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Article

Gastrointestinal Parasites of Dogs in Egypt: An Update on the Prevalence in Dakahlia Governorate and a Meta-Analysis for the Published Data from the Country

by
Ibrahim Abbas
1,*,
Hanadi B. Baghdadi
2,3,
Mohamed Abdo Rizk
4,*,
El-Sayed El-Alfy
1,
Bassem Elmishmishy
1 and
Mayada Gwida
5
1
Parasitology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
2
Biology Department, College of Science, Imam Abdulrahman Bin Faisal University, Dammam 31113, Saudi Arabia
3
Basic and Applied Scientific Research Center (BASRC), Imam Abdulrahman Bin Faisal University, Dammam 31113, Saudi Arabia
4
Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
5
Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
*
Authors to whom correspondence should be addressed.
Animals 2023, 13(3), 496; https://doi.org/10.3390/ani13030496
Submission received: 18 November 2022 / Revised: 14 January 2023 / Accepted: 16 January 2023 / Published: 31 January 2023
(This article belongs to the Section Veterinary Clinical Studies)
Browse Figures
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Abstract

:

Simple Summary

Dogs are hosts for several gastrointestinal (GIT) parasites that pose potential threats for health of humans and animals. Herein, various GIT parasites in feces of stray dogs in Dakahlia governorate, Egypt, were surveyed. Interestingly, the prevalence greatly declined compared to what had been detected in the latest surveys from Dakahlia published 40 years ago; nonetheless, a few parasites, including Toxocara canis, remain prevalent. Various meta-analyses were also conducted to combine our findings with findings of earlier surveys on dogs from Egypt, and the results highlighted the need for a close collaboration between veterinary and public health authorities in Egypt in a “One Health” approach.

Abstract

Since the last survey on gastrointestinal (GIT) parasites infecting dogs in Dakahlia governorate, Egypt, was published 40 years ago, the present study detected various GIT parasites in feces of 78 stray dogs in this governorate. Twenty-one dogs (35.9%) had eggs/oocysts of eight different parasites including Toxocara canis (19.2%), Toxascaris leonina (2.6%), hookworms (1.3%), Taenia species (5.1%), Dipylidium caninum (2.6%), Cystoisospora canis (5.1%), Cystoisospora ohioensis (2.6%), and Neospora caninum-like oocysts (1.3%). These results were combined in various meta-analyses with findings of all published surveys on GIT parasites of dogs in Egypt to underline the potential parasitic zoonoses from dogs in the country. Feces and/or gastrointestinal tracts of 19,807 dogs from various Egyptian governorates, but particularly Cairo, have been microscopically tested in 182 datasets published between 1938 and 2022, revealed during our systematic database search. Toxocara canis, interestingly, displayed a twofold higher pooled prevalence (24.7%) when compared to the published global pooled prevalence for T. canis, indicating that dogs represent a major risk for toxocariasis in humans from Egypt. Dipylidium caninum (25.4%) as well as various Taenia species (17.1%) also displayed high pooled prevalences. On the contrary, lower pooled prevalence was estimated for the most important zoonotic taeniid “Echinococcus granulosus” (2.4%) as well as for hookworms (1.8%) in comparison to what has been published from other countries in the region. Relatively high prevalences were estimated for three protozoa detected in dogs and are common to infect children in Egypt; Cryptosporidium (5.5%), Giardia (7.4%), and Entamoeba histolytica (9.8%). In general, the pooled prevalence estimated for various parasites detected in dogs from Egypt has decreased in the recent years, sometimes by as much as one-fifth, but this great decline is statistically insignificant, which should alert the veterinary and public health authorities to continue their efforts for controlling these parasites in a “One Health” approach.

Graphical Abstract

1. Introduction

Around 15 million dogs live as strays in Egypt and represent the majority of the dog population in this country (https://learningenglish.voanews.com/a/egypt-s-street-dogs-getting-chance-at-better-life/5297129.html, accessed on 15 October 2022). Those dogs can roam everywhere in rural and urban areas as well, spread various gastrointestinal parasites with potential zoonoses in the environment [1]. Many of these parasites are very serious, e.g., Echinococcus, which circulate in various dog–human and dog–animal cycles. Echinococcosis affects more than a million people worldwide at any one time, and it results in around 19,300 fatalities per year [2]. Although being underreported, echinococcosis has increasing prevalence patterns among Egyptians in the recent years, reviewed in [3]. For example, 45 cases were reported among patients who visited Tanta hospital in Gharbia governorate between 2012 and 2014; many of them had multiple cysts in their liver and/or lungs. Another 46 cases were documented in 2016–2018 in a hospital in Cairo. More recently, 10 CE cases were detected in children who visited a hospital in Cairo [3]. In addition, some surveys on animals are alarming with variable prevalence rates reaching up to 50.0% in camels and 27.0% in sheep, reviewed in [3].
Several surveys have been published describing parasitic infections of dogs in various Egyptian governorates. The majority of these surveys have recruited a limited number of dogs, and findings of these surveys are mostly fragmentary. This highlights the need for a meta-analysis study combining results of these surveys to provide a comprehensive overview on various parasites infecting dogs and their potential zoonoses in Egypt. Moreover, surveys from certain governorates are old and need updating. For example, the last survey on dogs from Dakahlia (the largest governorate in the Nile Delta) was published 40 years ago [4].
The objective of the present study was to provide the first meta-analysis investigation on various gastrointestinal parasites infecting dogs in Egypt, and to update the prevalence of GIT parasites infecting dogs in Dakahlia governorate. Results would be useful in highlighting the most important parasitic zoonoses from dogs in Egypt.

2. Materials and Methods

2.1. Experimental Study

Fresh fecal samples were collected over a period of 6 months from 78 dogs of different ages and sexes that lived as strays in Mansoura city suburbs, Dakahlia governorate, Egypt. Around 10 g of fresh feces were collected from each dog. Samples were grossly examined, then processed using the standard sedimentation test in combination with the modified Wisconsin sucrose flotation test [5]. Samples that had coccidian oocysts were kept in potassium dichromate 2.5% at room temperature for oocyst sporulation. Cryptosporidium oocysts were tested using the modified Ziehl-Neelsen’s staining technique [6]. Morphometrics of the revealed parasitic stages were detected using a binocular microscope (Carl Zeiss, Oberkochen, Germany) equipped with a calibrated ocular micrometer as well as a 3 megapixel camera (Amscope®, Irvine, CA, USA). The identity of the revealed coccidian oocysts was detected according to [7].

