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Article

Seroprevalence of Toxoplasma gondii, Neospora caninum and Trichinella spp. in Pigs from Cairo, Egypt

by
Ragab M. Fereig
1,*,†,
El-Sayed El-Alfy
2,†,
Hanan H. Abdelbaky
3,
Nour H. Abdel-Hamid
4,
Amira M. Mazeed
5,
Ahmed M. S. Menshawy
6,
Mohamed A. Kelany
7,
Mohamed El-Diasty
8,
Bader S. Alawfi
9 and
Caroline F. Frey
10,*
1
Division of Internal Medicine, Department of Animal Medicine, Faculty of Veterinary Medicine, South Valley University, Qena 83523, Egypt
2
Department of Parasitology, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
3
Doctor of Veterinary Sciences, Veterinary Clinic, Veterinary Directorate, Qena 83523, Egypt
4
Brucellosis Research Department, Agricultural Research Center, Animal Health Research Institute, Cairo 12618, Egypt
5
Department of Infectious Disease, Faculty of Veterinary Medicine, Arish University, Arish City 45511, North Sinai, Egypt
6
Department of Veterinary Medicine, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef 62511, Egypt
7
Department of Microbiology, The Central Laboratory of Residual Analysis of Pesticides and Heavy Metals in Foods, Agricultural Research Center, Dokki, Giza 12618, Egypt
8
Agricultural Research Center (ARC), Animal Health Research Institute-Mansoura Provincial Lab. (AHRI-Mansoura), Giza 12618, Egypt
9
Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Taibah University, Madinah 42353, Saudi Arabia
10
Institute of Parasitology, Department of Infectious Diseases and Pathobiology, Vetsuisse-Faculty, University of Bern, Länggassstrasse 122, CH-3012 Bern, Switzerland
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Vet. Sci. 2023, 10(12), 675; https://doi.org/10.3390/vetsci10120675
Submission received: 18 October 2023 / Revised: 12 November 2023 / Accepted: 25 November 2023 / Published: 27 November 2023
(This article belongs to the Special Issue Immunological Study of Toxoplasma gondii Infection in Animals)
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Abstract

:

Simple Summary

Toxoplasma gondii and Trichinella species are parasites of major public health importance because they cause severe clinical consequences in infected humans. In addition, infections of Neospora caninum in livestock are reported to cause substantial losses to the economy because of adverse effects on animal production and reproduction. In Egypt, the breeding of pigs has particular characteristics regarding the targeted consumers (tourists and Christians), breeding places (Cairo and Giza), and licensed abattoirs (only El-Bassatin in Cairo). Herein, we sought to provide a comprehensive investigation of the major parasites of pigs, including T. gondii, Trichinella species, and N. caninum, a parasite of high priority in ruminants. This study revealed variable seropositive rates against all tested parasites in pigs from Cairo, Egypt. Seropositivity was the highest for T. gondii (45.8%), followed by N. caninum (28.0%), mixed infection by both parasites (18.7%), and Trichinella spp. (1.2%). We also found the location was a predisposing factor for seropositivity for T. gondii, while location and sex were identified as predisposing factors for N. caninum seropositivity in pigs. The provided information in this study presents valuable information on the seroprevalence of T. gondii and Trichinella, and novel information on N. caninum existence among pigs in Cairo, Egypt.

Abstract

Pork production is a niche economy in Egypt, and pigs are typically raised as backyard animals with no sanitary control, potentially exposing them to various pathogens. Commercially available ELISAs were used to detect specific antibodies to the food-borne zoonotic parasites Toxoplasma gondii and Trichinella spp., as well as to Neospora caninum, in serum samples of pigs slaughtered at Egypt’s only licensed pig abattoir, the El-Bassatin abattoir in Cairo. Among the tested sera (n = 332), seroreactivity for T. gondii was 45.8% (95% confidence interval: 40.4–51.3), N. caninum was 28.0% (95% CI: 23.3–33.2), and Trichinella spp. was 1.2% (95% CI: 0.4–3.3). Mixed infection was only detected for T. gondii and N. caninum (18.7%; 95% CI: 14.7–23.4). The seroprevalence of T. gondii was significantly higher (p = 0.0003) in animals collected from southern Cairo (15 May city slum) than in eastern Cairo (Ezbet El Nakhl slum). Seroprevalence for N. caninum was higher in western (Manshiyat Naser slum; p = 0.0003) and southern Cairo (15 May city slum; p = 0.0003) than in that of eastern Cairo (Ezbet El Nakhl slum; p = 0.0003). Moreover, female pigs exhibited a higher rate of N. caninum antibodies than male ones (p < 0.0001). This study provides the first seroprevalence data for N. caninum in pigs in Egypt, and updates the prevalence of the zoonotic parasites Trichinella spp. and T. gondii.

