

cMost probably a T. saginata case due to dietary restrictions

dRefers to the period 1997–1998

eRefers to the period 2007–2008

fTwo different numbers reported regarding Taenia spp. prevalence in the publication

gChildren from regions where raw wastewater is used for irrigation

hChildren from regions where wastewater irrigation is not practiced

iMost probably T. saginata cases due to dietary restrictions

jExact prevalence rate not mentioned. Estimated from graph (see figure 5 in reference [49])

kRefers to expatriate workers from Philippines, Indonesia, Indian sub-continent and Africa (food handlers and housemaids)

lRefers to expatriate workers from different countries. Highest infection rates with T. saginata observed among Indonesian, Indian, Bangladeshis, Filipinos and Pakistanis. Not mentioned how differentiation of Taenia species was made, although faeces were checked for presence of gravid proglottids

mRefers to expatriate workers from Asia and Africa

nRefers to Asian female house keepers from Indonesia, Sri Lanka, Philippines and Thailand

oRefers to Sudanese food handlers

pRefers to food handlers

q64% of the samples were from expatriates and the rest 36% were from native Emiratis. The expatriate population was a heterologous mixture of various nationalities from Indian subcontinent, Middle East, Southeast Asia, Africa and east European countries

Abbreviations: na, not available; CI, confidence interval; Ref, Reference

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 (1973–2007) 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].
Table 3

Prevalence of bovine or buffalo cysticercosis

Country

Time-frame

Location of study

No. of positive animals/No. of animals tested

Prevalence (95% CI)

Technical diagnosis

Reference

Egypt

01/1994–12/1997

All official abattoirs

4885/2,124,629

0.2a (0.2-0.2)

Meat inspection

[26]

36,201/499,610

7.3b (7.1-7.3)

4902/3,536,743

0.1c (0.1–0.1)

Egypt

05/2006–06/2007

Assiut Governorate

8/510

1.6d (0.7-3.0)

Meat inspection

[29]

2/268

0.7c (0.1-2.7)

Egypt

09/2014–05/2015

El-Minia Governorate

20/100

20.0d (12.7–29.1)

Meat inspection

[114]

Egypt

on

Cairo Governorate

3/75

4.0d (0.8–11.2)

Meat inspection

[115]

22/75

29.3d (19.4–41.0)

Ab-ELISA

Egypt

03/2010–02/2013

Gharbia Governorate

50/11,281

0.4d (0.3–0.6)

Meat inspection

[116]

24/19,089

0.1c (0.08–0.2)

Egypt

01/2014–12/2014

Qalyubia Governorate

313/3450

9.1c (1.0–10.0)

Meat inspection and molecular confirmation

[24]

Egypt

08/2015–07/2016

Aswan Governorate

3433/45,780

7.5d (7.3-7.7)

Meat inspection

[27]

3/223

1.3c (0.3-3.9)

Israel

1973–2007

Marbek Abattoir, Qiryat Mal'akhi

2568/629,549

0.4 (0.4–0.4)

Meat inspection

[28]

aNative cattle

bImported cattle

cBuffaloes

dCattle

Abbreviations: na, not available; CI, confidence interval

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).
Table 4

Bovine cysticercosis occurrence and number of cases, if provided, based on OIE data

Country/territory

1996

1997

1998

1999

2000

2001

2002

2003

2004

2005

Algeriaa

3

2

+

on

on

on

on

on

on

on

Cyprusa

on

on

on

on

on

on

on

on

on

on

Egypta

216

235

15,072

98

172

2692

698

164

3642

270

Iraq

on

on

on

on

on

on

on

on

on

Israela

+

26

+

on

on

on

on

20

+

Jordana

+

+

+

Kuwaita

Lebanon

+

+

+

+

on

on

on

+

Libya

Morocco

+

+

+

+

+

+

+

+

+

+

Oman

on

on

on

on

on

on

on

on

Palestinea

on

on

on

on

on

on

on

5

1

Qatar

on

on

on

on

on

Saudi Arabia

on

on

on

+

 

Sudan/South Sudan

+

on

on

on

on

on

on

b

Syria

on

on

on

Tunisia

+

on

on

on

on

on

on

on

on

United Arab Emirates

+

+

on

+

 

on

Western Sahara

on

on

on

on

on

on

on

on

on

on

Yemen

on

on

on

on

on

on

on

on

on

aNotifiable disease

bRefers to Sudan

Key: +, reported present or known to be present; −, disease absent (date of last outbreak not known); na, not available

Fig. 1

PRISMA flow chart

Fig. 2

Countries with reports of taeniosis due to Taenia saginata and Taenia spp. in the period 1990–2017

Fig. 3

Bovine cysticercosis occurrence based on OIE reports and countries with studies reporting prevalence in the period 1990–2017

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 semi-arid 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 eco-system 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.

