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Review

Helminth Parasites among Rodents in the Middle East Countries: A Systematic Review and Meta-Analysis

by
Md Mazharul Islam
1,2,*,
Elmoubashar Farag
3,*,
Mohammad Mahmudul Hassan
4,
Devendra Bansal
3,
Salah Al Awaidy
5,
Abdinasir Abubakar
6,
Hamad Al-Romaihi
3 and
Zilungile Mkhize-Kwitshana
7,8
1
Department of Animal Resources, Ministry of Municipality and Environment, Doha, P.O. Box 35081, Qatar
2
School of Laboratory Medicine and Medical Sciences, College of Health Sciences, University of KwaZulu Natal, Durban 4000, South Africa
3
Ministry of Public Health, Doha, P.O. Box 42, Qatar
4
Faculty of Veterinary Medicine, Chattogram Veterinary and Animal Sciences University, Khulshi, Chattogram 4225, Bangladesh
5
Ministry of Health, P.O. Box 393, PC 113 Muscat, Oman
6
Infectious Hazard Preparedness (IHP) Unit, WHO Health Emergencies Department (WHE), World Health Organization, Regional Office for the Eastern Mediterranean, Cairo 11371, Egypt
7
School of Life Sciences, College of Agriculture, Engineering & Science, University of KwaZulu Natal, Durban 40000, South Africa
8
South African Medical Research Council, Cape Town 7505, South Africa
*
Authors to whom correspondence should be addressed.
Animals 2020, 10(12), 2342; https://doi.org/10.3390/ani10122342
Submission received: 3 October 2020 / Revised: 30 October 2020 / Accepted: 30 October 2020 / Published: 9 December 2020
(This article belongs to the Special Issue Veterinary Microbiology & Parasitology)
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Abstract

:

Simple Summary

The review was conducted to establish an overview of rodent helminths in the Middle East as well as their public health importance. Following a systematic search, 65 field research were identified, studied, and analyzed. The overall prevalence of cestodes, nematodes, and trematodes were 24.88%, 32.71%, and 10.17%, respectively. The review detected 21 species of cestodes, 56 nematodes, and 23 trematodes, from which 22 have zoonotic importance. Capillaria hepatica, Hymenolepis diminuta, Hymenolepis nana, and Cysticercus fasciolaris were the most frequent and widespread zoonotic helminths. The review identified that there is an information gap on rodent helminths at the humans-animal interface level in this region. Therefore, the public health importance of rodent-borne helminth parasites is not fully recognized. Countrywide detailed studies on rodent helminths, along with the impact on public health, should be conducted in this region.

Abstract

Rodents can be a source of zoonotic helminths in the Middle East and also in other parts of the world. The current systematic review aimed to provide baseline data on rodent helminths to recognize the threats of helminth parasites on public health in the Middle East region. Following a systematic search on PubMed, Scopus, and Web of Science, a total of 65 research studies on rodent cestodes, nematodes, and trematodes, which were conducted in the countries of the Middle East, were analyzed. The study identified 44 rodent species from which Mus musculus, Rattus norvegicus, and Rattus rattus were most common (63%) and recognized as the primary rodent hosts for helminth infestation in this region. Cestodes were the most frequently reported (n = 50), followed by nematodes (49), and trematodes (14). The random effect meta-analysis showed that the pooled prevalence of cestode (57.66%, 95%CI: 34.63–80.70, l2% = 85.6, p < 0.001) was higher in Saudi Arabia, followed by nematode (56.24%, 95%CI: 11.40–101.1, l2% = 96.7, p < 0.001) in Turkey, and trematode (15.83%, 95%CI: 6.25–25.1, l2% = 98.5, p < 0.001) in Egypt. According to the overall prevalence estimates of individual studies, nematodes were higher (32.71%, 95%CI: 24.89–40.54, l2% = 98.6, p < 0.001) followed by cestodes (24.88%, 95%CI: 19.99–29.77, l2% = 94.9, p < 0.001) and trematodes (10.17%, 95%CI: 6.7–13.65, l2% = 98.3, p < 0.001) in the rodents of the Middle East countries. The review detected 22 species of helminths, which have zoonotic importance. The most frequent helminths were Capillaria hepatica, Hymenolepis diminuta, Hymenolepis nana, and Cysticercus fasciolaris. There was no report of rodent-helminths from Bahrain, Jordan, Lebanon, Oman, United Arab Emirates, and Yemen. Furthermore, there is an information gap on rodent helminths at the humans-animal interface level in Middle East countries. Through the One Health approach and countrywide detailed studies on rodent-related helminths along with their impact on public health, the rodent control program should be conducted in this region.

Graphical Abstract

1. Introduction

Helminths are among the most diverse and geographically widespread groups of parasites that infect both humans and animals [1]. Although they are from different phyla or class (nematode, cestode, and trematode), the mode of transmission, infection, and pathogenesis, as well as host immune-responsiveness of these pathogens, follows a typical pattern. Approximately one-third of the world population is infected with one or more types of helminths. From amongst 300,000 species of helminths that typically infect vertebrates, 287 of them infect humans, from which 95% are either zoonoses or have evolved from animal parasites [2]. About 100 of the zoonotic helminths cause asymptomatic infection or mild symptoms in humans, while only a small percentage of them cause severe or even fatal infections [1]. In resource-poor countries, livestock is a source of food, production, income source, and deposit of wealth. Parasite infections in animals indirectly affect human health through financial hardship and malnutrition. Based on the burden of death, sickness, and treatment cost for both humans and animals for helminth infestation, the zoonotic parasites’ socioeconomic burden was presented as high or low socioeconomic impact [3].
Rodents are significant sources of parasitic zoonosis in humans, serving as reservoirs and vectors of at least 70 zoonotic diseases, of which 16 are helminth parasites [4]. Consumption of uncooked/improperly cooked food contaminated with the infective larvae, eggs, or metacercariae is the primary source of humans infestation with helminth parasites [5,6]. When pilfering humans food, rodents pass stool or urine that contaminates said food, leading to transmission of zoonotic helminths from rodents to humans [7].
The Middle East is an intercontinental region with a total population of over 411 million [8] in 17 sovereign countries, including Bahrain, Cyprus, Egypt, Iran, Iraq, Israel, Jordan, Kuwait, Lebanon, Oman, Palestine, Qatar, Kingdom of Saudi Arabia (KSA), Syria, Turkey, United Arab Emirates (UAE), and Yemen. The majority of people in this region live in poverty [9], with the highest percentage being specific to Yemen, Syria, Egypt, Palestine, and Iraq [10,11]. Cultural diversity, weak economic policy, poor governance, rapid population growth, low educational structure, gender discrimination, underdeveloped infrastructure, and war and conflict have turned the region into a hot spot for many emerging and re-emerging diseases, including rodent-borne parasitic infections [9,12,13]. In the past, rodent-borne infections have led to multiple instances of a fatal epidemic, in part due to a lack of relevant information available on the subject, which makes it difficult to maintain public health sustainability [14,15].
Helminth infestations are mostly neglected diseases [16]. Therefore, the complete picture of zoonotic helminths is not well known in the Middle East area. Despite several studies being done on helminths in this region, no systematic review or meta-analysis was performed on rodent helminths, including zoonotic importance in the Middle East region. Our objective is to summarize baseline information on rodent helminths in this region using evidence-based records of the helminths detected in rodents in the Middle Eastern countries. The review also identifies the rodent helminths with public health importance in this region.

2. Materials and Methods

We followed PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) guidelines [17] to conduct the systematic review using a four-step approach: database search, evaluating relevant articles, data extraction, and summarizing. One author conducted the data search. Two authors were involved in critical evaluation and data extraction from the selected articles, while one author managed the compilation of said data. Afterward, two authors arranged the data and conducted the meta-analysis (Figure 1, Supplementary Table S1).

2.1. Search Strategy

A literature search on rodent helminth parasites in the Middle East was performed on 17 June 2019 through PubMed, Web of Science, and Scopus (Figure 1). The search included all the original research articles containing field evidence of helminth parasites (trematode, nematode, cestode) among rodents in the Middle East countries. The search did not have any date range of publication. The keywords included (Rodent OR Rat OR Jird OR Gerbil OR Vole OR Mouse OR Hamster OR Porcupine OR Squirrel OR Jerboa) AND (Endoparasite OR Helminth OR Cestode OR Trematode OR Nematode) AND (17 Middle East country names individually). Screening on the search was conducted as [Title/Abstract] in PubMed, [TITLE-ABS-KEY] in Scopus, and [Topic] in Web of Science.

2.2. Search of Relevant Articles

The data search results were processed using EndNote X9 (clarivate analytics, Philadelphia, PA, USA), which was also used to identify and exclude duplicate studies. Then we proceeded to peruse through the titles and abstracts to find the relevant articles. However, articles that were ambiguous regarding their relevance by their title and abstract were subjected to full-text analysis. Only documents published in English were considered for the review [18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82].

2.3. Data Extraction and Summarizing

Evidence-based field reports give a clear picture of any pathogen’s availability, diversity, and dynamics in a locality [83,84]. We considered only the field reports containing rodent helminths for data abstraction. The extracted data included several variables such as country and location of sampling, season, year of sampling, rodent information (rodent species, sex, total rodent count, and the number of infected), helminth species and type, and possible associating factors of rodent infestation with helminth (Supplementary Table S2). The zoonotic rodent-borne helminths in this region were identified from the list of rodent helminths from this review with the support of published articles.