1. Introduction

A lack of food security is one of the issues plaguing the world’s rapidly growing human population, and the global prevalence of malnutrition increased dramatically between 2019 and 2020, owing mostly to the COVID-19 pandemic [1]. The population in Egypt is growing fast; the estimated population in 2021 was 109.3 million, with a population change rate of 1.59% [2]. Egypt is primarily a Muslim country; however, it has lately been estimated that approximately 10% of the Egyptian population are Christians [3]. The swine/pigs stock number in the country was estimated as 11,000 head by the year 2021 [4]. Pigs in Egypt are typically reared as backyard animals and fed on human garbage [5,6]. Consequently, it is critical to investigate pigs for parasites that are either of zoonotic or veterinary importance.
With a global distribution, Toxoplasma gondii infects nearly all warm-blooded animals, including humans, livestock, and marine mammals [7,8]. The definitive hosts are felids, which produce and shed environmentally-resistant oocysts [8,9]. Pigs, like humans and other animals, become infected with T. gondii after ingesting sporulated oocysts shed by cats or tissue cysts in the meat of other intermediate hosts [10]. Natural T. gondii infection in pigs is a public health issue, as transmission to humans by consumption of raw or undercooked pork meat or offal can occur [11]. Infections in pigs are usually asymptomatic or with non-pathognomonic symptoms, and severe clinical toxoplasmosis is rare [11]. Human primary infection with T. gondii normally manifests as mild flu-like symptoms in immune-competent hosts; however, it can induce life-threatening infections in immune-compromised persons. Furthermore, T. gondii transplacental transmission during pregnancy might result in significant complications such as abortion, stillbirth, or congenital anomalies [8].
The pooled global T. gondii seroprevalence in pigs (148,092 pigs from 47 countries) was estimated to be 19% based on different serological methods, among which enzyme-linked immunosorbent assays (ELISA) were used most frequently [12]. In Egypt, the reported seroprevalence in pigs varies between 14% and 80.4% [13,14,15,16,17,18,19,20,21]. Additionally, viable T. gondii was isolated from the heart of a healthy seropositive pig in Egypt. Many cases of human toxoplasmosis have been reported in Egypt and reviewed previously. The reported seroprevalence of T. gondii in the Egyptian human population ranges from 2.5% to 67.4%, and toxoplasmosis is commonly regarded by Egyptian physicians as a cause of abortions and complications in pregnant women; nonetheless, the published studies are not well-structured, and there is a lack of definitive diagnoses [20,21,22].
Neosporosis is a disease caused by the heteroxenous cyst-forming parasite Neospora caninum, an intracellular apicomplexan protozoan that infects a wide range of domestic and wild animals [23]. The definitive hosts of N. caninum are domestic and wild dogs, coyotes, and grey wolves [24,25]. Cattle are the most common intermediate hosts of N. caninum; however, sheep, water buffaloes, bison, and white-tailed deer have also been identified as intermediate hosts [26]. Abortions and newborn mortality are serious complications of neosporosis in livestock, particularly in cattle [23,24].
Anti-N. caninum antibodies have been reported in domestic and feral pigs from various countries [24], and, more recently, parasite DNA has been detected in the brains of domestic pigs in China [27], indicating natural infection. However, the pathogenesis of neosporosis and its consequences in pigs remains unclear [28,29]. The detection of N. caninum infection in live animals is based mainly on the identification of anti-N. caninum antibodies using a variety of serological tests, the most frequently used of which is ELISA [30,31]. In Egypt, N. caninum infections have been detected in domestic animals such as cattle, buffaloes, and camels, but there have been no reports in pigs.
Trichinella nematodes are zoonotic parasites with a global distribution [32]. Pork is the most common source of human trichinellosis, which can cause clinical symptoms such as myalgia, diarrhea, fever, facial edema, and headaches, and may even be fatal [33]. Trichinella spiralis is the only species reported in Egypt so far [32], and it has been identified in pigs [34,35], rodents [36], and dogs [34,37]. In Egypt, the reported infection rate in slaughtered pigs and pork products ranges from 0% to 6% [19,35,38,39,40,41]. Only one old report on the seroprevalence of Trichinella spp. in pigs in Egypt (35.6%) was found in a literature search, and it used an immunofluorescent antibody test (IFAT) [42]. Nevertheless, ELISA is the recommended assay for epidemiologic serosurveillance of pigs for Trichinella infection [43]. Human trichinellosis linked to the consumption of pork has recently been reported from Egypt based on ELISA, and the seroprevalence rate of T. spiralis (IgG) was 10% (9/90) [35] and 60.9% (56/92) [40] in the examined humans.
Based on the above-mentioned facts, there have been a few reports in Egypt on the prevalence of T. gondii and Trichinella spp. in pigs, but none on N. caninum. We therefore opted to update the information on the seroprevalence of T. gondii and Trichinella spp., as well as to provide baseline data for the seroprevalence of N. caninum infections, in pigs in Egypt. Our presented data will serve the public health and veterinary sectors in minimizing the health and economic hazards of these parasites in Egypt.