Notes

Acknowledgements

This work was performed within the framework of the COST Action FA1408, A European Network for Foodborne Parasites (Euro-FBP), as a continuation of work begun during CYSTINET, the European network on taeniosis/cysticercosis, COST Action TD1302.

Funding

Not applicable.

Availability of data and materials

All references found eligible in our literature review are included in the article.

Authors’ contributions

AS conducted the systematic review of literature, extracted and analysed the data, and drafted the first version of the manuscript. All authors contributed to the design of the study, interpretation of the data, and writing of the paper. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

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

Supplementary material

References

  1. 1.
    Boyazoglu J, Hatziminaoglou Y. Livestock genetic resources and production systems: Livestock genetic resources and production systems: A Mediterranean vision. Arch Latinoam Prod Anim. 2002;10:62–7.Google Scholar
  2. 2.
    Crabtree PJ. Early animal domestication in the Middle East and Europe. Archaeol Method Theory. 1993;5:201–45.Google Scholar
  3. 3.
    Harter S, Le Bailly M, Janot F, Bouchet F. First paleoparasitological study of an embalming rejects jar found in Saqqara, Egypt. Mem Inst Oswaldo Cruz. 2003;98:119–21.CrossRefPubMedGoogle Scholar
  4. 4.
    Araujo A, Reinhard K, Ferreira LF, Pucu E, Chieffi PP, Araujo A, et al. Paleoparasitology: the origin of human parasites. Arq Neuropsiquiatr. 2013;71:722–6.CrossRefPubMedGoogle Scholar
  5. 5.
    Søe MJ, Nejsum P, Seersholm FV, Fredensborg BL, Habraken R, Haase K, et al. Ancient DNA from latrines in Northern Europe and the Middle East (500 BC-1700 AD) reveals past parasites and diet. PLoS One. 2018;13:e0195481.PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Wernery U. Zoonoses in the Arabian Peninsula. Saudi Med J. 2014;35:1455–62.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Seimenis A, Tabbaa D. Stray animal populations and public health in the South Mediterranean and the Middle East regions. Vet Ital. 2014;50:131–6.PubMedGoogle Scholar
  8. 8.
    Jacobson RL. Leishmaniasis in an era of conflict in the Middle East. Vector Borne Zoon Dis. 2011;11:247–58.CrossRefGoogle Scholar
  9. 9.
    WHO. Middle East respiratory syndrome coronavirus (MERS-CoV). 2018. http://www.who.int/emergencies/mers-cov/en/. Accessed 17 Nov 2018.
  10. 10.
    WHO, Regional Office for the Eastern Mediterranean. Roadmap of WHO’s work for the Eastern Mediterranean Region 2017–2021. 2017. http://apps.who.int/iris/handle/10665/258986. Accessed 18 Nov 2018.
  11. 11.
    Gardner A. Gulf migration and the family. J Arab Stud. 2011;1:3–25.CrossRefGoogle Scholar
  12. 12.
    Craig P, Ito A. Intestinal cestodes. Curr Opin Infect Dis. 2007;20:524–32.CrossRefPubMedGoogle Scholar
  13. 13.
    Taylor M, Coop R, Wall R. Veterinary Parasitology. 4th ed. Chichester: Wiley Blackwell; 2016.Google Scholar
  14. 14.
    Boone I, Thys E, Marcotty T, de Borchgrave J, Ducheyne E, Dorny P. Distribution and risk factors of bovine cysticercosis in Belgian dairy and mixed herds. Prev Vet Med. 2007;82:1–11.CrossRefPubMedGoogle Scholar
  15. 15.
    Marshall LR, Prakashbabu BC, Ferreira JP, Buzdugan SN, Stärk KDC, Guitian J. Risk factors for Taenia saginata cysticercus infection in cattle in the United Kingdom: a farm-level case-control study and assessment of the role of movement history, age and sex. Prev Vet Med. 2016;135:1–8.CrossRefPubMedGoogle Scholar
  16. 16.
    Cabaret J, Geerts S, Madeline M, Ballandonne C, Barbier D. The use of urban sewage sludge on pastures: the cysticercosis threat. Vet Res. 2002;33:575–97.CrossRefPubMedGoogle Scholar
  17. 17.
    Flütsch F, Heinzmann D, Mathis A, Hertzberg H, Stephan R, Deplazes P. Case-control study to identify risk factors for bovine cysticercosis on farms in Switzerland. Parasitology. 2008;135:641–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Silva CV, Costa-Cruz JM. A glance at Taenia saginata infection, diagnosis, vaccine, biological control and treatment. Infect Disord Drug Targets. 2010;10:313–21.CrossRefPubMedGoogle Scholar