2.2. Meta-Analysis

2.2.1. Reports Collection, Testing for Eligibility, and Data Extraction

Various databases (PubMed, Scopus, ScienceDirect, and Google Scholar) were searched by the two authors (IA, MG) for studies listing the GIT parasites of dogs in Egypt. Several keywords were used in various combinations and linked using the Boolean operators “AND” and “OR”. The keywords included gastrointestinal parasites, helminths, Toxocara canis, Toxascaris leonina, hookworms, taeniids, Dipylidium caninum, protozoa, Isospora, Neospora caninum, Cryptosporidium, dogs, and Egypt. Websites of the scientific networks “ResearchGate and Academia” were also included in our search. The website of the Egyptian knowledge bank (http://www.ekb.eg, accessed on 30 September 2022) was searched to collect papers from Egypt published in local journals, which were not available in electronic copies. The collected articles were screened for inclusion by EE and BE and articles with disagreement were discussed with IA and MG. Only papers that had been published as research articles were considered. Articles were also defined as eligible when the study was conducted in Egypt, found positive samples for any of the GIT parasites in dogs, and had a defined number of tested as well as positive samples. Articles that did not meet these criteria were considered ineligible, e.g., articles listing non-GIT parasites in dogs, articles of non-original contributions (e.g., reviews), and articles with inappropriate methodologies. Data were extracted from the eligible studies and organized in Microsoft Excel® (Redmond, WA, USA) spreadsheets (version 2020) by EE and BE and any disagreement was resolved by consensus. The following information was extracted: study region/governorate, dogs’ life style, sample size, number of positives, parasites detected, and the detection method. A few authors of articles with unclear data were contacted.

2.2.2. Data Analysis

The extracted data were used for the meta-analysis conducted using the software Open Meta[Analyst] [8], and all analyses were established based on a 95% confidence interval (95% CI). Because of the high heterogeneity (estimated based on the I2 statistic) among the included datasets, pooled estimates representing the prevalence of various GIT parasites were computed using the random effects model based on the DerSimonian–Laird method. The heterogeneity among studies was considered high when the I2 value exceeded 50%. Various subgroup analyses were conducted to investigate the prevalence variation according to the dogs’ life style (strays or pets) and the regional origin of dogs sampled. The Egyptian governorates were assigned into 4 main regions (Nile Delta, Middle Egypt, Coastal governorates, and Southern governorates). Since the year of samples’ collection has not been provided in most reports from Egypt, datasets were classified into 2 groups according to the publishing year (before and after the year 2010) to detect the prevalence variation over time. Publication bias was not estimated for the collected data because it is not considered relevant for prevalence studies [9]. Data were also statistically tested using the software GraphPad Prism (version 6), and various tests were employed. For example, the one-way ANOVA was used in combination with the Kruskal–Wallis test to test the significance of variation among various regions. The unpaired t test coupled to the Mann–Whitney test were used to test the significance of variation according to the dogs’ life style. Variations were considered significant when the p-value ≤ 0.05.

3. Results

3.1. Experimental Study

Eggs/oocysts of eight different GIT parasites were identified in feces of 78 stray dogs from Dakahlia governorate, giving rise to an overall prevalence of 35.9% (28/78). Toxocara canis was the most frequently detected parasite; T. canis eggs were detected in 15 (19.2%) samples. Other helminths eggs were also observed, including T. leonina (2.6%), hookworms (1.3%), taeniid eggs (5.1%), and D. caninum (2.6%) (Table 1).
Table
Table 1. Prevalence of different parasites in feces of 78 stray dogs from Dakahlia governorate, Egypt.
Table 1. Prevalence of different parasites in feces of 78 stray dogs from Dakahlia governorate, Egypt.
Identified ParasitesNo. Positive%Single InfectionMixed Infection
Toxocara canis1519.2132
Toxoscaris leonina22.62--
Hookworms 11.31--
Taeniid eggs 45.131
Dipylidium caninum22.62--
Cystoisospora canis45.113
Cystoisospora ohioensis22.611
Neospora caninum-like oocysts 11.31--
Two species of the coccidium Cystoisospora were detected. Cystoisospora canis oocysts were found in four (5.1%) samples. Oocysts (n = 30) were ovoid and measured 37.5–44.2 × 32.8–36.3 µm. The oocyst wall was smooth, pale tan, and 1.5 µm thick. No micropyle or oocyst residuum were detected. Sporulated oocysts had two ellipsoidal to ovoid sporocysts with no stieda body (Figure S1A). Oocysts of the second type, Cystoisospora ohioensis [8], were found in two (2.6%) samples. Oocysts (n = 20) were broadly ovoid to subspherical with smooth colorless walls (0.8µm thick) and measured 20–25.6 × 18.5–24.1 µm. No micropyle or polar granules were noticed. The oocyst residual body was absent. Sporocysts were ellipsoidal to ovoid and devoid of the stieda body (Figure S1B).
Neospora caninum-like oocysts were detected in fecal floats of a single dog; a few oocysts (5–10) were noticed in each microscopic field. Oocysts (n = 30) were spherical to subspherical, measured 10.2–11.5 µm and had colorless walls (Figure S1C). Sporulated oocysts had two sporocysts each with four sporozoites. No polar granules, stieda, or oocyst residual bodies were detected (Figure S1D). In addition, no Cryptosporidium oocysts were detected in any stained fecal smear. Although not common, mixed infections were observed in three samples in the form of dual T. canis-D. caninum, T. canis-C. canis, or Taeniid-C. canis infection.