2. Materials and Methods

2.1. Description of the Animals and Regions of the Study

Blood samples were collected from male and female pigs (n = 332) during slaughtering in the El-Bassatin abattoir in the Cairo governorate. All pigs were raised in backyard pens containing 50 to 100 pigs in the slums of the Cairo governorate by garbage collectors as one of their main sources of income. These rearing pens and slums lack many procedures ensuring sanitary conditions or biosecurity and pigs are fed mainly on garbage. This condition allows for high rates of contact with free-roaming animals such as dogs, cats, rodents, and birds, increasing the incidence of infection with many biohazardous agents. In addition, other livestock animals, especially sheep, are also reared with these pigs. The majority of pigs are reared for fattening and are slaughtered at the age of 5 months. They are typically sold to pig merchants who collect animals from different small-scale farmers and ship them to the abattoir. Pigs used in this study originated from the following slums: Manshiyat Naser, Cairo’s largest pig farming slum in the western region (30.0362°N, 31.2783°E) (n = 108; female 75, male 33); Ezbet El Nakhl (30.1393°N, 31.3244°E) (n = 184; female 125, male 59) in the eastern Cairo region; and 15 May city (29.8579°N, 31.3885°E) (n = 40; all of them male) in the southern Cairo region (Figure 1). The pigs from various herds were held together in abattoir pens before slaughtering without identification.
Blood was collected in plain tubes without anticoagulants directly from the slaughtered animals during bleeding according to the El-Bassatin abattoir regulations for pig slaughtering and pork processing. All samples were labeled and transferred on ice to the Reference Laboratory at the Animal Health Research Institute (AHRI), Giza. Upon arrival at the laboratory, blood samples were kept overnight for serum separation and then centrifuged at 900× g for 10 min. Serum samples were aliquoted and kept at −20 °C until testing. Aliquots from these samples were sent on ice to the Faculty of Veterinary Medicine, South Valley University, Qena, for ELISA testing.