  19. 19.
    Jansen F, Dorny P, Trevisan C, Dermauw V, Laranjo-González M, Allepuz A, et al. Economic impact of bovine cysticercosis and taeniosis caused by Taenia saginata in Belgium. Parasit Vectors. 2018;11:241.PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Laranjo-González M, Devleesschauwer B, Gabriël S, Dorny P, Allepuz A. Epidemiology, impact and control of bovine cysticercosis in Europe: a systematic review. Parasit Vectors. 2016;9:81.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    FAO. Food and Agriculture Organization of the United Nations statistical databases. 2018. http://www.fao.org/faostat/en/#data/QL. Accessed 7 June 2018.
  22. 22.
    Maitah M, Smutka L. Economic analysis of milk production and consumption in the Middle East and North Africa. Acta Univ Agric Silvic Mendelianae Brun. 2012;60:245–54.CrossRefGoogle Scholar
  23. 23.
    Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Kandil OM, Fahmy HA, Khalifa NO, El-Madawy RS, Afify JSA, Aly NSM, et al. Prevalence of cysticercosis and Taenia saginata in man. Glob Vet. 2015;15:372-80.Google Scholar
  25. 25.
    Economides P. Control of zoonoses in Cyprus. Rev Sci Tech. 2000;19:725–34.CrossRefPubMedGoogle Scholar
  26. 26.
    Haridy FM, Ibrahim BB, Morsy TA, Ramadan NI. Human taeniasis and cysticercosis in slaughtered cattle, buffaloes and pigs in Egypt. J Egypt Soc Parasitol. 1999;29:375–94.PubMedGoogle Scholar
  27. 27.
    Dyab AK, Marghany ME, Othman RA, Ahmed MA, Abd-Ella OH. Taenia saginata in man and cysticercosis in cattle and buffaloes in Aswan Governorate, Egypt. J Egypt Soc Parasitol. 2017;47:389–94.Google Scholar
  28. 28.
    Meiry M, Brenner G, Markovitcs A, Klement E. A change in the epidemiology of bovine cysticercosis in Israel between 1973 and 2008 due to import of live cattle. Transbound Emerg Dis. 2013;60:298–302.CrossRefPubMedGoogle Scholar
  29. 29.
    Basem B, Abdo R, Sayed A, Hussein A, Mohsen M, Arafa I. Occurence of cysticercosis in cattle and buffaloes and Taenia saginata in man in Assiut Governance of Egypt. Vet World. 2009;2:173–6.CrossRefGoogle Scholar
  30. 30.
    Pew Research Center. Religious Composition by Country, 2010–2050. 2015. http://www.pewforum.org/2015/04/02/religious-projection-table/. Accessed 15 June 2018.
  31. 31.
    Del Brutto OH. Neurocysticercosis on the Arabian Peninsula, 2003–2011. Emerg Infect Dis. 2013;19:172–4.PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Rajshekhar V, Joshi DD, Doanh NQ, van De N, Xiaonong Z. Taenia solium taeniosis/cysticercosis in Asia: epidemiology, impact and issues. Acta Trop. 2003;87:53–60.CrossRefPubMedGoogle Scholar
  33. 33.
    Winkler AS. Neurocysticercosis in sub-Saharan Africa: a review of prevalence, clinical characteristics, diagnosis, and management. Pathog Glob Health. 2012;106:261–74.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Braae U, Saarnak C, Mukaratirwa S, Devleesschauwer B, Magnussen P, Johansen M. Taenia solium taeniosis/cysticercosis and the co-distribution with schistosomiasis in Africa. Parasit Vectors. 2015;8:323.PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Ale A, Victor B, Praet N, Gabriël S, Speybroeck N, Dorny P, et al. Epidemiology and genetic diversity of Taenia asiatica: a systematic review. Parasit Vectors. 2014;7:45.PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    WHO. Taenia solium taeniasis/cysticercosis diagnostic tools. Report of a stakeholder meeting. Geneva, 17–18 December 2015. Geneva: World Health Association; 2016.Google Scholar
  37. 37.