3.2. Meta-Analysis

Thirty-six studies in all (including eight in journals not available as electronic copies) were defined as eligible for inclusion in the meta-analysis (Table 2; Figure 1) and included 182 datasets describing prevalence of seven helminths (139 datasets) and five protozoa (43 datasets) inhabiting the GIT of dogs in Egypt. In total, 19,807 dogs were sampled in surveys mostly from Cairo (the Capital, 14,706 dogs), but also some other governorates including Dakahlia (1117 dogs). The number of samples collected from housed dogs (9679) was not far from that of stray dogs (10,076). The included studies tested the sampled dogs employing either fecal examination to detect eggs/oocysts (10,487 dogs) or examination of the intestine of the necropsied dogs (8635 dog) to retrieve the adult worms. PCR has not been used in any of the included studies to diagnose the GIT parasite found in the tested samples. Values of the overall and regional pooled prevalences for the included parasites are summarized through Table 3, Table 4, Table 5, Table 6, Table 7, Table 8, Table 9 and Table 10.
Table
Table 2. Characteristics of studies included in various meta-analyses conducted in the present study. Abbreviation: FE, fecal examination; NS, not stated.
Table 2. Characteristics of studies included in various meta-analyses conducted in the present study. Abbreviation: FE, fecal examination; NS, not stated.
GovernoratePublication YearSource of Samples Mode of LifeIdentification Stage, MethodNo. TestedIdentified Parasites (Prevalence)Reference
Cairo1938StrayAdult, Necropsy150E. granulosus (10%), Heterophyes heterophyes (59%)[10]
Alexandria 100E. granulosus (2%), H. heterophyes (75%)
Upper Egypt 70E. granulosus (3%)
Cairo1974StrayAdult, Necropsy570E. granulosus (3.9%)[11]
Alexandria1979StrayEggs, FE459T. canis (23.7%)[12]
Pet 128T. canis (13.3%)
Dakahlia1980StrayAdult, Necropsy58T. canis (84.7%), Taenia hydatigena (28.2%), D. caninum (62.4%), E. granulosus (1.2%), E. perfoliatus (4.7%), H. heterophyes (12.9%), Haplorchis yokogawai (10.6%), P. vivax (9.4%)[4]
Dakahlia1982StrayOocysts, FE125Isospora canis (97.6%), Isospora ohioensis (39.2%)[13]
Dakahlia1982StrayAdult, Necropsy289E. granulosus (1.4%)[14]
Cairo1988StrayOocysts, FE110Eimeria canis (1.8%), I. canis (6.4%), I.
ohioensis (2.7%), Hammondia heydorni (2.7%),
Sarcocystis spp. (4.5%)		[15]
Ismailia1991StrayAdult, Necropsy20T. canis (10%), T. leonina (30%), D. caninum (60%) [16]
Cairo1991StrayAdult, Necropsy5000Taenia pisiformis[17]
Menoufiya1993StrayAdult, Necropsy165T. canis (72.7%)[18]
Ismailia1995StrayEggs/oocysts, FE685T. canis (25.5%), T. leonina (32.1%), hookworm (1.3%), Taenia spp. (10.2%), D. caninum (17.5%), Spirometra spp. (0.2%), H. heterophyes (8.5%), I. canis (4.6%), I. ohioensis (13%), Isospora spp. (17.6%), Sarcocystis spp. (2.3%), Cryptosporidium spp. (3.8%), Giardia spp. (8.3%)[19]
Beni Suef1998StrayAdult, Necropsy87T. canis (18.4%), T. leonina (57.5%), T. pisiformis (19.5%), T. hydatigena (17.2%), D. caninum (43.7%), E. perfoliatus (3.45%), Spirocerca lupi (12.6%), Mesostephanus appendiculatus (3.45%), Mesostephanus melvi (4.6%), Mesostephanus fajardensis (4.6%), P. vivax (4.6%) [20]
Aswan1999Stray dogs Oocysts, FE27Cryptosporidium spp. (11.1%)[21]
Sharkia2002StrayAdult, Necropsy29T. canis (51.7%), S. lupi (3.4%), Rictularia affinis (6.9%), T. pisiformis (24.1%), D. caninum (86.2%), Spirometra erinacei (3.4%), Diplopylidium nolleri (3.4%), H. heterophyes (10.3%), P. vivax (6.9%)[22]
Assiut2003StrayAdult, Necropsy70T. pisiformis (18.5%), T. hydatigena (15.7%), Taenia ovis (4.2%), Taenia taeniaeformis (1.4%), E. granulosus (1.4%), D. caninum (45.7%), [23]
Dakahlia2007StrayAdult, Necropsy540E. garnulosus (5%)[24]
Cairo2007StrayAdult, Necropsy50T. canis, D. caninum, E. granulosus (16%)[25]
Cairo2007StrayAdult, Necropsy166T. canis (39.2%), T. leonina (30%), hookworms (25.9%), Taenia spp. (36.1%), D. caninum (32.5%), E. granulosus (1.2%), Cystoisospora spp. (15.7%), E. histolytica (34.9%), Sarcocystis spp. (1.8%)[26]
HousedEggs/oocysts, FE60T. canis (16.7%), T. leonina (30%), hookworms (6.7%) Taenia spp. (13.3%), D. caninum (5%), Cystoisospora spp. (10%), E. histolytica (21.7%), Sarcocystis spp. (1.7%)
Cairo2008HousedEggs, FE500T. canis (6%), D. caninum (40%), E. granulosus (1.8%)[27]
Beni Suef2008Stray dogsEggs, FE200 T. canis (10%), A. caninum (5%), Taenia spp. (3%), D. caninum (3%), H. heterophyes (1.5%)[28]
NS2009PetEggs/oocysts, FE3000T. canis (9.8%), E. granulosus, D. caninum, H. heterophyes [29]
Giza2009Stray dogsEgg/oocysts, FE27T. canis (37%), T. leonina (33.3%), A. caninum (18.5%), Taenia spp. (33.3%), D. caninum (37%), Isospora spp. (14.8%), Sarcocystis spp. (14.8%), Cryptosporidium spp. (18.5%), Giardia spp. (14.8%)[30]
Kalubiya2010Stray dogs with diarrheaOocysts, FE20Cryptosporidium spp. (50%), including 2 that were molecularly identified as C. parvum [31]
Giza2010StrayAdult, Necropsy25@T. canis (56%), T. leonina (8%), Ascaris lumbricoides (8%)[32]
NS2011Stray# Eggs, FE53T. canis (35.8%)[33]
Housed 45T. canis (21.3%)
Alexandria2012StrayEggs/oocysts, FE33T. canis (15.1%), A. caninum (21.2%), Echinococcus spp. (24.2%), E. perfoliates (9.1%), D. caninum (60.6%), H. heterophyes (27.2%), Ascocotyle spp. (3.03%)[34]
Alexandria2014HousedEggs/oocysts, FE120T. canis (0.8%), A. caninum (1.7%), T. vulpis (0.8%), Cystoisospora canis (4.2%), Giardia spp. (1.7%)[35]
Police 60T. canis (5%), T. leonina (1.7%), C. canis (3.3%), Giardia spp. (31.7%), Entamoeba histolytica (18.3%), Cryptosporidium spp. (1.7%)
Cairo2014StrayEggs/oocysts, FE180T. canis (46.1%), T. leonina (3.9%), T. vulpis (34.4%), Capillaria spp. (12.2%), Taenia spp. (10%), D. caninum (22.8%), Isospora spp. (37.8%)[36]
Ismailia2015StrayAdult, Necropsy50T. canis (20%), T. leonina (10%), S. lupi (10%), R. affinis (8%), T. hydatigena (10%), D. caninum (100%), P. vivax (4%), M. appendiculatus (16%), M. melvi (6%), Mesostephanus spp. (2%), E. liliputans (16%), H. dispar (14%), P. genata (20%), Pygidiopsis summa (6%), Ascocotyle rara (4%), Phagicola longus (6%), Phagicola longicollis (4%), Metagonimus yokogawai (4%), Haplorchis pumilio (6%), Apophallus donicus (4%) [37]
Kalubiya2015Military (30), housed (60), stray (30)Eggs/oocysts, FE130T. canis (5.4%), T. leonina (3.1%), Ancylostoma spp. (6.2%), Taenia spp. (2.3%), D. caninum (1.5%), Heterophyes spp. (3.9%), Paragonimus spp. (0.8%), Cryptosporidium spp. (5.4%), Blastocystis spp. (3.1%), Entamoeba canis (0.8%), Cyclosppora caytanensis (0.8%)[38]
Cairo2015HousedEggs, FE3864T. canis (3%)[39]
Cairo, Giza2016HousedEggs/oocysts, FE395T. canis (0.3%), T. leonina (5.8%), T. vulpis (3.3%), Cryptosporidium spp. (10.1%), Giardia spp. (0.5%), Entamoeba histolytica/Entamoeba dispar (5.6%)[40]
Sohag, Luxor2018HousedEggs, FE120T. canis (23.3%), T. leonina (4.2%), A. caninum (3.3%), D. caninum (1.7%)[41]
Sharkia2018HousedOocysts, FE50Cryptosporidium spp. (34%)[42]
Nested-PCR Cryptosporidium spp. (24%)
Alexandrina, Ismailia, Menoufiya, Sohag2019PetEggs, FE296T. canis (53.1%)[43]
Various2021PetEggs/oocysts, FE986Giardia spp. (8.5%)[44]
Dakahlia StrayEggs/oocysts, FE78T. canis (19.2%), T. leonina (2.6%), hookworms (1.3%), Taenia spp. (5.1%), D. caninum (2.6%), C. canis (5.1%), C. ohioensis (2.6%), N. caninum-like oocyst (1.3%) Present study
# Toxocara canis eggs have also been noticed in hair samples from 26.6% of 64 stray and 10.7% of 54 domestic dogs.