2.2. ELISAs for Screening Antibodies to T. gondii, N. caninum, and Trichinella Species in Pigs

Regarding T. gondii, the serum samples were tested using an indirect multi-species ELISA for toxoplasmosis (ID.vet, Grabels, France) according to the manufacturer’s instructions. Serum samples and controls were diluted 1:10. The optical density (OD) obtained was used to determine the percentage of sample (S) to positive (P) ratio (S/P %) for each of the test samples using the following formula: S/P (%) = (OD sample – OD negative control)/(OD positive control − OD negative control) × 100. Samples with an S/P% less than 40% were regarded as negative, an S/P% between 40% and 50% was regarded as doubtful, and the test was considered positive if the S/P% was more than 50%.
For N. caninum, serum samples were analyzed using a competitive multi-species ELISA for neosporosis (ID.vet, Grabels, France). Serum samples and controls were diluted 1:2. The ODs obtained were used to calculate the percentage of sample (S) to negative (N) ratio (S/N%) for each of the test samples according to the following formula S/N (%) = OD sample/OD negative control × 100. Samples with an S/N% more than 60% were regarded as negative, an S/N% between 50% and 60% was regarded as doubtful, and the test was considered positive if the S/N% was less than 50%.
Serum samples were analyzed for Trichinella species using an indirect multi-species ELISA for trichinellosis (ID.vet, Grabels, France). Serum samples and controls were diluted 1:20. The ODs obtained were used to determine the percentage of sample (S) to positive (P) ratio (S/P %) for each of the test samples using the following formula: S/P (%) = (OD sample − OD negative control)/(OD positive control − OD negative control) × 100. Samples with an S/P% less than 50% were regarded as negative, an S/P% between 50% and 60% was regarded as doubtful, and the test was considered positive if the S/P% was greater than or equal to 60%.
The ODs of all ELISA results were read at 450 nm using an Infinite® F50/Robotic ELISA reader (Tecan Group Ltd., Männedorf, Switzerland). See Table 1 for additional information on the ELISAs used in this study.

2.3. Statistical Analysis

The significance of the differences in the prevalence rates and risk factors were analyzed using Fisher’s exact test, 95% confidence intervals (95% CI) (including a continuity correction), and odds ratios (OR) using an online statistical website www.vassarstats.net (accessed on 22 July 2023). From this website, calculator 3 was selected from the clinical research calculators. Then, in squares of data entry, the numbers of negative (absent) and positive (present) samples from group 1 (regarded as the reference group) were added. Similarly in the lower squares, the numbers of negative and positive samples were added. In these tests, we used the two-tailed p values of Fisher’s exact test. p-values and odds ratios were confirmed with GraphPad Prism version 5 (GraphPad Software Inc., La Jolla, CA, USA) [44,45].

3. Results

The overall seroprevalence in the studied pigs for T. gondii was 45.8% (152/332; 95% CI: 40.4–51.3), N. caninum was 28.0% (93/332; 95% CI: 23.3–33.2), and Trichinella spp. was 1.2% (4/332; 95% CI: 0.4–3.3). Mixed infections were only detected for T. gondii and N. caninum at 18.7% (62/332; 95% CI: 14.7–23.4) (Table 2).
Risk factor analysis was conducted to assess the influence of sex and breeding location on the seroprevalence of T. gondii and N. caninum, but not for Trichinella because of the limited number of seropositive samples. Breeding site was identified as the only predisposing factor for T. gondii infection. The seroprevalence of T. gondii in pigs reared in 15 May city, southern Cairo (67.5%) set as the reference group was higher than that in Ezbet El Nakhl, eastern Cairo (35.3%) (OR = 3.8, p = 0.0003), but not significantly higher than in Manshiyat Naser, western Cairo (55.6%) (OR = 0.6, p = 0.259). On the other hand, sex had no influence on the T. gondii seroprevalence (Table 3).
For N. caninum antibody levels, both sex and breeding site were considered risk factors. The seropositive rate was significantly higher in female pigs (38%) set as a reference than in male pigs (12.9%, OR = 4.1, p ≤ 0.0001). Also, the seroprevalence of N. caninum in pigs located in Ezbet El Nakhl (13%) set as the reference group was significantly lower than that recorded in Manshiyat Naser (53.7%, OR = 7.7, p ≤ 0.0001) and 15 May city (27.5%, OR = 2.5, p ≤ 0.031) (Table 4).