    Ng-Nguyen D, Stevenson MA, Dorny P, Gabriël S, Van VT, Nguyen VAT, et al. Comparison of a new multiplex real-time PCR with the Kato-Katz thick smear and copro-antigen ELISA for the detection and differentiation of Taenia spp in human stools. PLoS Negl Trop Dis. 2017;11:e0005743.PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    van Lieshout L, Roestenberg M. Clinical consequences of new diagnostic tools for intestinal parasites. Clin Microbiol Infect. 2015;21:520–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Laranjo-González M, Devleesschauwer B, Trevisan C, Allepuz A, Sotiraki S, Abraham A, et al. Epidemiology of taeniosis/cysticercosis in Europe, a systematic review: western Europe. Parasit Vectors. 2017;10:349.PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Braae UC, Thomas LF, Robertson LJ, Dermauw V, Dorny P, Willingham AL, et al. Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in the Americas. Parasit Vectors. 2018;11:518.PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Trevisan C, Sotiraki S, Laranjo-González M, Dermauw V, Wang Z, Kärssin A, et al. Epidemiology of taeniosis/cysticercosis in Europe, a systematic review: eastern Europe. Parasit Vectors. 2018;11:569.PubMedCentralCrossRefPubMedGoogle Scholar
  42. 42.
    Dermauw V, Dorny P, Braae UC, Devleesschauwer B, Robertson LJ, Saratsis A, et al. Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in southern and eastern Africa. Parasit Vectors. 2018;11:578.PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Bobić B, Thomas LF, Djaković OD, Devleesschauwer B, Dermauw V, Dorny P, et al. Epidemiology of Taenia saginata taeniosis/cysticercosis in the Russian Federation. Parasit Vectors. 2018;11:636.PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Jansen F, Dorny P, Berkvens D, Van Hul A, Van den Broeck N, Makay C, et al. High prevalence of bovine cysticercosis found during evaluation of different post-mortem detection techniques in Belgian slaughterhouses. Vet Parasitol. 2017;244:1–6.CrossRefPubMedGoogle Scholar
  45. 45.
    Eichenberger RM, Lewis F, Gabriël S, Dorny P, Torgerson PR, Deplazes P. Multi-test analysis and model-based estimation of the prevalence of Taenia saginata cysticercus infection in naturally infected dairy cows in the absence of a “gold standard” reference test. Int J Parasitol. 2013;43:853–9.CrossRefPubMedGoogle Scholar
  46. 46.
    Dixon J, Gulliver A, Gibbon D. Global Farming Systems Study: Challenges and priorities to 2030. 2001. https://www.biw.kuleuven.be/DTP/TRO/_data/GFSS.pdf. Accessed 20 Nov 2018.
  47. 47.
    Qadir M, Bahri A, Sato T, Al-Karadsheh E. Wastewater production, treatment, and irrigation in Middle East and North Africa. Irrig Drain Syst. 2010;24:37–51.CrossRefGoogle Scholar
  48. 48.
    Habbari K, Tifnouti A, Bitton G, Mandil A. Intestinal parasitosis and environmental pollution: 1343 pediatric cases in Beni-Mellal, Morocco. Tunis Med. 2000;78:109–14.PubMedGoogle Scholar
  49. 49.
    Alhindi AI, Al-Louh M. Trends of intestinal parasites prevalence in the Gaza Strip, 1998–2007: the use of government health records. Turkish J Med Sci. 2013;43:652–9.CrossRefGoogle Scholar
  50. 50.
    Yassin MM, Amr SSA, Al-Najar HM. Assessment of microbiological water quality and its relation to human health in Gaza Governorate, Gaza Strip. Public Health. 2006;120:1177–87.CrossRefPubMedGoogle Scholar
  51. 51.
    Ben Ayed L, Schijven J, Alouini Z, Jemli M, Sabbahi S. Presence of parasitic protozoa and helminth in sewage and efficiency of sewage treatment in Tunisia. Parasitol Res. 2009;105:393–406.CrossRefPubMedGoogle Scholar
  52. 52.
    Al-Morshidy KAH, Al-Amari MJY. Detection of parasitic contamination in Hilla city drinking water/Babylon province/Iraq. Adv Nat Appl Sci. 2015;9:80–4.Google Scholar
  53. 53.
    USDA. Egypt: Livestock and Products Annual 2017. 2017. https://www.fas.usda.gov/data/egypt-livestock-and-products-annual-2017. Accessed 18 Dec 2018.
  54. 54.
    USDA. Lebanon: Lebanese Market Overview. 2016. https://www.fas.usda.gov/data/lebanon-lebanese-market-overview. Accessed 18 Dec 2018.
  55. 55.
    Hoang V-T, Gautret P. Infectious diseases and mass gatherings. Curr Infect Dis Rep. 2018;20:44.CrossRefPubMedGoogle Scholar
  56. 56.
    Alishani M, Sherifi K, Rexhepi A, Hamidi A, Armua-Fernandez MT, Grimm F, et al. The impact of socio-cultural factors on transmission of Taenia spp. and Echinococcus granulosus in Kosovo. Parasitology. 2017;144:1736–42.CrossRefPubMedGoogle Scholar