2.4. Data Analysis

The aggregated data was transcribed and stored in a Microsoft Excel spreadsheet, and then the data was forwarded to STATA/IC-13.0 (Stata Corp, 4905 Lakeway Drive, College Station, Texas 77845, USA) for statistical analysis. Crude prevalence estimation was performed by dividing the total number of helminth-positive rodents with the total number of rodents sampled and expressed as a percentage. The crude estimate of prevalence was used throughout, the 95% confidence interval (CI), and the p-value were calculated on different types of helminths among the countries. Study variations among the studies were evaluated using the Chi-square (χ2) test on Cochran’s Q statistics (with p-value) followed by I2 statistics to determine the study’s degree of heterogeneity. Standard Error (SE) was calculated using a standard formula for proportion calculation. A random-effect meta-analysis model was applied using the “mean” command specifying random due to the study’s high degree of heterogeneity (I2 > 75%). The output has been illustrated using a forest plot [85].

3. Results

3.1. Descriptive Analysis

The literature search returned 65 articles (Figure 1, Supplementary Table S2) published from 1969 to 2019. These articles were from 11 out of 17 Middle East countries, such as Cyprus, Egypt, Iran, Iraq, Israel, Kuwait, Palestine, Qatar, Saudi Arabia, Syria, and Turkey (Figure 2). No report on rodent helminths was available from Bahrain, Jordan, Lebanon, Oman, United Arab Emirates, and Yemen. Cestodes were the most frequently reported (50 articles) helminths in the Middle Eastern rodents, followed by nematodes (49), and trematodes (14).
All 65 studies reported at least 9628 rodents (47% females and 53% males). A total of 44 rodent species from 6 families were listed (Supplementary Table S3). The analysis identified Acomys dimidiatus, Jaculus jaculus, Meriones crassus, Mus musculus, and Rattus norvegicus, Rattus ratus were widely distributed as these rodents were reported from where Mus musculus (n = 1251, 12.6%), Rattus norvegicus (n = 3325, 33.6%), and Rattus rattus (n = 1694, 17.1%) as the most common. Besides, three sub-species of Rattus rattus, such as Rattus rattus alexandrines, Rattus rattus frugivorous, and Rattus rattus rattus, are prevalent in the Middle East. Moreover, the review found some other rodents, which are important as zoonotic helminth carrier. These include Acomys cahirinus, Acomys dimidiatus, Apodemus sylvaticus, Apodemus witherby, Arvicanthus niloticus, Calomyscus elburzensis, Cricetulus migratorius, Gerbillus cheesmani, Gerbillus gerbillus, Meriones libycus, Meriones persicus, Mesocricetus auratus, Microtus socialis, Microtus transcaspicus, Mus domesticus, Rhombomys opimus, and Tatera indica. A total of 100 species of rodent helminths were identified. Based on the available data, the estimated pooled prevalence of the different types of parasites in rodents has been presented in Table 1. The random effect meta-analysis showed that the pooled prevalence of cestode ranged from 12.87% (95%CI: 5.17–20.57, l2% = 80.6, p < 0.001) in Turkey to 57.66% (95%CI: 34.63–80.70, l2% = 85.6, p < 0.001) in Saudi Arabia. The nematode prevalence was varying from 0.16% (95%CI: −0.15–0.47, l2% = 0.0) in Cyprus to 56.24% (95%CI: 11.40–101.1, l2% = 96.7, p < 0.001) in Turkey. Moreover, the prevalence of trematode ranged from 0.24% (95%CI: −0.11–0.59 l2% = 0.0, p < 0.001) in Iran to 15.83% (95%CI: 6.25–25.1, l2% = 98.5, p < 0.001) in Egypt.

3.2. Rodent Cestodes in the Middle East Countries

Rodent cestodes information was available from all 11 Middle Eastern countries (Supplementary Table S3). A total of 21 rodent cestode species that belongs to 8 families have been reported in this review. Most of the cestodes were from Egypt and Iran (12 cestode species from each county). Out of 44 rodent species, Mus musculus, Rattus norvegicus, and Rattus rattus were frequently identified with the cestode infestation. Three species of cestodes have been frequently reported, viz: Hymenolepis diminuta (20 reports from 5 countries), Hymenolepis nana (30, 9), and Cysticercus fasciolaris (23, 4). Figure 3 shows the prevalence estimates from individual studies on cestodes in rodents of the Middle East countries, which ranged from 7.69 (95%CI: 2.22–13.17) to 68.57 (95%CI: 59.69–77.45) with an overall estimated prevalence 24.88 (95%CI: 19.99–29.77, l2% = 94.9, p < 0.001).

3.3. Rodent Nematodes in the Middle East Countries

Rodent nematodes were studied in 8 countries in the Middle East, namely Cyprus, Egypt, Iran, Iraq, Israel, Kuwait, Palestine, and Turkey (Supplementary Table S3). Nematodes from 23 families represented the 56 nematode species in this region. Most of the rodent nematodes were reported from Egypt (n = 24) and Iran (n = 31) and the rodent species such as Mus musculus, Rattus norvegicus, Rattus rattus, Meriones persicus, Acomys dimidiatus, and Tatera indica. However, the nematodes, Aspiculuris tetraptera, Capillaria hepatica, Syphacia obvelata, Streptopharagus kuntzi, and Trichuris muris were most frequently reported and widely distributed. These nematodes were reported from three or more countries in the Middle East. Figure 4 shows the prevalence estimates from individual studies on nematodes in rodents of the Middle East countries, which ranged from 0.16 (95%CI: −0.15–0.47) to 79.41 (95%CI: 65.82–93.0) with an overall estimated prevalence of 32.71 (95%CI: 24.89–40.54, l2% = 98.6, p < 0.001).

3.4. Rodent Trematodes in the Middle East Countries

The reviewed studies reported rodent trematodes in Egypt, Iran, Israel, and Saudi Arabia (Supplementary Table S3). At least 23 trematode species from 11 families of trematodes were reported in the Middle Eastern rodents. Reports from Egypt (n = 21) were more descriptive of these trematodes. Moreover, Fasciola sp. was detected in Saudi Arabia, Scaphiostomum sp. in Israel, and Notocotylus neyrai and Plagiorchis muris were identified in Iran. The review found Arvicanthus niloticus, Rattus norvegicus, and Rattus rattus are three rodent species important for trematode infestation. Figure 5 shows the prevalence estimates from individual studies on trematode in rodents of the Middle East countries, which ranged from 0.20 (95%CI: −0.19–0.59) to 36.90 (95%CI: 26.59–47.22) with an overall estimated prevalence of 10.17 (95%CI: 6.7–13.65, l2% = 98.3, p < 0.001).

3.5. Zoonotic Importance of the Rodent Helminths in the Middle East Countries

Out of the 100 species of rodent helminths detected in this review, 22 species have zoonotic importance; 7 cestodes, 6 nematodes, and 9 trematodes. The zoonotic helminths, their hosts, and possible human infection sources have been illustrated in Table 2.