4. Discussion

Despite the presence of a considerable pig population and pig consumers in Egypt, there has been relatively little effort to conduct parasite epidemiological studies. Herein, we targeted pigs as sentinel animals for infection with three parasites: T. gondii, N. caninum, and Trichinella species. All animals were admitted to El-Bassatin abattoir, Cairo, the only licensed place for pig slaughtering in Egypt. The highest seroprevalence was recorded for T. gondii (45.8%), followed by N. caninum (28.0%) and T. gondii and N. caninum co-infection (18.7%), and the lowest was for Trichinella spp. (1.2%).
A variety of techniques and antigens are available for the detection of distinct immunoglobulin isotypes against T. gondii [46,47], among which ELISA has been the most frequently used method in the past century [48]. In Egypt, few serological studies have been published for T. gondii infections in pigs, and prevalence rates between 14% and 80.4% have been reported [13,14,15,16,17,18,19,20,21]. These studies were conducted over a large time span (1972–2015), and a multitude of test types were used, such as indirect fluorescent antibody test (IFAT) [13,16], indirect hemagglutination assay (IHA) [19,20], dye test (DT) [14], modified agglutination test (MAT) [15], and ELISA [17,18]. In the present study, we opted for commercially available ELISAs, which have the advantage of good repeatability, robustness, and reportedly very good sensitivity and specificity. The detected seroprevalence of 45.8% for T. gondii in the assessed backyard pigs indicates a potential risk to the health of pig fatteners, abattoir workers, and consumers. A similar finding was published by Barakat et al. [16], who reported a seroprevalence for T. gondii of 74.7% in pigs reared entirely on waste feed in Cairo, and a seroprevalence of 37.7% (48 of 127) in the workers at these pig farms.
Neospora caninum infection in Egyptian animals is underestimated, with a few seroprevalence reports in cattle, buffaloes, sheep, goats, camels, dogs, and cats, as well as limited information on clinical neosporosis. In our previous reports using the same ELISA as in the current study, we demonstrated seroprevalence rates for N. caninum of 3.9% in camels [44], 15.5% and 5% in sheep and goats, respectively [45], 5.8% in dogs, 3.4% in cats [49], and 24.6% in cattle [50]. Nonetheless, serum samples from aborted cows revealed N. caninum infections in addition to Coxiella burnetii [51] or Bovine Viral Diarrhoea Virus [52]. Furthermore, the number of N. caninum seropositive camels increased among females with an abortion history [53]. On the other hand, the pathogenesis of neosporosis and its consequences in pigs remains unclear [28,29]. Neospora caninum experimental infection in pigs can be transferred through the placenta and produce reproductive problems such as mummified fetuses, particularly in the first and second gestational thirds [28].
To the best of our knowledge, the current study is the first serological study of N. caninum infection in pigs in Egypt. Thus, we compared our recorded prevalence (28%) with the rates in other animals in different regions of Egypt. Although N. caninum might not be a serious parasite for the pig industry, its detection in pigs might constitute a major risk for ruminants and other animals because of multiple species being raised in the same place. The seroprevalence in pigs was most similar to rates reported in cattle (24.6% [50], 29% [51], and 30.2% [52]) and higher than the rates reported in all other animal species, with the exception of one study in buffaloes (Table 5). Furthermore, in comparison with the seroprevalence rate of N. caninum in domestic pigs from other countries, our infection rate seemed higher. For example, a rate of 3% was reported in the Czech Republic [54]; 1.9% in Hunan province, China [27]; 5.2% in Brazil [55]; and 6.7% in Italy [56] for N. caninum infections in pigs. Only one study found a higher seroprevalence rate (36.4%) in Qinghai-Tibetan plateau, China [57].
Overall, these findings can best be explained by the sanitary conditions in which the pigs were raised. They were garbage-fed backyard pigs and fattened as an additional income by inhabitants of the slums of Cairo. Both parasites can be transmitted through the feeding of uncooked infected meat from other species or via oocysts shed by cats for T. gondii or by dogs for N. caninum [8,23]. Slums typically harbor a large population of stray cats, dogs, and other animals that may serve as sources of infection for the pigs.
Little is known about the oocyst-shedding rates of cats and dogs in Egypt. The presence of T. gondii-like oocysts in the feces of cats in Egypt may have been overestimated, where 1432 cats were examined, revealing a pooled prevalence of 11.9% [64]. Neospora caninum-like oocysts were found in the feces of one of 78 dogs tested in a single study (Dakahlia governorate), and it is conceivable that certain small-sized oocysts detected in prior studies from Egypt are N. caninum [65]. Furthermore, N. caninum-like oocysts were found in the feces of five of nine puppies fed the placentas and brains of nine aborted bovine fetuses in Egypt [66].