  57. 57.
    Levantine cuisine. 2018. https://en.wikipedia.org/wiki/Levantine_cuisine. Accessed 18 Dec 2018.
  58. 58.
    Gagaoua M, Boudechicha H-R. Ethnic meat products of the North African and Mediterranean countries: an overview. J Ethn Foods. 2018;5:83–98.CrossRefGoogle Scholar
  59. 59.
  60. 60.
    Dorny P, Vercammen F, Brandt J, Vansteenkiste W, Berkvens D, Geerts S. Sero-epidemiological study of Taenia saginata cysticercosis in Belgian cattle. Vet Parasitol. 2000;88:43–9.CrossRefPubMedGoogle Scholar
  61. 61.
    Bekraki A, Hanna K. Peritonitis caused by jejunal perforation with Taenia saginata: report of a case. J Parasit Dis. 2016;40:203–4.CrossRefPubMedGoogle Scholar
  62. 62.
    Atitar I, Amrani L, Serraj I, Amrani N. Small bowel parasitosis. Clin Res Hepatol Gastroenterol 2012;36:399.CrossRefPubMedGoogle Scholar
  63. 63.
    Baleela RM, Huessain MY, Ahmed ME. Anastomotic esophageal leak due to Taenia saginata following esophagectomy for esophageal cancer. Saudi Med J. 2006;27:241–3.PubMedGoogle Scholar
  64. 64.
    Adam A. Oral expulsion of Taenia saginata by a Sudanese woman in Nyala, western Sudan. Sudan JMS. 2008;3:79–80.Google Scholar
  65. 65.
    Antaki N. Endoscopic discovery of a Taenia in the duodenal bulb. Endoscopy. 2002;34:1033.CrossRefPubMedGoogle Scholar
  66. 66.
    Benouis A, Bekkouche Z, Benmasour Z. Epidemiological study of human intestinal parasitosis at the level of CHU of Oran (Algeria). Int J Innov Appl Stud. 2013;2:613–20 (In French).Google Scholar
  67. 67.
    Omran EK, Mohammad AN. Intestinal parasites in patients with chronic abdominal pain. J Egypt Soc Parasitol. 2015;45:389–96.CrossRefPubMedGoogle Scholar
  68. 68.
    El Hady HA, Hussein SMM, Mohamed AM, Elrahim BAEA. Association between phlyctenular conjuctivitis and intestinal parasites. J Egypt Soc Parasitol. 2015;45:315–20.CrossRefPubMedGoogle Scholar
  69. 69.
    Bayoumy AMS, Mohammed KAEH, Shahat SAER, Ghannam MMM, Gazy MESM. Role of parasites among chronic diarrheic patients. J Egypt Soc Parasitol. 2010;40:679–98.PubMedGoogle Scholar
  70. 70.
    El Shazly AM, Awad SE, Sultan DM, Sadek GS, Khalil HHM, Morsy TA. Intestinal parasites in Dakahlia Governorate, with different techniques in diagnosing protozoa. J Egypt Soc Parasitol. 2006;36:1023–34.PubMedGoogle Scholar
  71. 71.
    El-Shazly AM, El-Nahas HA, Soliman M, Sultan DM, Abedl Tawab AH, Morsy TA. The reflection of control programs of parasitic diseases upon gastrointestinal helminthiasis in Dakahlia Governorate, Egypt. J Egypt Soc Parasitol. 2006;36:467–80.PubMedGoogle Scholar
  72. 72.
    Tosson, Morsy A, Farrag AM, Sabry AH, Salama MM, Arafa MA. Ecto- and endoparasites in two primary schools in Qualyob City, Egypt. J Egypt Soc Parasitol. 1991;21:391–401.PubMedGoogle Scholar
  73. 73.
    Sabry AH. Parasitic infection in Sennores Primary School, El-Fayum Governorate, Egypt. J Egypt Soc Parasitol. 1991;21:571–4.PubMedGoogle Scholar
  74. 74.
    Salem SA, Mohamed NH, Azab ME, Soffa SA, el Kadery AA, Sabry NM. A survey for enteroparasites in Menoufia Governorate, Egypt with special reference to Strongyloides stercoralis. J Egypt Soc Parasitol. 1990;20:335–44.PubMedGoogle Scholar
  75. 75.
    Zakaria OM. The controversy of parasitic infection in pediatric appendicitis. Ann Pediatr Surg. 2012;8:15–8.CrossRefGoogle Scholar
  76. 76.
    Hany AAE-SH, Mahmoud A. Ecto- and endoparasites in primary school pupils in El-Ghanayem City, Assiut Governorate, Upper Egypt. Asiut Med J. 2001;25:1–8.Google Scholar
  77. 77.
    Kadir M, Salman Y. Prevalence of intestinal parasites among primary school children in Al-Taameem Province. Iraq. Ann Coll Med Mosul. 1999;25:94–8.Google Scholar
  78. 78.
    Greenberg Z, Giladi L, Bashary A, Zahavi H. Prevalence of intestinal parasites among Thais in Israel. Harefuah. 1994;126:507–9.PubMedGoogle Scholar
  79. 79.
    Ben-Shimol S, Sagi O, Greenberg D. Differences in prevalence of parasites in stool samples between three distinct ethnic pediatric populations in southern Israel, 2007–2011. Parasitol Int. 2014;63:456–62.CrossRefPubMedGoogle Scholar