4. Discussion

This study reviewed the literature published in English on helminths-infested rodents in the Middle East region. The majority of the studies (47 of 65) were from Iran and Egypt, most likely due to their long history of rodent-borne zoonotic disease (like murine typhus, plague, tularemia) epidemics, which resulted in millions of death [4,91,92,93,94]. Thus, this topic became a central focus of public health research in these countries. The present review found three commensal rodent species: Mus musculus, Rattus norvegicus, and Rattus rattus to be more common and carrying most of the zoonotic helminths within this region. Previous literature described that these species occupy different habitats with higher population density than the other species and pose considerable risk to public health [4]. Although rodent cestodes were most frequently reported (n = 50) helminth in this review, the meta-analysis detected the overall rodent nematode prevalence was highest (32.7%) compared to cestodes (24.88%) and trematodes (10.17%) prevalence. Out of the 22 zoonotic helminths detected in this review, Capillaria hepatica, H. diminuta, H. nana, and C. fasciolaris have been found as widespread distribution. Furthermore, some non-zoonotic helminths such as Aspiculuris tetraptera, Syphacia obvelata, Streptopharagus kuntzi, and Trichuris muris were reported from three or more countries in this region.
Rodents have several beneficiary activities in ecology, such as soil aeration and water absorption ability, biotic recovery, and insect control [4,95]. In this regard, the presence of healthy rodents is essential for ecology [96]. Helminths infestation in rodents affects their own health and can subsequently alter the rodent-environment ecology to a considerable degree. Moreover, rodent helminths are important for humans, livestock, and pet animal health. Hymenolepiais is a major zoonotic rodent cestode [6]. Fascioliasis is hazardous for livestock health as well as for humans [6,97]. The definite host of Taenia taeniaeformis is the cat, where a stage of this cestode lifecycle (the cystic form, Cysticercus fasciolaris) is completed in rodents. An increase of Cysticercus fasciolaris in rodents can increase the health risk of cats [98]. Thus, rodent helminths have an impact on the ecology as well as humans and animal health.
Rodent-borne zoonotic helminths incur significant socioeconomic losses, although the zoonotic helminths’ socioeconomic burden can differ from species to species [3]. Hymenolepis diminuta and Hymenolepis nana are major zoonotic cestodes [3,99]. Trichostrongylus sp. and Trichuris trichiura are generally considered as major nematode threats [100]. The socioeconomic burden caused by Angiostrongylus cantonensis, Gongylonema pulchrum, Trichinella sp., and Capillaria hepatica are likely to be very low [3].
There is an information gap on rodent-borne zoonotic helminths in the Middle East countries. Some zoonotic cases of helminths infestation were reported in rodents by some countries in the Middle East, but none involved humans who might have been infected with the same helminths. Humans hymenolepiasis were reported in Bahrain [101], Cyprus [102], Jordan [103], Oman [104], Palestine [105], Qatar [106], and Yemen [107]. The Hymenolepis nana is a common zoonotic helminth transmitted from rodents to humans and the prevalence ranged from 0.15% to 12.2% in some Middle East countries with prevalence of specific countries such as Jordan (1.8%) [103], Oman (5.9%) [104], Palestine (1.0%) [105], Qatar (0.15%) [106], and Yemen (12.2%) [107]. Egg of Hymenolepis diminuta was detected from soil samples of school playgrounds of Jordan [108]. There is no report of rodent hymenolepiasis within these countries. Echinococcus spp. is a major helminth for human health, which was detected in rodents of Egypt, Iran, and Turkey. Human cases of alveolar hydatid cysts were reported from Iran, Kuwait, Saudi Arabia, and Turkey [109,110].
The rodent lungworm, Angiostrongylus cantonensis, causes eosinophilic meningomyelitis in humans, reported in Israel [111]. Gongylonema infection is reported in humans [112] and dromedaries [113] from Iran. Trichinella was a widespread parasite infecting humans and other mammals, although the former makes for a poor host for said organism [6]. There are reports of humans trichinellosis from Iran [114], Israel [115], Lebanon [116], and Turkey [117]. Human cases of trichostrongyliasis infestation were reported in Egypt [118], Iran [119], Israel [120], and Turkey [121]. Eggs of Trichostrongylus sp. were detected from soil samples of public places of Jordan [108] and Iraq [122]. Humans reports of Trichuris trichiura are available from Bahrain [123], Egypt [118], Israel [120], Jordan [103], Oman [104], Palestine [105], Qatar [124], Saudi Arabia [125], Turkey [126], and Yemen [107]. Trichuris muris, the rodent whipworm, does not have any zoonotic importance. Eggs of Trichuris were found in the soil of the public place of Iraq [122]. Trichuris trichiura is not a rodent specific nematode. The report of Trichuris trichiura in Iranian rodents [67] may be a case of accidental infestation.
Schistosoma and Fasciola are two major humans trematodes globally [3]. The high prevalence of Fasciola was recorded in Egypt, Iran, and Yemen [127]. Human cases of schistosomiasis were noted in Egypt [3], Iran [128], Israel [129], Jordan [103], Saudi Arabia [130], Turkey [131], and Yemen [3,132], whereas Heterophyes heterophyes were reported from Egypt and Saudi Arabia [133,134]. There are non-humans (fish, dogs, and cats) reports of Pygidiopsis genata, Haplorchis pumilio, Haplorchis yokogawai, and Heterophyes heterophyes from Egypt, Iran, Iraq, Israel, Palestine, Kuwait, Saudi Arabia, Turkey, UAE, and Yemen [135,136,137,138]. However, these rodent trematodes in the current review were mostly reported from Egypt and Iran.
Based on the meta-analysis, the overall prevalence of rodent trematodes was less than that of nematodes and cestodes in the Middle East, which had received more emphasis in other similar reports [110,127]. Efficient management of water resources are important factor for prevalence of trematode prevalence [139,140]. The presence of deserts means shortage of surface water in some of the countries of Arabian Peninsula such as Bahrain, Kuwait, Oman, Qatar, Saudi Arabia, and United Arab Emirates [141], which may be the cause of shortage of aquatic intermediate hosts of trematodes in these countries. Therefore, rodent trematodes are less reported in these countries. More research should be conducted to find rodent-borne trematodes in the countries of this region.
The reviewed articles in the current study described some of the factors that can influence the population of rodent-borne helminths within the Middle East, necessitating a need to develop a plan of action to control rodent helminths. The abundance of rodent-borne helminths depends on the host organism’s prevalence and its distribution [29,44]. An increase in the rodent population may increase the risk of humans getting infected by rodent parasites [142]. Rodents who inhabit animal farms have easy access to animal feed, and thus, they can be considered a potential vector and reservoir of animal and zoonotic diseases where animals serve as hosts [26]. Hymenolepis diminuta in the rodent are linked with some insects as intermediate hosts, such as Xenopsylla astia, which has a clear seasonal pattern. In Qatar, a research found that rodents are more infested with Hymenolepis diminuta in summer due to the X. astia abundance [24]. Several studies reported that the prevalence of rodent helminths is increased with rodent age [23,24,35,51]. Rodent helminths infestation can change with rodent host species [48]. The nematode, Syphacia obvelata, was reported to be most abundant in Mus musculus [64].
Rodent population control is a primary way to control rodent zoonotic diseases [143,144]. The other contributing factors, such as rodent species, seasons of the year, intermediate host, rodent control management in the residential areas, and animal farms, should also be considered on rodent related zoonoses control. As most of the rodent-related zoonotic helminths are linked to herbivores and carnivores [5,6,86,88], it is vital to manage dogs, cats, and livestock animals to avoid the spread of helminth infestation. Thus, One Health practice comes as a practical approach to control rodent-borne helminth prevalence [145]. “One Health is a collaborative, multisectoral, and transdisciplinary approach - working at the local, regional, national, and global levels—with the goal of achieving optimal health outcomes recognizing the interconnection between people, animals, plants, and their shared environment” [146]. One Health practice by linking veterinary, medical, ecology, entomology, parasitology, zoology fields, and local people are essential for rodent helminths prevention and control.

5. Conclusions

Rodent helminths in the Middle Eastern countries have been documented, which also highlighted rodent-borne zoonotic helminths. Rattus norvegicus, Rattus rattus, and Mus musculus were the most frequently reported rodents and infected with helminth parasites. Out of the 22 rodent-related zoonotic helminths, Capillaria hepatica, H. diminuta, H. nana, and C. fasciolaris were most frequent in this region. The current study illustrates that there is an information gap on the availability, diversity, and dynamics of rodent helminths and their interaction between humans and animals in the Middle East. Thus, the public health importance of rodent-borne helminth parasites is not fully recognized. However, rodent control should be the primary concentration by a One Health approach to control the spread of these helminths at the humans-animal-environmental interface in the countries of this region. We also suggest countrywide and detailed studies be conducted on rodent-borne helminths along with their impact on public health in this region.

Supplementary Materials

The following are available online at https://www.mdpi.com/2076-2615/10/12/2342/s1, Table S1: Prisma checklist, Table S2: Extracted data from the selected 65 studies, Table S3: Prevailing rodents and common cestodes, nematodes, and trematodes in the Middle East.

Author Contributions

Conceptualization, M.M.I., E.F. and Z.M.-K.; methodology, M.M.I., E.F. and M.M.H.; formal analysis, M.M.I. and M.M.H.; writing—original draft preparation, M.M.I., M.M.H. and Z.M.-K.; writing—review and editing, M.M.I., M.M.H., D.B., S.A.A., A.A., H.A.-R. and Z.M.-K.; visualization, D.B., E.F. and Z.M.-K.; supervision, Z.M.-K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