4. Discussion

In the present study, feces of 78 stray dogs from Dakahlia governorate, Egypt, were screened for various GIT parasites, and some parasites that are widely known as potential agents of zoonosis (e.g., T. canis, hookworms, and D. caninum) were detected in variable infection rates. It is worthy to mention that the prevalence of these parasites greatly declined from what was reported 40 years ago from stray dogs in Dakahlia [4]. Our findings from dogs in Dakahlia were combined with findings of the earlier surveys on dogs from Egypt in various meta-analyses to illustrate the role of dogs in the epidemiology of dog–man transmitted parasites throughout Egypt. The following sections cover the most common parasitic zoonoses from dogs in Egypt based on findings of various meta-analyses conducted in the present study.

4.1. Common Nematodes in Dogs from Egypt

Toxocara canis is one of the major zoonotic helminths worldwide. Eggs of this nematode were detected in feces of 19.2% of the 78 screened dogs from Dakahlia. In total, 11,477 dogs from various Egyptian governorates were sampled and 1406 were found infected, giving rise to a pooled prevalence (24.7%, 95% CI: 21.1–28.3%) that is more than double the estimated T. canis global prevalence (11.1%) [45], suggesting a higher risk for human health in Egypt (Table 3; Figure 2). The pooled prevalence did not significantly vary over time (p-value = 0.7390); however, the estimated pooled prevalence for the published datasets after the year 2010 was lower (21.4%, 17.5–25.4%) than that for datasets published before 2010 (27.0%, 19.8–34.3%). In general, dogs in Africa and the Middle East, where Egypt is located, have higher T. canis prevalence than any other region worldwide due to socio-economic, environmental, and climatic factors [45]. While dogs from the Nile Delta had the highest T. canis prevalence (42.6%, 8.2–77.1%) in Egypt when compared to the other three regions (Table 3), prevalence variations between regions were insignificant (p-value = 0.231), assuming that dogs have similar susceptibility to T. canis infection throughout Egypt. This was also true for prevalence variation between stray and housed dogs: no significant difference (p-value = 0.141) was found; however, stray dogs (30.3%) had a higher prevalence than housed dogs (16.4%) (Table 3). In Egypt, many dogs spend a time in their life as strays before being housed. A recent report by Abdel Aziz et al. [43] underlines this assumption. The authors examined 296 pet dogs admitted to veterinary hospitals in four different Egyptian governorates and found a very high T. canis prevalence (53.1%). This report is alarming since keeping a dog has become a popular trend among youth particularly in urban cities in Egypt. On the other hand, the high prevalence in stray dogs reflects a significant level of environmental contamination with T. canis eggs, which have been detected in high prevalences in soil samples from various Egyptian governorates [46]. Humans can be accidentally infected through ingesting T. canis eggs, and infected humans often develop ocular toxocariasis or visceral larval migrans with subsequent allergic and neurological disorders [47]. Although a high prevalence of T. canis antibodies has been observed in several surveys from humans in Egypt, toxocariasis is underestimated [48]. Nevertheless, T. canis represents a significant zoonosis in this country taking into consideration the high prevalence of T. canis in dogs from Egypt.
Table
Table 3. Overall and regional pooled prevalence of Toxocara canis in dogs from various Egyptian regions, and variabilities according to dog life style and detection method.
Table 3. Overall and regional pooled prevalence of Toxocara canis in dogs from various Egyptian regions, and variabilities according to dog life style and detection method.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence2911,477140624.7 (21.1–28.3)98.67
Prevalence variation over time
Before 201013615197627.0 (19.8–34.3)98.53
After 201014532643021.4 (17.5–25.4)98.00
Regional prevalence
Nile Delta692524842.6 (8.2–77.1)99.33
Dakahlia370310635.4 (−12.9–83.7)99.48
Menoufiya219312749.9 (2.7–96.2)96.53
Sharkia1291551.7 (33.5–69.9)NA
Middle Egypt10622832213.6 (9.9–17.2)98.32
Cairo7816560514.3 (10.2–18.4)98.84
Giza1271037.0 (18.8–55.3)NA
Kalubiya213076.4 (−3.1–16.0)61.20
Coastal governorates9176242723.1 (12.4–33.7)97.34
Alexandria596221821.0 (5.5–36.5)98.10
Ismailia480020925.6 (14.2–36.9)81.39
Southern governorates410946830.9 (8.1–53.7)97.62
Beni-Suef22873311.4 (7.0–15.9)21.78
Luxor11203025.0 (17.3–32.7)NA
Sohag1614675.4 (64.6–86.2)NA
Dog life style
Stray16283473730.3 (19.3–41.2)98.44
Housed13864366916.4 (12.8–19.9)98.30
Detection method
Necropsy9163934633.3 (18.3–48.3)99.02
Fecal examination209835106020.7 (17.1–24.2)98.37