  80. 80.
    Jaran AS. Prevalence and seasonal variation of human intestinal parasites in patients attending hospital with abdominal symptoms in northern Jordan. East Mediterr Health J. 2016;22:756–60.CrossRefGoogle Scholar
  81. 81.
    Al-Lahham AB, Abu-Saud M, Shehabi AA. Prevalence of Salmonella, Shigella and intestinal parasites in food handlers in Irbid, Jordan. J Diarrhoeal Dis Res. 1990;8:160–2.PubMedGoogle Scholar
  82. 82.
    Francis IM, Hira PR, Matusik J, Farid L, Tungekar FM. Parasite infestation of the vermiform appendix: the experience in Kuwait. Med Princ Pract. 1992;3:31–9.CrossRefGoogle Scholar
  83. 83.
    Alkarmi T, Alharbi S, Abu-Lisan M, Salman A, Behbehani K. Prevalence of intestinal parasitic infections in Kuwait. Med Princ Pract. 1990;2:10–7.Google Scholar
  84. 84.
    Araj GF, Musharrafieh UM, Haydar A, Ghawi A, Itani R, Saliba R. Trends and prevalence of intestinal parasites at a tertiary care center in Lebanon over a decade. J Med Liban. 2011;59:143–8.PubMedGoogle Scholar
  85. 85.
    Hamze M, Dabboussi F, Al-Ali K, Ourabi L. Prevalence of infection by intestinal parasites in north Lebanon: 1997–2001. East Mediterr Health J. 2004;10:343–8.PubMedGoogle Scholar
  86. 86.
    Araj GF, Abdul-Baki NY, Hamze MM, Alami SY, Nassif RE, Naboulsi MS. Prevalence and etiology of intestinal parasites in Lebanon. Leban Med J. 1996;44:129-33.Google Scholar
  87. 87.
    Saab BR, Musharrafieh U, Nassar NT, Khogali M, Araj GF. Intestinal parasites among presumably healthy individuals in Lebanon. Saudi Med J. 2004;25:34–7.PubMedGoogle Scholar
  88. 88.
    Hamze M, Naja M, Mallat H. Biological analyzes carried out among workers in the food sector in northern Lebanon. East Mediterr Health J. 2008;14:1425–34 (In French).PubMedGoogle Scholar
  89. 89.
    Ben Musa NA. Intestinal parasites in school aged children and the first case report on amoebiasis in urinary bladder in Tripoli, Libya. J Egypt Soc Parasitol. 2007;37:775–84.PubMedGoogle Scholar
  90. 90.
    El Guamri Y, Belghyti D, Achicha A, Tiabi M, Aujjar N, Barkia A, et al. Retrospective epidemiological survey of intestinal parasitosis at El Idrissi Provincial Hospital (Kenitra, Morocco): a 10-year review (1996–2005). Ann Biol Clin. 2009;67:191–202 (In French).Google Scholar
  91. 91.
    Patel PK, Khandekar R. Intestinal parasitic infections among school children of the Dhahira Region of Oman. Saudi Med J. 2006;27:627–32.PubMedGoogle Scholar
  92. 92.
    Dept. of Surveillance & Disease Control. Study on intestinal parasitic infection in Dhofar region. Community Heal Dis Surveill Newsl. 1995;4:1–4.Google Scholar
  93. 93.
    Astal Z. Epidemiological survey of the prevalence of parasites among children in Khan Younis Governorate, Palestine. Parasitol Res. 2004;94:449–51.CrossRefPubMedGoogle Scholar
  94. 94.
    Abu-Madi MA, Behnke JM, Ismail A. Patterns of infection with intestinal parasites in Qatar among food handlers and housemaids from different geographical regions of origin. Acta Trop. 2008;106:213–20.CrossRefPubMedGoogle Scholar
  95. 95.
    Abu-Madi MA, Behnke JM, Doiphode SH. Changing trends in intestinal parasitic infections among long-term-residents and settled immigrants in Qatar. Parasit Vectors. 2010;3:98.PubMedCentralCrossRefPubMedGoogle Scholar
  96. 96.
    Hassen Amer O, Ashankyty IM, Haouas NAS. Prevalence of intestinal parasite infections among patients in local public hospitals of Hail, northwestern Saudi Arabia. Asian Pac J Trop Med. 2016;9:44–8.CrossRefPubMedGoogle Scholar
  97. 97.
    Zakaria OM, Zakaria HM, Daoud MY, Al Wadaani H, AlBuali W, Al-Mohammed H, et al. Parasitic infestation in pediatric appendicitis: a local experience. Oman Med J. 2013;28:92–6.PubMedCentralCrossRefPubMedGoogle Scholar
  98. 98.
    Mohammad KAH, Koshak EAK. A prospective study on parasites among expatriate workers in Al-Baha from 2009–2011, Saudi Arabia. J Egypt Soc Parasitol. 2011;41:423–32.PubMedGoogle Scholar
  99. 99.