The authors acknowledge the Qatar National Library for providing some full-text articles and partially paying the publication fee.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Macpherson, C.N.L.; Craig, P.S. Parasitic Helminths and Zoonoses in Africa; Springer: Eindhoven, The Netherlands, 1991. [Google Scholar]
  2. Bruschi, F. Helminth Infections and Their Impact on Global Public Health; Springer: Wien, Austria, 2014. [Google Scholar]
  3. Torgerson, P.R.; Macpherson, C.N. The socioeconomic burden of parasitic zoonoses: Global trends. Vet. Parasitol. 2011, 182, 79–95. [Google Scholar] [CrossRef] [PubMed]
  4. Rabiee, M.H.; Mahmoudi, A.; Siahsarvie, R.; Krystufek, B.; Mostafavi, E. Rodent-borne diseases and their public health importance in Iran. PloS Negl. Trop. Dis. 2018, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Centers for Disease Control and Prevention. DPDx A-Z Index. Available online: https://www.cdc.gov/dpdx/az.html (accessed on 5 September 2020).
  6. Dhaliwal, B.B.S.; Juyal, P.D. Parasitic Zoonoses; Springer: New Delhi, India, 2013; pp. 1–135. [Google Scholar]
  7. Meerburg, B.G.; Singleton, G.R.; Kijlstra, A. Rodent-borne diseases and their risks for public health. Crit. Rev. Microbiol. 2009, 35, 221–270. [Google Scholar] [CrossRef] [PubMed]
  8. World Population Review. The Middle East Population. Available online: http://worldpopulationreview.com/continents/the-middle-east-population/ (accessed on 21 November 2019).
  9. Dabrowski, M.; Wulf, L. Economic Development, Trade and Investment in the Eastern and Southern Mediterranean Region. SSRN Electron. J. 2013, 10. [Google Scholar] [CrossRef] [Green Version]
  10. The World Bank. GDP Growth; All Countries and Economies. Available online: https://data.worldbank.org/indicator/NY.GDP.MKTP.KD.ZG (accessed on 21 November 2019).
  11. The World Bank. Palestine’s Economic Update—October 2019. Available online: https://www.worldbank.org/en/country/westbankandgaza/publication/economic-update-october-2019 (accessed on 21 November 2019).
  12. Buliva, E.; Elhakim, M.; Tran Minh, N.N.; Elkholy, A.; Mala, P.; Abubakar, A.; Malik, S.M.M.R. Emerging and Reemerging Diseases in the World Health Organization (WHO) Eastern Mediterranean Region-Progress, Challenges, and WHO Initiatives. Front. Public Health 2017, 5, 276. [Google Scholar] [CrossRef] [PubMed]
  13. Stewart, F. Root causes of violent conflict in developing countries. BMJ 2002, 324, 342–345. [Google Scholar] [CrossRef]
  14. Bannazadeh Baghi, H.; Alinezhad, F.; Kuzmin, I.; Rupprecht, C.E. A Perspective on Rabies in the Middle East-Beyond Neglect. Vet. Sci. 2018, 5, 67. [Google Scholar] [CrossRef] [Green Version]
  15. Hashemi Shahraki, A.; Carniel, E.; Mostafavi, E. Plague in Iran: Its history and current status. Epidemiol. Health 2016, 38. [Google Scholar] [CrossRef]
  16. World Health Organization. Neglected Tropical Diseases. Available online: https://www.who.int/neglected_diseases/diseases/en/ (accessed on 12 September 2020).
  17. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009, 6. [Google Scholar] [CrossRef] [Green Version]
  18. Abd el-Wahed, M.M.; Salem, G.H.; el-Assaly, T.M. The role of wild rats as a reservoir of some internal parasites in Qalyobia governorate. J. Egypt. Soc. Parasitol. 1999, 29, 495–503. [Google Scholar]
  19. Abdel-Gaber, R.; Abdel-Ghaffar, F.; Al Quraishy, S.; Morsy, K.; Saleh, R.; Mehlhorn, H. Morphological Re-Description and 18 S rDNA Sequence Confirmation of the Pinworm Aspiculuris tetraptera (Nematoda, Heteroxynematidae) Infecting the Laboratory Mice Mus musculus. J. Nematol. 2018, 50, 117–132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Abdel-Gaber, R. Syphacia obvelata (Nematode, Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae): Phylogeny and host-parasite relationship. Parasitol. Res. 2016, 115, 975–985. [Google Scholar] [CrossRef]
  21. Abdel-Salam, F.A.; Galal, A.A.; Ali, M.K. The Role of Rodents as a Reservoir of Zoonotic Intestinal Parasites at Sohag Governorate, Egypt. Assiut Vet. Med. J. 1994, 30, 14. [Google Scholar]
  22. Abou-Zinadah, N.Y.; Fouad, M.A. Anti-Fasciola antibodies among rodents and sheep in Jeddah, Saudi Arabia. J. Egypt. Soc. Parasitol. 2005, 35, 711–716. [Google Scholar] [PubMed]
  23. Abu-Madi, M.A.; Behnke, J.M.; Mikhail, M.; Lewis, J.W.; Al-Kaabi, M.L. Parasite populations in the brown rat Rattus norvegicus from Doha, Qatar between years: The effect of host age, sex and density. J. Helminthol. 2005, 79, 105–111. [Google Scholar] [CrossRef]
  24. Abu-Madi, M.A.; Lewis, J.W.; Mikhail, M.; El-Nagger, M.E.; Behnke, J.M. Monospecific helminth and arthropod infections in an urban population of brown rats from Doha, Qatar. J. Helminthol. 2001, 75, 313–320. [Google Scholar] [CrossRef]
  25. Al Hindi, A.I.; Abu-Haddaf, E. Gastrointestinal parasites and ectoparasites biodiversity of Rattus rattus trapped from Khan Younis and Jabalia in Gaza strip, Palestine. J. Egypt. Soc. Parasitol. 2013, 43, 259–268. [Google Scholar] [CrossRef]
  26. Allymehr, M.; Tavassoli, M.; Manoochehri, M.H.; Ardavan, D. Ectoparasites and Gastrointestinal Helminths of House Mice (Mus musculus) from Poultry Houses in Northwest Iran. Comp. Parasitol. 2012, 79, 283–287. [Google Scholar] [CrossRef]
  27. Al-Quraishy, S.; Gewik, M.M.; Abdel-Baki, A.A. The intestinal cestode Hymenolepis diminuta as a lead sink for its rat host in the industrial areas of Riyadh, Saudi Arabia. Saudi J. Biol. Sci. 2014, 21, 387–390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Al-Qureishy, S. Lead concentrations in some organs of the rat Meriones libycus and its parasite Hymenolepis diminuta from Riyadh City, KSA. J. Egypt. Soc. Parasitol. 2008, 38, 351–358. [Google Scholar]
  29. Antoniou, M.; Psaroulaki, A.; Toumazos, P.; Mazeris, A.; Ioannou, I.; Papaprodromou, M.; Georgiou, K.; Hristofi, N.; Patsias, A.; Loucaides, F.; et al. Rats as Indicators of the Presence and Dispersal of Pathogens in Cyprus: Ectoparasites, Parasitic Helminths, Enteric Bacteria, and Encephalomyocarditis Virus. Vector Borne Zoonotic Dis. 2010, 10, 867–873. [Google Scholar] [CrossRef]
  30. Arzamani, K.; Salehi, M.; Mobedi, I.; Adinezade, A.; Hasanpour, H.; Alavinia, M.; Darvish, J.; Shirzadi, M.R.; Mohammadi, Z. Intestinal Helminths in Different Species of Rodents in North Khorasan Province, Northeast of Iran. Iran. J. Parasitol. 2017, 12, 267–273. [Google Scholar]
  31. Ashour, A.A.; Lewis, J.W. Gongylonema aegypti n. sp. (Nematoda: Thelaziidae) from Egyptian rodents. Syst. Parasitol. 1986, 8, 199–206. [Google Scholar] [CrossRef]
  32. Avcioglu, H.; Guven, E.; Balkaya, I.; Kirman, R.; Bia, M.M.; Gulbeyen, H.; Kurt, A.; Yaya, S.; Demirtas, S. First detection of Echinococcus multilocularis in rodent intermediate hosts in Turkey. Parasitology 2017, 144, 1821–1827. [Google Scholar] [CrossRef]
  33. Azzam, K.M.; Abd El-Hady, E.A.; El-Abd, N. Survey of Natural Infection with Echinostoma liei in Aquatic Snails and Wild Rodents in Egypt. Egypt. J. Biol. Pest. Control. 2015, 25, 427–432. [Google Scholar]
  34. Azzam, K.M.; El-Abd, N.M.; Abd El-Hady, E.A. Survey of endoparasites of different rodent species in Egypt. Egypt. J. Biol. Pest. Control. 2016, 26, 815–820. [Google Scholar]
  35. Behnke, J.M.; Barnard, C.J.; Mason, N.; Harris, P.D.; Sherif, N.E.; Zalat, S.; Gilbert, F.S. Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St Katherine’s Protectorate in the Sinai, Egypt. J. Helminthol. 2000, 74, 31–43. [Google Scholar] [CrossRef] [Green Version]
  36. Behnke, J.M.; Harris, P.D.; Bajer, A.; Barnard, C.J.; Sherif, N.; Cliffe, L.; Hurst, J.; Lamb, M.; Rhodes, A.; James, M.; et al. Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St Katherine region of the Sinai Peninsula in Egypt. Parasitology 2004, 129, 379–398. [Google Scholar] [CrossRef]