NA, not applicable.
The other Ascarid “T. leonina” common to infect dogs and cats worldwide has been examined in 21 datasets from dogs in Egypt (Table 4). When compared to T. canis, the parasite displayed a much lower pooled prevalence (2.8%, 2.0–3.6%) in 7429 tested dogs in Egypt, and the prevalence did not significantly (p-value = 0.5772) vary over time (Table 4; Figure S2). This very low prevalence is consistent with that has been estimated for 119,317 dogs worldwide (2.9%) [49], and can be attributed to the limited routes for T. leonina transmission among dogs in comparison to T. canis [49]. Toxascaris leonina prevalence did not significantly differ according to the Egyptian region studied (p-value = 0.313) or the life style of dogs (p-value = 0.645). Although not common, there have been a few cases of T. leonina infections in humans worldwide [50].
Table
Table 4. Overall and regional pooled prevalence of Toxascaris leonina in dogs from various Egyptian regions, and variabilities according to dog life style and detection method.
Table 4. Overall and regional pooled prevalence of Toxascaris leonina in dogs from various Egyptian regions, and variabilities according to dog life style and detection method.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence2174293322.8 (2.0–3.6)96.13
Prevalence variation over time
Before 20101123992855.2 (3.5–7.0)97.83
After 2010105030472.5 (1.0–4.0)82.00
Regional Prevalence
Nile Delta473220.1 (0.1–0.4)0.00
Dakahlia370320.2 (−0.3–0.7)10.15
Sharkia12901.7 (−2.9–6.2)NA
Middle governorates95322430.8 (0.2–1.4)84.19
Cairo65165300.6 (0.0–1.1)84.77
Kalubiya213043.9 (−4.3–12.1)61.74
Giza127933.3 (15.6–51.1)NA
Coastal governorates596823214.0 (0.9–28.9)98.65
Alexandria221310.6 (0.4–1.7)0.00
Ismailia375523123.6 (6.7–40.6)91.34
Southern governorates34075519.0 (3.3–34.7)98.33
Beni-Suef22875028.6 (−27.5–84.7)99.14
Luxor112054.2 (0.6–7.7)NA
Dog life style
Stray1321802997.8 (5.2–10.4)97.46
Housed85249330.7 (0.1–1.2)80.32
Detection method
Necropsy1461182712.2 (0.6–3.8)95.45
Fecal examination71311614.3 (2.6–6.1)96.61
NA, not applicable.
In the present study, a single dog out of 78 tested from Dakahlia had hookworm eggs in his feces. In total, 20 datasets from Egypt that tested 6923 dogs for hookworms were revealed during our search; 139 dogs were found infected, resulting in a pooled prevalence of 1.8% (1.0–2.6%) (Table 5; Figure S3). This prevalence is much lower when compared to that detected for dogs in some African countries [51]. A very high pooled prevalence (41.0%) has also been estimated for dogs in Asia [52]. Although being much declined, the pooled prevalence did not significantly (p-value = 0.8497) vary when datasets published after the year 2010 (0.9%) on dogs from Egypt were compared to those published earlier (3.9%). In Egypt, comparable prevalences were detected for dogs from various regions with no significant differences (Table 5). Likewise, the life style of dogs had no significant effect (p-value = 0.967) on the prevalence (Table 5). Various hookworm species can infect dogs worldwide, e.g., Ancylostoma caninum, Ancylostoma braziliense, Ancylostoma ceylanicum, and Uncinaria stenocephala. These species can cause anemia and hypoproteinemia with varying degrees in dogs [53]. Based on morphometrics of eggs recovered from the tested fecal samples, A. caninum has been identified in the majority of surveys on dogs from Egypt. All canine hookworms are zoonotic [53], and hookworm infections were detected in patients from Egypt early in the 1990s [54]. Additionally, hookworms have been identified as being responsible for acute and recurrent abdominal pain in 11 of 95 patients from Egypt [55] Hookworm eggs and/or larvae have also been detected in soil samples as well as wastewater in Egypt [56].
Table
Table 5. Overall and regional pooled prevalence of hookworms in dogs from various Egyptian regions, and variabilities according to dog life style.
Table 5. Overall and regional pooled prevalence of hookworms in dogs from various Egyptian regions, and variabilities according to dog life style.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence2069231391.8 (1.0–2.6)82.84
Prevalence variation over time
Before 2010101893823.9 (1.8–5.9)86.63
After 2010105030570.9 (0.2–1.6)70.91
Regional prevalence
Nile Delta4732121.5 (0.6–2.4)0.0
Dakahlia3703111.5 (0.6–2.4)3.40
Sharkia12901.7 (−2.9–6.2)NA
Middle governorates84822952.2 (0.9–3.5)91.63
Cairo54665821.6 (0.3–3.0)94.34
Giza127518.5 (3.9–33.2)NA
Kalubiya213086.8 (−1.6–15.2)51.37
Coastal governorates5968181.5 (0.0–2.9)50.29
Alexandria221399.9 (−9.6–29.5)87.31
Ismailia375591.3 (0.5–2.1)0.0
Southern governorates3401142.7 (0.1–5.6)71.67
Beni-Suef2281102.6 (−1.7–6.9)83.84
Luxor112043.3 (0.1–6.5)NA
Dog life style
Stray142204902.9 (1.4–4.4)75.97
Housed64719491.0 (0.2–1.8)91.92
NA, not applicable.