    Imam NA, Abdulbaqi Z, Fahad R. The prevalence of intestinal parasitic infections among foreign workers in Madinah, Kingdom of Saudi Arabia. Saudi J Med Med Sci. 2015;3:112–7.CrossRefGoogle Scholar
  100. 100.
    Al-Madani AA, Mahfouz AA. Prevalence of intestinal parasitic infections among Asian female house keepers in Abha District, Saudi Arabia. Southeast Asian J Trop Med Public Health. 1995;26:135–7.PubMedGoogle Scholar
  101. 101.
    Marnell F, Guillet A, Holland C. A survey of the intestinal helminths of refugees in Juba, Sudan. Ann Trop Med Parasitol. 1992;86:387–93.CrossRefPubMedGoogle Scholar
  102. 102.
    Babiker MA, Ali MSM, Ahmed ES. Frequency of intestinal parasites among food-handlers in Khartoum, Sudan. East Mediterr Health J. 2009;15:1098–104.CrossRefPubMedGoogle Scholar
  103. 103.
    Karrar ZA, Rahim FA. Prevalence and risk factors of parasitic infections among under-five Sudanese children: a community based study. East Afr Med J. 1995;72:103–9.PubMedGoogle Scholar
  104. 104.
    Siddig HS, Mohammed IA, Mohammed MN, Bashir AM. Prevalence of intestinal parasites among selected group of primary school children in Alhag Yousif Area, Khartoum, Sudan. Int J Med Res Health Sci. 2017;6:125–31.Google Scholar
  105. 105.
    Sun C. Prevalence and associated risk factors of intestinal helminth infections among pre-school children (1 to 5 years old) in IDPs settlements of Khartoum state, Sudan. J Glob Health. 2015. http://www.ghjournal.org/prevalence-and-associated-risk-factors-of-intestinal-helminths-infections-among-pre-school-children-1-to-5-years-old-in-idps-settlements-of-khartoum-state-sudan/#. Accessed 18 Dec 2018.
  106. 106.
    Gabbad AA, Elawad MA. Prevalence of intestinal parasite infection in primary school children in Elengaz area, Khartoum, Sudan. Acad Res Int. 2014;5:86–90.Google Scholar
  107. 107.
    Almerie MQ, Azzouz MS, Abdessamad MA, Mouchli MA, Sakbani MW, Alsibai MS, et al. Prevalence and risk factors for giardiasis among primary school children in Damascus, Syria. Saudi Med J. 2008;29:234–40.PubMedGoogle Scholar
  108. 108.
    Cheikhrouhou F, Trabelsi H, Sellami H, Makni F. Intestinal parasitoses in the Sfax Region (southern Tunisia): a retrospective study. Rev Tun Infect. 2009;3:14–8 (In French).Google Scholar
  109. 109.
    Siala E, Toumi I, Béttaieb J, Boulehmi N, Zallega N, Aoun K, et al. Evolution of the prevalence of intestinal parasitosis in the region of Tunis from 1996 at 2012. Tunis Med. 2015;93:687–91.PubMedGoogle Scholar
  110. 110.
    Dash N, Al-Zarouni M, Anwar K, Panigrahi D. Prevalence of intestinal parasitic infections in Sharjah, United Arab Emirates. Hum Parasit Dis. 2010;2:21–4.CrossRefGoogle Scholar
  111. 111.
    Dafalla AIA, Almuhairi SASO, AlHosani MHJ, Mohamed MY, Alkous MIA, AlAzzawi MA, et al. Intestinal parasitic infections among expatriate workers in various occupations in Sharjah, United Arab Emirates. Rev Inst Med Trop Sao Paulo. 2017;59:e82.PubMedCentralCrossRefPubMedGoogle Scholar
  112. 112.
    Al-Haddad AM, Baswaid SH. Frequency of intestinal parasitic infection among children in Hadhramout Governorate (Yemen). J Egypt Soc Parasitol. 2010;40:479–88.PubMedGoogle Scholar
  113. 113.
    Raja’a YA, Mubarak JS. Intestinal parasitosis and nutritional status in schoolchildren of Sahar district, Yemen. East Mediterr Health J. 2006;12:189–94.Google Scholar
  114. 114.
    Abdel-Hafeez EH, Kamal AM, Abdelgelil NH, Abdel-Fatah M. Parasites transmitted to human by ingestion of different types of meat, El-Minia city, El-Minia Governorate, Egypt. J Egypt Soc Parasitol. 2015;45:671–80.CrossRefPubMedGoogle Scholar
  115. 115.
    Kandil OM, Nasr SM, Mahmoud MS, Nassar SA, El-Metanawey TM, Abd El-Aziz MHMA, et al. Serological and biochemical studies on cattle naturally infested with Taenia saginata cysticercosis. Glob Vet. 2012;9:571–9.Google Scholar
  116. 116.
    Elmonir W, Mousa W, Sultan K. The prevalence of some parasitic zoonoses in different slaughtered animal species at abattoir in the Mid-Delta of Egypt; with special reference to its economic implications. Alexandria J Vet Sci. 2015;47:97.CrossRefGoogle Scholar