  37. Beiromvand, M.; Akhlaghi, L.; Fattahi Massom, S.H.; Meamar, A.R.; Darvish, J.; Razmjou, E. Molecular Identification of Echinococcus multilocularis Infection in Small Mammals from Northeast, Iran. PLoS Negl. Trop. Dis. 2013, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Borji, H.; Khoshnegah, J.; Razmi, G.; Amini, H.; Shariatzadeh, M. A survey on intestinal parasites of golden hamster (Mesocricetus auratus) in the northeast of Iran. J. Parasit. Dis. 2014, 38, 265–268. [Google Scholar] [CrossRef] [Green Version]
  39. Celebi, B.; Taylan Ozkan, A.; Babur, C. Capillaria Hhepatica in mouse (Apodemus flavicollis) from Giresun Province of Turkey. Turk. Parazitol. Derg. 2014, 38, 208–210. [Google Scholar] [CrossRef]
  40. Ebrahimi, M.; Sharifi, Y.; Nematollahi, A. Assessment of gastrointestinal helminths among house mice (Mus musculus) caught in the north-west of Iran, with a special view on zoonotic aspects. Comp. Clin. Pathol. 2016, 25, 1047–1051. [Google Scholar] [CrossRef]
  41. El Gindy, M.S.; Morsy, T.A.; Bebars, M.A.; Sarwat, M.A.; Arafa, M.A.; Salama, M.M. Rodents as reservoir of zoonotic intestinal helminths in Suez Canal Zone with the possible immunological changes. J. Egypt. Soc. Parasitol. 1987, 17, 259–273. [Google Scholar]
  42. El Kady, G.A.; Gheneam, Y.M.; Bahgat, I.M. Zoonotic helminthes of commensal rodents in Talkha Center, Dakahlia Governorate. J. Egypt. Soc. Parasitol. 2008, 38, 863–872. [Google Scholar]
  43. El Shazly, A.M.; Morsy, T.A.; el Kady, G.A.; Ragheb, D.A.; Handousa, A.E.; Ahmed, M.M.; Younis, T.A.; Habib, K.S. The helminthic parasites of rodents in Dakahlia Governorate, with reference to their Egyptian helminth fauna. J. Egypt. Soc. Parasitol. 1994, 24, 413–428. [Google Scholar]
  44. Elshazly, A.M.; Awad, S.I.; Azab, M.S.; Elsheikha, H.M.; Abdel-Gawad, A.G.; Khalil, H.H.; Morsy, T.A. Helminthes of synanthropic rodents (Rodentia: Muridae) from Dakahlia and Menoufia, Egypt. J. Egypt. Soc. Parasitol. 2008, 38, 727–740. [Google Scholar] [PubMed]
  45. El-Shazly, A.M.; Romia, S.A.; el Ganayni, G.A.; Abou-Zakham, A.A.; Sabry, A.H.; Morsy, T.A. Antibodies against some zoonotic parasites in commensal rodents trapped from Dakahlia Governorate, Egypt. J. Egypt. Soc. Parasitol. 1991, 21, 169–177. [Google Scholar] [PubMed]
  46. Fair, J.M.; Schmidt, G.D.; Wertheim, G. New species of Andrya and Paranoplocephala (Cestoidea: Anoplocephalidae) from voles and mole-rats in Israel and Syria. J. Parasitol. 1990, 76, 641–644. [Google Scholar] [CrossRef]
  47. Fasihi Harandi, M.; Madjdzadeh, S.M.; Ahmadinejad, M. Helminth parasites of small mammals in Kerman province, southeastern Iran. J. Parasit. Dis. 2016, 40, 106–109. [Google Scholar] [CrossRef]
  48. Garedaghi, Y.; Afshin Khaki, A. Prevalence of Gastrointestinal and Blood Parasites of Rodents in Tabriz, Iran, with Emphasis on Parasitic Zoonoses. Crescent J. Med. Biol. Sci. 2014, 1, 9–12. [Google Scholar]
  49. Gholipoury, M.; Rezai, H.R.; Namroodi, S.; Arab Khazaeli, F. Zoonotic and Non-zoonotic Parasites of Wild Rodents in Turkman Sahra, Northeastern Iran. Iran. J. Parasitol. 2016, 11, 350–357. [Google Scholar]
  50. Greenberg, Z. Helminths of mammals and birds of israel i. helminths of acomys spp. (Rodentia, Murinae). Isr. J. Ecol. Evol. 1969, 18, 25–38. [Google Scholar] [CrossRef]
  51. Gurler, A.T.; Beyhan, Y.E.; Bolukbas, C.S.; Acici, M.; Umur, S. Gastro-intestinal helminths of wild rats (brown rat-Rattus norvegicus, Berkenhout 1769) in Samsun, Turkey. Ank. Univ. Vet. Fak. Derg. 2011, 58, 289–290. [Google Scholar] [CrossRef]
  52. Haridy, F.M.; Morsy, T.A.; Ibrahim, B.B.; Abdel Gawad, A.G.; Mazyad, S.A. Rattus rattus: A new host for fascioliasis. J. Egypt. Soc. Parasitol. 2003, 33, 647–648. [Google Scholar] [PubMed]
  53. Hasson, R.H. Zoonotic &Nonzoonotic Endoparasites of Rodents from Some Districts in Baghdad. Diyala J. Pure Sci. 2010, 6, 11. [Google Scholar]
  54. Jones, A.; El-Azazy, O.M.E. Coelomotrema aegyptiaca sp, nov., an unusual prosthogonimid trematode from Rattus norvegicus (berkenhout) in Egypt. J. Nat. Hist. 1986, 20, 707–712. [Google Scholar] [CrossRef]
  55. Kamranrashani, B.; Kia, E.; Mobedi, I.; Mohebali, M.; Zarei, Z.; Mowlavi, G.; Hajjaran, H.; Abai, M.; Sharifdini, M.; Kakooei, Z.; et al. Helminth Parasites of Rhombomys opimus from Golestan Province, Northeast Iran. Iran. J. Parasitol. 2013, 8, 78–84. [Google Scholar]
  56. Khajeh, A.; Mohammadi, Z.; Darvish, J.; Razmi, G.R.; Ghorbani, F.; Mohammadi, A.; Mobedi, I.; Shahrokhi, A.R. A survey on endoparasites in wild rodents of the Jaz Murian depression and adjacent areas, southeast of Iran. J. Parasit. Dis. 2018, 42, 589–597. [Google Scholar] [CrossRef]
  57. Khalil, L.F.; Hassounah, O.; Behbehani, K. Helminth parasites of rodents in Kuwait with the description of a new species Abbreviata kuwaitensis (Nematoda: Physalopteridae). Syst. Parasitol. 1979, 1, 67–73. [Google Scholar] [CrossRef]
  58. Kia, E.B.; Homayouni, M.M.; Farahnak, A.; Mohebai, M.; Shojai, S. Study of Endoparasites of Rodents and their Zoonotic Importance In Ahvaz, South West Iran. Iran. J. Public Health 2001, 30, 4. [Google Scholar]
  59. Kia, E.; Shahryary-Rad, E.; Mohebali, M.; Mahmoudi, M.; Mobedi, I.; Zahabiun, F.; Zarei, Z.; Miahipoor, A.; Mowlavi, G.; Akhavan, A.; et al. Endoparasites of rodents and their zoonotic importance in germi, dashte-mogan, ardabil province, Iran. Iran. J. Parasitol. 2010, 5, 15–20. [Google Scholar]
  60. Meshkekar, M.; Sadraei, J.; Mahmoodzadeh, A.; Mobedi, I. Helminth Infections in Rattus ratus and Rattus norvigicus in Tehran, Iran. Iran. J. Parasitol. 2014, 9, 548–552. [Google Scholar]
  61. Metwally, D.M.; Al-Enezy, H.A.; Al-Turaiki, I.M.; El-Khadragy, M.F.; Yehia, H.M.; Al-Otaibi, T.T. Gene-based molecular characterization of cox1 and pnad5 in Hymenolepis nana isolated from naturally infected mice and rats in Saudi Arabia. Biosci. Rep. 2019, 39. [Google Scholar] [CrossRef] [Green Version]
  62. Mikhail, M.W.; Metwally, A.M.; Allam, K.A.; Mohamed, A.S. Rodents as reservoir host of intestinal helminthes in different Egyptian agroecosystems. J. Egypt. Soc. Parasitol. 2009, 39, 633–640. [Google Scholar]
  63. Mirjalali, H.; Kia, E.B.; Kamranrashani, B.; Hajjaran, H.; Sharifdini, M. Molecular analysis of isolates of the cestode Rodentolepis nana from the great gerbil, Rhombomys opimus. J. Helminthol. 2016, 90, 252–255. [Google Scholar] [CrossRef]
  64. Moradpour, N.; Borji, H.; Darvish, J.; Moshaverinia, A.; Mahmoudi, A. Rodents Helminth Parasites in Different Region of Iran. Iran. J. Parasitol. 2018, 13, 275–284. [Google Scholar]
  65. Morsy, T.A.; Michael, S.A.; Bassili, W.R.; Saleh, M.S. Studies on rodents and their zoonotic parasites, particularly leishmania, in Ismailiya Governorate, A.R. Egypt. J. Egypt. Soc. Parasitol. 1982, 12, 565–585. [Google Scholar]
  66. Mowlavi, G.; Mobedi, I.; Abedkhojasteh, H.; Sadjjadi, S.M.; Shahbazi, F.; Massoud, J. Plagiorchis muris (Tanabe, 1922) in Rattus norvegicus in Iran. Iran. J. Parasitol. 2013, 8, 486–490. [Google Scholar]
  67. Nateghpour, M.; Motevalli-Haghi, A.; Akbarzadeh, K.; Akhavan, A.A.; Mohebali, M.; Mobedi, I.; Farivar, L. Endoparasites of wild rodents in Southeastern Iran. J. Arthropod Borne Dis. 2014, 9, 1–6. [Google Scholar]
  68. Pakdel, N.; Naem, S.; Rezaei, F.; Chalehchaleh, A.A. A survey on helminthic infection in mice (Mus musculus) and rats (Rattus norvegicus and Rattus rattus) in Kermanshah, Iran. Vet. Res. Forum Int. Q. J. 2013, 4, 105–109. [Google Scholar]
  69. Ranjbar, M.J.; Sarkari, B.; Mowlavi, G.R.; Seifollahi, Z.; Moshfe, A.; Abdolahi Khabisi, S.; Mobedi, I. Helminth Infections of Rodents and Their Zoonotic Importance in Boyer-Ahmad District, Southwestern Iran. Iran. J. Parasitol. 2017, 12, 572–579. [Google Scholar]
  70. Sadighian, A.; Ghadirian, E.; Sadjadpour, E. Two new species of nematodes of lagomorphs and rodents from Iran. J. Helminthol. 1974, 48, 241–245. [Google Scholar] [CrossRef] [PubMed]