4.2. Common Cestodes in Dogs from Egypt

Various cestodes can circulate in dog–human/animal cycles. Dogs are definitive hosts for several taeniids, and infections can be diagnosed through detection of the gravid segments and/or eggs in dog feces; however, eggs are not discriminative to the species level [57]. In Egypt, 12,021 dogs were tested for Taenia species in 19 datasets, and 3926 were found positive, yielding a pooled prevalence of 17.1% (7.2–27.7%) (Table 6; Figure S4). Datasets published before 2010 displayed a five times higher pooled prevalence (26.4%) than those published after 2010 (5.2%), with a significant variation (p-value = 0.0085). The prevalence was approximately four times higher (27.0%) in 6501 dogs tested via intestinal necropsy than in 5520 dogs tested via fecal examination (7.2%), with the difference being statistically insignificant (p-value = 0.139). Similarly, insignificant variations were detected in Taenia prevalence according to the life style of tested dogs (p-value = 0.348) or the Egyptian region studied (p-value = 0.565) (Table 6). It is worthy to mention that T. hydatigena cysticerci have been frequently observed in small ruminants from Egypt [58]. While no Taenia multiceps has been detected in dogs from Egypt [59], T. multiceps coenurosis has been reported in an Egyptian woman (40 years old) from Tanta city [60], and the disease is quite common in sheep from Egypt [61].
Table
Table 6. Overall and regional pooled prevalence of Taenia spp. detected in dogs from various Egyptian regions, and variabilities according to dog life style.
Table 6. Overall and regional pooled prevalence of Taenia spp. detected in dogs from various Egyptian regions, and variabilities according to dog life style.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence1912,021392617.5 (7.2–27.7)99.82
Prevalence variation over time
Before 2010117390381826.4 (5.2–47.4)99.87
After 2010846311085.3 (2.1–8.6)87.98
Regional prevalence
Nile Delta47324012.8 (2.5–23.1)92.83
Dakahlia37033310.2 (0.5–20.9)94.04
Sharkia129724.1 (8.6–39.7)NA
Middle Egypt89868370820.5 (6.6–47.7)99.93
Cairo59711369625.2 (12.5–63.0)99.96
Giza127933.3 (15.6–51.1)NA
Kalubiya213032.2 (−0.3–4.7)0.0
Coastal governorates3768577.0 (0.5–13.6)85.56
Alexandria13301.5 (−2.6–5.5)NA
Ismailia27357510.2 (8.0–12.4)0.96
Southern governorates33576626.2 (1.8–54.2)97.35
Assiut1702840.0 (28.5–51.5)NA
Beni-Suef22873819.5 (−13.6–52.6)97.53
Various *1 2963712.5 (8.7–16.3)NA
Life style
Stray157701383820.4 (3.4–37.4)99.81
Housed44320886.3 (1.0–11.6)93.06
Detection method
Necropsy96501372027.0 (0.4–54.5)99.89
Fecal examination1055201967.2 (3.7–10.6)93.32
* Alexandria, Ismailia, Menoufia, and Sohag; NA, not applicable.
In the present study, 4 out of 78 dogs tested in Dakahlia had taeniid eggs. In addition to the genus Taenia, the family Taeniidae also includes the genus Echinococcus (canine dwarf tapeworms), and both of these genera have quite similar eggs that cannot be distinguished morphologically [57]. As a result, the possibility of Echinococcus infection in the sampled dogs from Dakahlia cannot be ruled out. Sixteen datasets from Egypt have examined the necropsied intestine of 2809 dogs, mostly strays (n = 2309), for Echinococcus, and E. granulosus was found in 96 dogs, giving rise to a pooled prevalence of 2.4% (1.4–3.5%) (Table 7; Figure 3). Only two datasets have been published after the year 2010, and recruited a small number of dogs (n = 83), giving rise to a high pooled prevalence (11.5%), which is five times higher than that estimated for 2726 dogs tested in 14 datasets published before 2010 (2.3%); nonetheless, the prevalence variation is statistically insignificant (p-value = 0.8162). At the regional level, higher infection rates have been detected in dogs from North Africa, e.g., Tunisia (18.4%), Libya (27.8%), Morocco (35.3%), and Sudan (51.0%) [62,63,64,65]. Cystic echinococcosis (CE) caused by E. granulosus is a common zoonoses from dogs worldwide. In Egypt, many CE-infected cases have been reported in the recent few years [66]. In animals, CE occurrence has increased over time and the recent surveys are alarming from Egypt [67]. Echinococcus granulosus senso lato is a complex of 5 species/11 genotypes involving E. granulosus sensu stricto (G1-2 genotypes), primarily circulates in a sheep–dog cycle, and contributes approximately to 88% of the global cases of human CE [68]. However, most of human cases in Egypt have been attributed to the G6 (Echinococcus canadensis) underlining the dog–camel transmission cycle [69]. Unfortunately, no studies have been conducted to verify Echinococcus genotypes in dogs from Egypt, which would aid in understanding the epidemiology of CE in the country.
A recent report that identified D. caninum eggs in stools of 4 out of 996 Egyptian children highlights this parasitic zoonoses from dogs in Egypt [70]. In the present study, D. caninum had a high estimated pooled prevalence (25.4%, 20.4–30.4%) in 7675 dogs that had been tested in 22 datasets (Table 8; Figure 4), which could be attributed to the wide dispersal of Ctenocephalides canis, the vector for D. caninum, among populations of stray dogs in Egypt [71]. Although the estimated pooled prevalence for datasets published after 2010 (20.8%) was two-thirds of that for datasets published before 2010 (30.0%), the variation was insignificant (p-value = 0.1588). Stray dogs (38.4%) had a significantly (p-value = 0.004) higher prevalence than housed dogs (3.3%). Globally, the prevalence is highly variable and correlated with the life style of dogs, level of flea infestation in dogs, environmental sanitation, and geographical areas [72]. There have been a few cases of human dipylidiasis that have been documented worldwide [72].
Table
Table 7. Overall and regional prevalence of Echinococcus granulosus detected in dogs from various Egyptian regions, and variabilities according to dog life style.
Table 7. Overall and regional prevalence of Echinococcus granulosus detected in dogs from various Egyptian regions, and variabilities according to dog life style.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence162809962.4 (1.4–3.5)67.98
Prevalence variation over time
Before 2010142726882.3 (1.3–3.4)65.24
After 2010283811.5 (−11.2–34.1)98.36
Regional prevalence
Nile Delta4943282.2 (0.5–3.9)61.72
Dakahlia3914282.3 (0.3–4.3)74.28
Sharkia12901.7 (−2.9–6.2)NA
Middle governorates5 (Cairo)1436564.0 (1.6–6.3)82.39
Coastal governorates4207103.1 (−0.9–7.2)68.22
Alexandria21331011.9 (−9.8–33.6)88.35
Ismailia27001.2 (−1.3–3.7)0.0
Southern governorates322720.8 (−0.3–2.0)0.0
Assiut17000.7 (−1.2–2.6)NA
Beni-Suef18700.6 (−1.0–2.1)NA
NS17022.9 (−1.0–6.8)NA
Life style
Stray152309872.5 (1.3–3.8)69.98
Housed150091.8 (0.6–3.0)NA
NA, not applicable.
Table
Table 8. Overall and regional prevalence of Dipylidium caninum in dogs from various Egyptian regions, and variabilities according to dog life style.
Table 8. Overall and regional prevalence of Dipylidium caninum in dogs from various Egyptian regions, and variabilities according to dog life style.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence22767565125.4 (20.4–30.4)99.64
Prevalence variation over time
Before 201012246937930.0 (22.7–37.3)98.23
After 201010520627220.8 (13.2–28.4)99.93
Regional prevalence
Nile Delta47328636.7 (15.8–57.6)99.03
Dakahlia37036120.4 (3.9–36.9)98.52
Sharkia1292586.2 (73.7–98.8)NA
Middle governorates953222106.2 (4.0–8.3)96.01
Cairo651651987.0 (4.4–9.5)97.27
Giza1271037.0 (18.8–55.3)NA
Kalubiya213021.9 (−3.2–7.1)44.27
Coastal governorates598620247.3 (2.0–92.6)99.92
Alexandria22132029.8 (−29.3–89)98.01
Ismailia375518258.8 (−5.9–1.00)99.88
Southern governorates33577630.5 (2.5–63.5)98.01
Beni-Suef22874432.0 (−16.8–62.9)98.20
Assiut1703245.7 (34.0–57.4)NA
Various *1 2967726.0 (21.0–31.0)NA
Dog life style
Stray15228047138.4 (19.9–57.0)99.72
Housed752951803.3 (1.6–5.0)96.24
* Alexandria, Ismailia, Menoufiya, Sohag; NA, not applicable.