Copyright information

© The Author(s) 2019

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

Authors and Affiliations

  • Anastasios Saratsis
    • 1
    Email author
  • Smaragda Sotiraki
    • 1
  • Uffe C. Braae
    • 2
    • 3
  • Brecht Devleesschauwer
    • 4
    • 5
  • Veronique Dermauw
    • 6
  • Ramon M. Eichenberger
    • 7
  • Lian F. Thomas
    • 8
    • 9
  • Branko Bobić
    • 10
  • Pierre Dorny
    • 6
    • 11
  • Sarah Gabriël
    • 5
  • Lucy J. Robertson
    • 12
  1. 1.Veterinary Research InstituteHellenic Agricultural Organization DemeterThermiGreece
  2. 2.One Health Center for Zoonoses and Tropical Veterinary MedicineRoss University School of Veterinary MedicineBasseterreSaint Kitts and Nevis
  3. 3.Department for Infectious Disease Epidemiology and PreventionStatens Serum InstitutCopenhagenDenmark
  4. 4.Department of Epidemiology and Public HealthSciensanoIxellesBelgium
  5. 5.Department of Veterinary Public Health and Food SafetyGhent UniversityMerelbekeBelgium
  6. 6.Department of Biomedical SciencesInstitute of Tropical MedicineAntwerpBelgium
  7. 7.Institute of Parasitology, Vetsuisse FacultyUniversity of ZurichZurichSwitzerland
  8. 8.Institute of Infection & Global HealthUniversity of LiverpoolLiverpoolUK
  9. 9.International Livestock Research InstituteNairobiKenya
  10. 10.Centre of Excellence for Food- and Vector-borne Zoonoses, Institute for Medical ResearchUniversity of BelgradeBelgradeSerbia
  11. 11.Department of Virology, Parasitology and ImmunologyGhent UniversityMerelbekeBelgium
  12. 12.Department of Food Safety and Infection Biology, Faculty of Veterinary MedicineNorwegian University of Life SciencesOsloNorway

Personalised recommendations