  71. Saoud, M.F.; Ramadan, M.M.; Ashour, A.A.; Shahawy, A.A. On the helminth parasites of rodents in the Eastern Delta. I. General survey. J. Egypt. Soc. Parasitol. 1986, 16, 197–209. [Google Scholar]
  72. Soliman, M.F.; Ibrahim, M.M.; Zalat, S.M. Gastrointestinal nematode community of spiny mice (Acomys dimidiatus) from St. Katherine, South Sinai, Egypt. J. Parasit. Dis. 2015, 39, 705–711. [Google Scholar] [CrossRef] [Green Version]
  73. Sures, B.; Scheible, T.; Bashtar, A.R.; Taraschewski, H. Lead concentrations in Hymenolepis diminuta adults and Taenia taeniaeformis larvae compared to their rat hosts (Rattus norvegicus) sampled from the city of Cairo, Egypt. Parasitology 2003, 127, 483–487. [Google Scholar] [CrossRef] [PubMed]
  74. Sursal, N.; Gokpinar, S.; Yildiz, K. Prevalence of intestinal parasites in hamsters and rabbits in some pet shops of Turkey. Turk. Parazitol. Derg. 2014, 38, 102–105. [Google Scholar] [CrossRef]
  75. Wanas, M.Q.; Shehata, K.K.; Rashed, A.A. Larval occurrence of Hydatigera taeniaeformis Batsch (1786) (Cestoda: Taeniidae) in the liver of wild rodents in Egypt. J. Egypt. Soc. Parasitol. 1993, 23, 381–388. [Google Scholar]
  76. Mohamed; Wanas, Q.A.; Shehata, K.K.; Rashed, A.A. Studies on the nematode parasites from Egyptian rodents. I. Spirurid nematodes. J. Egypt. Soc. Parasitol. 1994, 23, 851–863. [Google Scholar]
  77. Wertheim, G.; Chabaud, A.G. Helminths of birds and mammals of Israel. VIII.—Skrjabinocapillaria rodentium n. sp. (Nematoda Capillariidae) from gerbillid and murid rodents. Ann. De Parasitol. Hum. Comp. 1979, 54, 65–68. [Google Scholar] [CrossRef] [Green Version]
  78. Wertheim, G.; Giladi, M. Helminths of birds and mammals of Israel. VII.—Pneumospirura rodentium n. sp. (Pneumospiruridae-Thelazioidea). Ann. Parasitol. Hum. Comp. 1977, 52, 643–646. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Wertheim, G. Helminths of Birds and Mammals from Israel: III. Helminths from Chromosomal Forms of the Mole-Rat, Spalax ehrenbergi. J. Helminthol. 1971, 45, 161–169. [Google Scholar] [CrossRef]
  80. Yousefi, A.; Eslami, A.; Mobedi, I.; Rahbari, S.; Ronaghi, H. Helminth Infections of House Mouse (Mus musulus) and Wood Mouse (Apodemus sylvaticus) from the Suburban Areas of Hamadan City, Western Iran. Iran. J. Parasitol. 2014, 9, 511–518. [Google Scholar]
  81. Yousif, F.; Ibrahim, A. The first record of Angiostrongylus cantonensis from Egypt. Z. Parasitenkdunde 1978, 56, 73–80. [Google Scholar] [CrossRef] [PubMed]
  82. Zarei, Z.; Mohebali, M.; Heidari, Z.; Davoodi, J.; Shabestari, A.; Haghi, A.M.; Khanaliha, K.; Kia, E.B. Helminth infections of meriones persicus (Persian jird), Mus musculus (house mice) and cricetulus migratorius (grey ham-ster): A cross-sectional study in Meshkin-Shahr district, north-west Iran. Iran. J. Parasitol. 2016, 11, 213–220. [Google Scholar]
  83. Nijsten, T.; Stern, R.S. How Epidemiology Has Contributed to a Better Understanding of Skin Disease. J. Investig. Dermatol. 2012, 132, 994–1002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Neta, G.; Brownson, R.C.; Chambers, D.A. Opportunities for Epidemiologists in Implementation Science: A Primer. Am. J. Epidemiol. 2018, 187, 899–910. [Google Scholar] [CrossRef]
  85. Higgins, J.P.; Thompson, S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002, 21, 1539–1558. [Google Scholar] [CrossRef]
  86. Chatterjee, K.D. Parasitology: Protozoology and Helminthology in Relation to Clinical Medicine: With Two Hundred Fourteen Illustrations; CBS Publishers & Distributors: New Delhi, India, 2012. [Google Scholar]
  87. Gárate, I.; Jimenez, P.; Flores, K.; Espinoza, B. Xenopsylla cheopis record as natural intermediate host of Hymenolepis diminuta in Lima, Peru. Rev. Peru. Biol. 2011, 18, 249–252. [Google Scholar] [CrossRef] [Green Version]
  88. Stĕrba, J.; Barus, V. First record of Strobilocercus fasciolaris (Taenidae-larvae) in man. Folia Parasitol. 1976, 23, 221–226. [Google Scholar]
  89. Toledo, R.; Esteban, J.G. An update on human echinostomiasis. Trans. R. Soc. Trop. Med. Hyg. 2016, 110, 37–45. [Google Scholar] [CrossRef]
  90. Boyce, K. Transmission Ecology of Gastrointestinal Trematodes of Small Mammals, Malham Tarn, North Yorkshire, UK. Ph.D. Thesis, University of Salford, Salford, UK, July 2013. [Google Scholar]
  91. Loftis, A.D.; Reeves, W.K.; Szumlas, D.E.; Abbassy, M.M.; Helmy, I.M.; Moriarity, J.R.; Dasch, G.A. Surveillance of Egyptian fleas for agents of public health significance: Anaplasma, bartonella, coxiella, ehrlichia, rickettsia, and Yersinia pestis. Am. J. Trop. Med. Hyg. 2006, 75, 41–48. [Google Scholar] [CrossRef] [Green Version]
  92. Trevisanato, S.I. The ‘Hittite plague’, an epidemic of tularemia and the first record of biological warfare. Med. Hypotheses 2007, 69, 1371–1374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Bishara, J.; Hershkovitz, D.; Yagupsky, P.; Lazarovitch, T.; Boldur, I.; Kra-Oz, T.; Pitlik, S. Murine typhus among Arabs and Jews in Israel 1991–2001. Eur. J. Epidemiol. 2004, 19, 1123–1126. [Google Scholar] [CrossRef] [PubMed]
  94. Rosenthal, T.; Michaeli, D. Murine typhus and spotted fever in Israel in the seventies. Infection 1977, 5, 82–84. [Google Scholar] [CrossRef] [PubMed]
  95. Khaghani, R. The economic and health impact of rodent in urban zone and harbours and their control methods. Ann. Mil. Health Sci. Res. 2007, 4, 1071–1078. [Google Scholar]
  96. Morand, S.; Bordes, F. Parasite diversity of disease-bearing rodents of Southeast Asia: Habitat determinants and effects on sexual size dimorphism and life-traits. Front. Ecol. Evol. 2015, 3. [Google Scholar] [CrossRef] [Green Version]
  97. Radostits, O.M.; Done, S.H. Veterinary Medicine: A Textbook of the Diseases of Cattle, Sheep, Pigs, Goats, and Horses; Elsevier Saunders: Philadelphia, PA, USA, 2007. [Google Scholar]
  98. Rodan, I.; Sparkes, A.H. Chapter 8-Preventive Health Care for Cats. In The Cat, Little, S.E., Ed.; W.B. Saunders: Saint Louis, MO, USA, 2012; pp. 151–180. [Google Scholar] [CrossRef]
  99. Dorny, P.; Praet, N.; Deckers, N.; Gabriel, S. Emerging food-borne parasites. Vet. Parasitol. 2009, 163, 196–206. [Google Scholar] [CrossRef]
  100. Youn, H. Review of zoonotic parasites in medical and veterinary fields in the Republic of Korea. Korean J. Parasitol. 2009, 47, S133–S141. [Google Scholar] [CrossRef]
  101. Amin, O.M. Pathogenic micro-organisms and helminths in sewage products, Arabian Gulf, country of Bahrain. Am. J. Public Health 1988, 78, 314–315. [Google Scholar] [CrossRef] [Green Version]
  102. Berger, S. Infectious Diseases of Cyprus; Incorporated Gideon e-book series; Global Infectious Diseases and Epidemiology Network Informatics: Winconsin, WI, USA, 2019. [Google Scholar]
  103. Al-Lahham, A.B.; Abu-Saud, M.; Shehabi, A.A. Prevalence of Salmonella, Shigella and intestinal parasites in food handlers in Irbid, Jordan. J. Diarrhoeal Dis Res. 1990, 8, 160–162. [Google Scholar]
  104. Patel, P.K.; Khandekar, R. Intestinal parasitic infections among school children of the Dhahira Region of Oman. Saudi Med. J. 2006, 27, 627–632. [Google Scholar]
  105. Astal, Z. Epidemiological survey of the prevalence of parasites among children in Khan Younis governorate, Palestine. Parasitol. Res. 2004, 94, 449–451. [Google Scholar] [CrossRef]
  106. Abu-Madi, M.A.; Behnke, J.M.; Boughattas, S.; Al-Thani, A.; Doiphode, S.H.; Deshmukh, A. Helminth infections among long-term-residents and settled immigrants in Qatar in the decade from 2005 to 2014: Temporal trends and varying prevalence among subjects from different regional origins. Parasites Vectors 2016, 9, 153. [Google Scholar] [CrossRef] [Green Version]
  107. Alharbi, R.A.; Alwajeeh, T.S.; Assabri, A.M.; Almalki, S.S.R.; Alruwetei, A.; Azazy, A.A. Intestinal parasitoses and schistosome infections among students with special reference to praziquantel efficacy in patients with schistosomosis in Hajjah governorate, Yemen. Ann. Parasitol. 2019, 65, 217–223. [Google Scholar] [CrossRef]