4.3. Common Trematodes in Dogs from Egypt

Due to their fish-eating habits, dogs are susceptible to infection with trematodes of the family Heterophyidae, of which 29 species can infect humans [73]. In the present study, no eggs of any trematode parasite were observed in the tested fecal samples from 78 dogs in Dakahlia. However, various heterophyids have been detected in some earlier surveys on dogs from Egypt. In 12 datasets, 1780 dogs from Egypt were screened for the heterophyids, and 322 were found infected with H. heterophyes, resulting in an estimated high pooled prevalence (18.7%, 11.7–25.7%) (Table 9; Figure S5). This high prevalence is consistent with the frequent occurrence and heavy intensity of heterophyid metacercariae in tissues of grey mullet and Nile Tilapia widely consumed in Egypt [74], which represents a potential health threat for Egyptians. The estimated pooled prevalence for datasets published before 2010 (24.4%) was five times higher than that estimated for datasets published after 2010 (4.6%); however, this variation was insignificant (p-value = 0.3010). Heterophyes heterophyes infections have been also documented in humans from Egypt [75].
Table
Table 9. Overall and regional prevalence of Heterophyes heterophyes detected in dogs from various Egyptian regions, and variabilities according to dog life style.
Table 9. Overall and regional prevalence of Heterophyes heterophyes detected in dogs from various Egyptian regions, and variabilities according to dog life style.
ParameterNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Overall prevalence12178032218.7 (11.7–25.7)98.16
Prevalence variation over time
Before 20108153930824.4 (14.0–34.9)98.75
After 20104241144.6 (−0.5–9.8)78.45
Regional prevalence
Nile Delta3192147.3 (−11.7–16.7)84.92
Dakahlia2163116.3 (−5.7–18.3)90.73
Sharkia129310.3 (−0.7–21.4)NA
Middle Egypt440016424.3 (1.1–47.5)98.42
Cairo237015845.1 (18.8–71.4)96.39
Kalubiya213053.8 (0.5–7.1)0.0
Coastal governorates381814236.9 (−10.2–84.0)99.12
Alexandria21338451.6 (4.8–98.3)96.54
Ismailia1685588.5 (6.4–10.6)NA
Southern governorates227031.2 (0.1–2.4)0.0
Beni-Suef120031.5 (−0.2–3.2)NA
NS17000.7 (−1.2–2.6)NA
Life style
Stray11168031820.2 (12.6–27.8)98.32
Housed110044.0 (0.2–7.8)NA
NA, not applicable.

4.4. Common Protozoa in Dogs from Egypt

Coccidiosis is common among dogs worldwide. Before the discovery of N. caninum in 1998, there was uncertainty about the identity of various coccidian protozoans infecting dogs [76]. Three types of coccidian oocysts can be identified in feces of infected dogs: large-sized oocysts (∼40 μm long) belong to C. canis, medium-sized oocysts (∼25 μm long) belong to C. ohioensis, and small-sized oocysts (∼10–12 μm long) belong either to N. caninum or Hammondia heydroni [77]. Sarcocystis spp. commonly excreted as sporocysts can also be found in dog feces [7]. A few reports on dog coccidiosis in Egypt are available and some reports were published before the year 1998. Therefore, some oocysts have been given invalid names. For example, Abdul-Magied et al. [13] identified small-sized oocysts in 3 out of 125 dogs from Dakahlia as Isospora bigemina. El Ghaysh [15], on the other hand, identified small-sized oocysts in feces of 3 out of 110 dogs from Cairo as H. heydroni oocysts. The same species name was given for oocysts collected from feces of three dogs after being fed on camel and buffalo meats; however, dogs started shedding oocysts at different times [78]. Therefore, it is possible that some small-sized oocysts that were detected in earlier reports from Egypt belong to N. caninum. Oocysts of N. caninum have been detected in a few dogs worldwide [7]. In the present study, N. caninum-like oocysts were detected in feces of 1 out of 78 dogs tested in Dakahlia. Neospora caninum is a significant cause of abortion in cattle [7]. A recent survey detected N. caninum antibodies in 35.0% out of 116 tested sera from aborted cows in Egypt [79]. In addition, N. caninum-like oocysts were detected in feces of five out of nine puppies experimentally fed on placentas and brains of aborted foeti from nine aborted cows in Egypt [80].
Unlike N. caninum, Cystoisopspora spp. (formerly known as Isospora) has no clinical relevance, but a few dogs showed weakness, loss of appetite, diarrhea, and dehydration [77]. However, Cystoisospora spp. was the most frequently detected protozoa in dogs from Egypt, and it was found in 6 out of 78 dogs tested in Dakahlia. The estimated pooled prevalence (Table 10) for Cystoisospora spp. in dogs from Egypt was high (21.2%, −14.2–56.7%) when compared to the reported infection rates from other regions worldwide [77]. In addition, two species have been identified in dogs from Egypt; C. canis (23.3%, 15.6–62.2%) had a higher prevalence than C. ohioensis (12.2%, 3.7–20.8%) (Table 10). Dogs are definitive hosts for several Sarcocystis spp. that can utilize various herbivores as intermediate hosts, causing significant economic losses. Some of these species are common among ruminants in Egypt [81], which suggests the high prevalence of Sarcocystis oocysts in feces of dogs in Egypt. However, a few datasets (n = 6) from the country have been published in which fecal samples from 1126 dogs were examined and Sarcocystis oocysts were detected in 29 with a very low pooled prevalence (2.0%, 0.8–3.2%) (Table 10). Since Sarocystis hominis and Sarcocystis suihominis can infect humans and both species utilize nonhuman primates as definitive hosts [82], dogs have no role yet in the zoonotic sarcocystosis.
Table
Table 10. Pooled prevalences estimated for protozoa detected in feces and/or intestinal scrapings of dogs from Egypt.
Table 10. Pooled prevalences estimated for protozoa detected in feces and/or intestinal scrapings of dogs from Egypt.
ParasiteNo. Data SetsNo. TestedNo. PositivePooled Estimate % Based on 95% CIHeterogeneity
I2%
Cystoisospora spp.10547537021.2 (−14.2–56.7)99.97
C. canis4117816323.3 (15.6–62.2)99.9
C. ohioensis399811912.2 (3.7–20.8)95.88
Sarcocystis spp.61126292.0 (0.8–3.2)36.84
Cryptosporidium1217541115.5 (3.0–8.1)89.25
Giardia726992107.4 (3.6–11.1)94.33
Entamoeba79611079.8 (4.1–15.5)93.90
On the contrary, dogs have a potential role in human cryptosporidiosis, since Cryptosporidium parvum has been confirmed in dogs [83]. Oocysts of C. parvum were molecularly detected in feces of 2 out of 20 diarrheic puppies in Egypt [31], where cryptosporidiosis is common among humans [84]. In total, 12 datasets from Egypt tested 1754 dogs for Cryptosporidium; 111 were found infected, yielding a pooled prevalence of 5.5% (3.0–8.1%) (Table 10), which is slightly lower than that estimated for dogs worldwide (8.0%) [85]. Other protozoa that have potential health risks for humans were also detected in dogs from Egypt and showed estimated high pooled prevalences, e.g., Giardia spp. (7.4%, 3.6–11.1%) and Entamoeba histolytica (9.8%, 4.1–15.5%) (Table 10). Both parasites are prevalent among Egyptian children [86].