  108. Abo-Shehada, M.N. Prevalence of Toxocara ova in some schools and public grounds in northern and central Jordan. Ann. Trop Med. Parasitol. 1989, 83, 73–75. [Google Scholar] [CrossRef]
  109. Geramizadeh, B.; Baghernezhad, M. Hepatic Alveolar Hydatid Cyst: A Brief Review of Published Cases from Iran in the Last 20 Years. Hepat Mon. 2016, 16. [Google Scholar] [CrossRef] [Green Version]
  110. Al-Aboody, M.S.; Omar, M.A.; Alsayeqh, A.F. Epizootiology of zoonotic parasites in Middle East: A comprehensive review. Ann. Parasitol. 2020, 66, 125–133. [Google Scholar] [CrossRef] [PubMed]
  111. Fellner, A.; Hellmann, M.A.; Kolianov, V.; Bishara, J. A non-travel related case of Angiostrongylus cantonensis eosinophilic meningomyelitis acquired in Israel. J. Neurol. Sci. 2016, 370, 241–243. [Google Scholar] [CrossRef]
  112. Molavi, G.H.; Massoud, J.; Gutierrez, Y. Human Gongylonema infection in Iran. J. Helminthol. 2006, 80, 425–428. [Google Scholar] [CrossRef]
  113. Mirzayans, A.; Halim, R. Parasitic infection of Camelus dromedarius from Iran. Bull. Soc. Pathol Exot. Fil. 1980, 73, 442–445. [Google Scholar]
  114. Moazeni, M.; Khamesipour, F.; Anyona, D.N.; Dida, G.O. Epidemiology of taeniosis, cysticercosis and trichinellosis in Iran: A systematic review. Zoonoses Public Health 2019, 66, 140–154. [Google Scholar] [CrossRef]
  115. Eisenman, A.; Einat, R. A family outbreak of trichinosis acquired in Israel. Harefuah 1992, 122, 702–704, 751. [Google Scholar] [PubMed]
  116. Haim, M.; Efrat, M.; Wilson, M.; Schantz, P.M.; Cohen, D.; Shemer, J. An outbreak of Trichinella spiralis infection in southern Lebanon. Epidemiol. Infect. 1997, 119, 357–362. [Google Scholar] [CrossRef]
  117. Turk, M.; Kaptan, F.; Turker, N.; Korkmaz, M.; El, S.; Ozkaya, D.; Ural, S.; Vardar, I.; Alkan, M.Z.; Coskun, N.A.; et al. Clinical and laboratory aspects of a trichinellosis outbreak in Izmir, Turkey. Parasite 2006, 13, 65–70. [Google Scholar] [CrossRef] [Green Version]
  118. El Shazly, A.M.; Awad, S.E.; Sultan, D.M.; Sadek, G.S.; Khalil, H.H.; Morsy, T.A. Intestinal parasites in Dakahlia governorate, with different techniques in diagnosing protozoa. J. Egypt. Soc. Parasitol. 2006, 36, 1023–1034. [Google Scholar]
  119. Ghanbarzadeh, L.; Saraei, M.; Kia, E.B.; Amini, F.; Sharifdini, M. Clinical and haematological characteristics of human trichostrongyliasis. J. Helminthol. 2019, 93, 149–153. [Google Scholar] [CrossRef]
  120. Greenberg, Z.; Giladi, L.; Bashary, A.; Zahavi, H. Prevalence of intestinal parasites among Thais in Israel. Harefuah 1994, 126, 507–509, 563. [Google Scholar]
  121. Akdemir, C.; Helvaci, R. Evaluation of parasitology laboratory results of a group of people older than 15 years of age in Kutahya. Turk. Parazit. Derg. 2007, 31, 129–132. [Google Scholar]
  122. Nooraldeen, K. Contamination of public squares and parks with parasites in Erbil city, Iraq. Ann. Agric. Environ. Med. 2015, 22, 418–420. [Google Scholar] [CrossRef] [Green Version]
  123. Mukhtar, A. Intestinal parasites in the state of Bahrain. Indian J. Pathol. Microbiol. 1995, 38, 341–344. [Google Scholar] [PubMed]
  124. Abu-Madi, M.A.; Behnke, J.M.; 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, 213–220. [Google Scholar] [CrossRef]
  125. Amer, O.S.O.; Al-Malki, E.S.; Waly, M.I.; AlAgeel, A.; Lubbad, M.Y. Prevalence of Intestinal Parasitic Infections among Patients of King Fahd Medical City in Riyadh Region, Saudi Arabia: A 5-Year Retrospective Study. J. Parasitol. Res. 2018, 2018. [Google Scholar] [CrossRef] [PubMed]
  126. Yentur Doni, N.; Yildiz Zeyrek, F.; Simsek, Z.; Gurses, G.; Sahin, I. Risk Factors and Relationship Between Intestinal Parasites and the Growth Retardation and Psychomotor Development Delays of Children in Sanliurfa, Turkey. Turk. Parazitol. Derg. 2015, 39, 270–276. [Google Scholar] [CrossRef]
  127. Hotez, P.J.; Savioli, L.; Fenwick, A. Neglected tropical diseases of the Middle East and North Africa: Review of their prevalence, distribution, and opportunities for control. PLoS Negl. Trop. Dis. 2012, 6. [Google Scholar] [CrossRef] [Green Version]
  128. Rollinson, D.; Knopp, S.; Levitz, S.; Stothard, J.R.; Tchuem Tchuente, L.A.; Garba, A.; Mohammed, K.A.; Schur, N.; Person, B.; Colley, D.G.; et al. Time to set the agenda for schistosomiasis elimination. Acta Trop. 2013, 128, 423–440. [Google Scholar] [CrossRef]
  129. Hornstein, L.; Lederer, G.; Schechter, J.; Greenberg, Z.; Boem, R.; Bilguray, B.; Giladi, L.; Hamburger, J. Persistent Schistosoma mansoni infection in Yemeni immigrants to Israel. Isr. J. Med. Sci. 1990, 26, 386–389. [Google Scholar] [PubMed]
  130. Taha, H.A.; Soliman, M.I.; Banjar, S.A. Intestinal parasitic infections among expatriate workers in Al-Madina Al-Munawarah, Kingdom of Saudi Arabia. Trop Biomed. 2013, 30, 78–88. [Google Scholar]
  131. Kiremit, M.C.; Cakir, A.; Arslan, F.; Ormeci, T.; Erkurt, B.; Albayrak, S. The bladder carcinoma secondary to schistosoma mansoni infection: A case report with review of the literature. Int. J. Surg. Case. Rep. 2015, 13, 76–78. [Google Scholar] [CrossRef] [Green Version]
  132. Al-Mekhlafi, A.M.; Abdul-Ghani, R.; Al-Eryani, S.M.; Saif-Ali, R.; Mahdy, M.A. School-based prevalence of intestinal parasitic infections and associated risk factors in rural communities of Sana’a, Yemen. Acta Trop. 2016, 163, 135–141. [Google Scholar] [CrossRef]
  133. El-Shazly, A.M.; el-Nahas, H.A.; Soliman, M.; Sultan, D.M.; Abedl Tawab, A.H.; Morsy, T.A. The reflection of control programs of parasitic diseases upon gastrointestinal helminthiasis in Dakahlia Governorate, Egypt. J. Egypt. Soc. Parasitol. 2006, 36, 467–480. [Google Scholar]
  134. Chai, J.Y.; Seo, B.S.; Lee, S.H.; Hong, S.J.; Sohn, W.M. Human infections by Heterophyes heterophyes and H. dispar imported from Saudi Arabia. Kisaengchunghak Chapchi 1986, 24, 82–86. [Google Scholar] [CrossRef]
  135. Chai, J.Y.; Jung, B.K. Foodborne intestinal flukes: A brief review of epidemiology and geographical distribution. Acta Trop. 2019, 201. [Google Scholar] [CrossRef]
  136. El-Gayar, A.K. Studies on some trematode parasites of stray dogs in Egypt with a key to the identification of intestinal trematodes of dogs. Vet. Parasitol. 2007, 144, 360–365. [Google Scholar] [CrossRef]
  137. El-Azazy, O.M.; Abdou, N.E.; Khalil, A.I.; Al-Batel, M.K.; Majeed, Q.A.; Henedi, A.A.; Tahrani, L.M. Potential Zoonotic Trematodes Recovered in Stray Cats from Kuwait Municipality, Kuwait. Korean J. Parasitol. 2015, 53, 279–287. [Google Scholar] [CrossRef]
  138. Khalil, M.I.; El-Shahawy, I.S.; Abdelkader, H.S. Studies on some fish parasites of public health importance in the southern area of Saudi Arabia. Rev. Bras. Parasitol. Vet. 2014, 23, 435–442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  139. Steinmann, P.; Keiser, J.; Bos, R.; Tanner, M.; Utzinger, J. Schistosomiasis and water resources development: Systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 2006, 6, 411–425. [Google Scholar] [CrossRef]
  140. El-Sayed, H.F.; Rizkalla, N.H.; Mehanna, S.; Abaza, S.M.; Winch, P.J. Prevalence and epidemiology of Schistosoma mansoni and S. haematobium infection in two areas of Egypt recently reclaimed from the desert. Am. J. Trop. Med. Hyg. 1995, 52, 194–198. [Google Scholar] [CrossRef]
  141. Odhiambo, G.O. Water scarcity in the Arabian Peninsula and socio-economic implications. Appl. Water Sci. 2017, 7, 2479–2492. [Google Scholar] [CrossRef] [Green Version]
  142. Bordes, F.; Blasdell, K.; Morand, S. Transmission ecology of rodent-borne diseases: New frontiers. Integr. Zool. 2015, 10, 424–435. [Google Scholar] [CrossRef]