5. Conclusions

The present study provides an overview for various GIT parasites infecting dogs in Egypt based on various analyses for the published data addressing this topic. It is important to note that compared to reports from strays dogs in Dakahlia 40 years ago, the prevalence of these parasites has significantly decreased. However, the uneven geographical distribution and high heterogeneity of the published datasets represent possible limitations for this study. In addition, lack of sensitive diagnostic techniques (e.g., PCR) used to identify the parasite found to the species level is another limitation, for example, T. multiceps. While cerebral coenurosis is frequently detected in sheep from Egypt, eggs/adult worms of T. multiceps have not been identified in any survey on dogs from Egypt, leaving a gap in the epidemiology of this economically important parasite in this country. Despite these limitations, the present study was able to underline the role of dogs from Egypt in the epidemiology of various parasites with public health and veterinary importance.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/ani13030496/s1. Figure S1: Photomicrographs for oocysts (arrow/s) of coccidian parasites detected in feces of stray dogs in Dakahlia governorate, Egypt. A. Cystoisospora canis. B. Cysatoisospora ohioensis. C. Neospora caninum-like unsporulated oocysts. D. Neospora caninum-like sporulated oocyst. Scale bar in all parts = 20 μm; Figure S2: Forest plot diagram for random effects in the meta-analysis of the prevalence of T. leonina in dogs from Egypt. The length of line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence; Figure S3: Forest plot diagram for random effects in the meta-analysis of the prevalence of hookworms in dogs from Egypt. The length of line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence; Figure S4: Forest plot diagram for random effects in the meta-analysis of the prevalence of Taenia spp. in dogs from Egypt. The length of line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence. Figure S5: Forest plot diagram for random effects in the meta-analysis of the prevalence of H. heterophyes in dogs from Egypt. The length of line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.

Author Contributions

Conceptualization, I.A., M.G. and M.A.R.; methodology, I.A., M.G. and M.A.R.; software, I.A.; validation, M.G. and M.A.R.; formal analysis, I.A. and E.-S.E.-A.; investigation, M.G. and M.A.R.; resources, I.A., M.G. and M.A.R.; data curation, I.A. and M.G.; writing—original draft preparation, I.A., M.G., M.A.R. and B.E.; writing—review and editing, I.A. and E.-S.E.-A.; visualization, H.B.B. and M.A.R.; supervision, I.A. and M.A.R.; project administration, I.A. and M.A.R.; funding acquisition, H.B.B. and M.A.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The study was approved by Mansoura University Animal Care and Use Committee (MU-ACUC) MU-ACUC, approval number and date: VM.R.22.11.29, 23/11/2022.

Data Availability Statement

On reasonable request, the corresponding authors will provide the datasets created and/or analyzed during the current work.

Conflicts of Interest

The authors have declared no conflicts of interest.

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Animals 13 00496 g001 550
Figure 1. Flow diagram established according to PRISMA guidelines and showing methodologies of databases search and selection of eligible articles.
Figure 1. Flow diagram established according to PRISMA guidelines and showing methodologies of databases search and selection of eligible articles.
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Animals 13 00496 g002 550
Figure 2. Forest plot diagram for random effects in the meta-analysis of the prevalence of T. canis in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
Figure 2. Forest plot diagram for random effects in the meta-analysis of the prevalence of T. canis in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
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Animals 13 00496 g003 550
Figure 3. Forest plot diagram for random effects in the meta-analysis of the prevalence of E. granulosus in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
Figure 3. Forest plot diagram for random effects in the meta-analysis of the prevalence of E. granulosus in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
Animals 13 00496 g003
Animals 13 00496 g004 550
Figure 4. Forest plot diagram for random effects in the meta-analysis of the prevalence of D. caninum in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
Figure 4. Forest plot diagram for random effects in the meta-analysis of the prevalence of D. caninum in dogs from Egypt. The length of the line indicates 95% confidence interval of each study and the middle point of each line refers to the prevalence. Diamond refers to the overall prevalence.
Animals 13 00496 g004
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Abbas, I.; Baghdadi, H.B.; Rizk, M.A.; El-Alfy, E.-S.; Elmishmishy, B.; Gwida, M. Gastrointestinal Parasites of Dogs in Egypt: An Update on the Prevalence in Dakahlia Governorate and a Meta-Analysis for the Published Data from the Country. Animals 2023, 13, 496. https://doi.org/10.3390/ani13030496

AMA Style

Abbas I, Baghdadi HB, Rizk MA, El-Alfy E-S, Elmishmishy B, Gwida M. Gastrointestinal Parasites of Dogs in Egypt: An Update on the Prevalence in Dakahlia Governorate and a Meta-Analysis for the Published Data from the Country. Animals. 2023; 13(3):496. https://doi.org/10.3390/ani13030496

Chicago/Turabian Style

Abbas, Ibrahim, Hanadi B. Baghdadi, Mohamed Abdo Rizk, El-Sayed El-Alfy, Bassem Elmishmishy, and Mayada Gwida. 2023. "Gastrointestinal Parasites of Dogs in Egypt: An Update on the Prevalence in Dakahlia Governorate and a Meta-Analysis for the Published Data from the Country" Animals 13, no. 3: 496. https://doi.org/10.3390/ani13030496

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