  143. Eisen, R.J.; Enscore, R.E.; Atiku, L.A.; Zielinski-Gutierrez, E.; Mpanga, J.T.; Kajik, E.; Andama, V.; Mungujakisa, C.; Tibo, E.; MacMillan, K.; et al. Evidence that rodent control strategies ought to be improved to enhance food security and reduce the risk of rodent-borne illnesses within subsistence farming villages in the plague-endemic West Nile region, Uganda. Int. J. Pest. Manag. 2013, 59, 259–270. [Google Scholar] [CrossRef]
  144. Brown, L.M.; Laco, J. Rodent Control and Public Health: A Description of Local Rodent Control Programs. J. Environ. Health 2015, 78, 28–29. [Google Scholar]
  145. Kaplan, B.; Kahn, L.H.; Monath, T.P.; Woodall, J. ‘ONE HEALTH’ and parasitology. Parasites Vectors 2009, 2, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  146. Centers for Disease Control and Prevention. One Health Basics. Available online: https://www.cdc.gov/onehealth/basics/ (accessed on 2 October 2020).
Animals 10 02342 g001 550
Figure 1. Systematic review PRISMA flow diagram describing the selection of published articles on rodent helminths in the Middle East and inclusion/exclusion process used in the study.
Figure 1. Systematic review PRISMA flow diagram describing the selection of published articles on rodent helminths in the Middle East and inclusion/exclusion process used in the study.
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Animals 10 02342 g002 550
Figure 2. The map depicted the Middle East countries with the total number of studies and the number of helminths detected in rodents.
Figure 2. The map depicted the Middle East countries with the total number of studies and the number of helminths detected in rodents.
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Animals 10 02342 g003 550
Figure 3. Forest plot of the prevalence estimates of cestode in rodents among the Middle East countries (the center dot representing point estimates whereas Gray Square representing the weight of each study to the meta-analysis).
Figure 3. Forest plot of the prevalence estimates of cestode in rodents among the Middle East countries (the center dot representing point estimates whereas Gray Square representing the weight of each study to the meta-analysis).
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Animals 10 02342 g004 550
Figure 4. Forest plot of the prevalence estimates of nematode in rodents among the Middle East countries (the center dot representing point estimates whereas Gray Square representing the weight of each study to the meta-analysis).
Figure 4. Forest plot of the prevalence estimates of nematode in rodents among the Middle East countries (the center dot representing point estimates whereas Gray Square representing the weight of each study to the meta-analysis).
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Animals 10 02342 g005 550
Figure 5. Forest plot of the prevalence estimates of trematode in rodents among the Middle East countries (the center dot representing point estimates, whereas Gray Square representing the weight of each study to the meta-analysis).
Figure 5. Forest plot of the prevalence estimates of trematode in rodents among the Middle East countries (the center dot representing point estimates, whereas Gray Square representing the weight of each study to the meta-analysis).
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Table
Table 1. Estimated pooled prevalence of the rodent helminths in the Middle East countries.
Table 1. Estimated pooled prevalence of the rodent helminths in the Middle East countries.
CountryParasitePooled Estimates (%)95% CIHeterogeneity Chi-Squared (χ2)l2%p-Value
CyprusNematode0.160−0.15–0.470.000-
Cestode14.7211.94–17.500.000-
EgyptNematode31.8119.83–43.78259.6297.3<0.001
Cestode27.4923.72–31.2617.1870.9<0.001
Trematode15.8276.56–25.1344.7498.5<0.001
IranCestode18.2111.59–24.8356.0887.5<0.001
Nematode33.9316.52–51.35154.5396.8<0.001
Trematode0.24−0.11–0.590.190<0.001
PalestineNematode24.3911.25–37.540.000-
Cestode36.5921.84–51.320.000-
QatarCestode26.648.89–44.3913.9492.8<0.001
Saudi ArabiaCestode57.6634.63–80.706.7485.6<0.001
Trematode14.6858.88–20.490.000-
TurkeyNematode56.2411.40–101.130.1096.7<0.001
Cestode12.875.17–20.5710.3480.6<0.001
CI: confidence interval; I2: inverse variance index; χ2: Cochran’s Q chi-square.
Table
Table 2. Rodent-borne zoonotic helminths in the Middle East countries.
Table 2. Rodent-borne zoonotic helminths in the Middle East countries.
ParasitesHostSource of Human InfectionReference
Rodent-borne zoonotic cestodes:
Raillieitina celebensis and R. demerariensis.DH: rodent; IH: ant and beetleIngestion of food contaminated with infected insects[5,6]
Hymenolepis diminuta and H. nanaDH: rodent; IH: H. diminuta: flea and beetle. H. nana does not require IH.Consumption contaminated food with rodent feces containing parasitic egg[6,86,87]
Mesocestoides sp.DH: dog and cat; 1st IH: ant and mite, 2nd IH: rodent, bird, amphibian, and reptileConsumption of undercooked meat of amphibians and reptiles containing infective larva (tetrathyridium)[5,6]
Taenia taeniaeformisDH: cat; IH: rodentThere is a report that Taenia taeniaformis can infect humans[88]
Echinococcus multilocularisDH: dog, fox; IH: ratIngestion of embryonated eggs[86]
Rodent-borne zoonotic nematodes:
Angiostrongylus cantonensisDH: rat and mollusk; IH: snail, prawn, crab, and frogIngestion of uncooked IH or vegetables contaminated with infected larvae[6]
Gongylonema pulchrumDH: ruminant, pig, wild boar, non-human primate, carnivore, and rodent; IH: beetles and cockroachesIngestion of IH or drinking of water contaminated with infective larvae[5,6]
Trichinella spp.Pig, wild boar, and rodentIngestion of uncooked muscle with encysted larvae [6]
Trichostrongylus spp.Herbivorous animalConsumption of food and water contaminated with animal feces containing infective larvae[6]
Capillaria hepaticaRat, carnivore, and humansConsumption of food contaminated with feces containing embryonated eggs[5]
Trichuris trichiuraHumansConsumption of food contaminated with feces containing Trichuris egg.[5]
Rodent-borne zoonotic trematodes:
Echinochasmus sp., Echinoparyphium recurvatum, and Echoinostoma sp.DH: humans, rat, duck
1st IH: snail, 2nd IH: snail, amphibian, bivalve, fish		Ingestion of uncooked fish containing metacercariae[2,89]
Fasciola hepaticaDH: herbivore; IH: snailIngestion of metacercariae contaminated vegetable[6,34]
Haplorchis pumilio,
Pygidiopsis genata, Stictodora tridactyla, Prosthodendrium spp., and Plagiorchis muris		DH: dog, cat, rat, duck, humans; 1st IH: snail, 2nd IH: fishEating uncooked fish harboring viable metacercariae[88,90]
Schistosoma mansoniDH: Vertebrate animal; IH: snailPenetrate the DH skin[6,86]
Note: DH: Definite host, IH: Intermediate host.
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Islam, M.M.; Farag, E.; Hassan, M.M.; Bansal, D.; Awaidy, S.A.; Abubakar, A.; Al-Romaihi, H.; Mkhize-Kwitshana, Z. Helminth Parasites among Rodents in the Middle East Countries: A Systematic Review and Meta-Analysis. Animals 2020, 10, 2342. https://doi.org/10.3390/ani10122342

AMA Style

Islam MM, Farag E, Hassan MM, Bansal D, Awaidy SA, Abubakar A, Al-Romaihi H, Mkhize-Kwitshana Z. Helminth Parasites among Rodents in the Middle East Countries: A Systematic Review and Meta-Analysis. Animals. 2020; 10(12):2342. https://doi.org/10.3390/ani10122342

Chicago/Turabian Style

Islam, Md Mazharul, Elmoubashar Farag, Mohammad Mahmudul Hassan, Devendra Bansal, Salah Al Awaidy, Abdinasir Abubakar, Hamad Al-Romaihi, and Zilungile Mkhize-Kwitshana. 2020. "Helminth Parasites among Rodents in the Middle East Countries: A Systematic Review and Meta-Analysis" Animals 10, no. 12: 2342. https://doi.org/10.3390/ani10122342

APA Style

Islam, M. M., Farag, E., Hassan, M. M., Bansal, D., Awaidy, S. A., Abubakar, A., Al-Romaihi, H., & Mkhize-Kwitshana, Z. (2020). Helminth Parasites among Rodents in the Middle East Countries: A Systematic Review and Meta-Analysis. Animals, 10(12), 2342. https://doi.org/10.3390/ani10122342

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