In this study, we analyzed the effects of sex and breeding locations on the seroprevalence of T. gondii and N. caninum infection. The breeding location was identified as a risk factor for T. gondii where 15 May city had a significantly higher seroprevalence than the two other places. For N. caninum, both sex and location significantly affected the prevalence rate; females had a higher rate than males, and meanwhile, 15 May and Manshiyat Naser had higher rates than Ezbet El Nakhl. Notably, 15 May city recorded the highest prevalence for both T. gondii and N. caninum. This might be related to the more recent establishment of 15 May city, which has a larger desert area compared to the other two locations, and thus a higher chance of the presence of wild canines and felines. Another reason might be its distant location from the crowded areas of Cairo, which rendered it a main place for garbage collection. However, because this is the first study that investigated such factors in Egypt, other investigations are required to confirm these results and reveal the cause of variations. Meanwhile, numerous studies have found that location is a risk factor for the seroprevalence of T. gondii in pigs or other animals [21]. Concerning N. caninum in pigs, the available data are very scanty, both in Egypt and globally. Nevertheless, the location is considered a potential risk factor for N. caninum in other animal species [45,50,67,68]. Similarly, and taking into account the limited data concerning pigs, sex is regarded as a risk factor for T. gondii and N. caninum in cases of other animal species [50,69]. Age is usually also a risk factor for seropositivity to T. gondii or N. caninum, but this could not be assessed in our study, as all pigs were slaughtered at approx. 5 months old.
Trichinella spp. transmission primarily occurs in poor areas where veterinary services are unavailable, as well as in traditional small-scale “backyard” rearing of pigs for household and local use, particularly by the feeding of food waste [70,71]. Trichinella infection in pigs can be prevented through management practices such as grain feeding or cooking the feed garbage, indoor production, and removing rat carcasses from the premises [72,73,74,75].
In Egypt, larvae of Trichinella spp. have infrequently been found by trichinoscopy and/or digestion methods (Table 6). Interestingly, data on 33,812 slaughtered pigs were collected through a standard form from the El-Bassatin abattoir archives during one year of screening, and 359 (1.06%) were found to be infected [35]. However, Mohammed et al. [35] additionally tested a subsample of pigs with the digestion method and found a higher prevalence of 3.3%. Using artificial digestion, a prevalence rate of 13.3% was determined in rodents from Alexandria, and high infection rates were identified in rodents taken from and surrounding abattoirs [36]. Based on the isoenzyme electrophoretic patterns, Trichinella spiralis was identified in two stray dogs [37], two isolates from domestic pigs, and one isolate from a domestic dog from Egypt [34], and by PCR in domestic pigs [35]. Furthermore, human trichinellosis linked to the consumption of pork has been reported in Egypt [35,40,76,77,78].
Although current serodiagnostic approaches cannot replace traditional meat inspection for this zoonotic nematode, ELISA can be useful for surveillance programs and generally has an increased sensitivity compared to direct detection of larvae [79]. ELISA testing of 14,579 sera from pigs in 21 studies indicated an overall prevalence of 4.3% worldwide [75]. The seroprevalence rate obtained for Trichinella infection in pigs in our study was quite low (1.2%) and very similar to the infection rates determined by trichinoscopy at slaughter. Experimental studies have shown that Trichinella species have a different larval burden and immunological response in pigs at 30–70 days post-infection that can last up to 40 weeks [80,81,82,83]. Thus, the low seroprevalence of Trichinella spp. might be related to the younger age of tested pigs that are slaughtered at an age of 5 months. Likewise, the seroprevalence of Trichinella spp. in Vietnam increased with the pigs’ age: it was 1.1%, 1.2%, 32.9%, and 55.6% for pigs < 2 months, 2–8 months, 9–36 months, and >36 months, respectively [84]. Larger studies including different age groups and combining serological and direct methods should be envisaged to determine the infection rate in Egyptian pigs.
In conclusion, this study revealed variable seropositive rates against all tested parasites in pigs from Cairo, Egypt. Seropositivity was highest in T. gondii (45.8%) followed by N. caninum (28%) and Trichinella spp. (1.2%). Likewise, a high rate of mixed infections (18.7%) was noticed for T. gondii and N. caninum. Location was reported as a risk factor for seropositivity for T. gondii, while location and sex significantly affected N. caninum seropositivity in pigs. Future studies, including larger sample sizes and more diverse regions of Egypt, are required to highlight the national prevalence of these parasites and determine their potential public health risk. Furthermore, using molecular methods for genotyping and species identification of T. gondii and Trichinella spp., respectively, is critical to evaluate pigs’ role in the transmission of these parasites to humans in Egypt.

Author Contributions

Conceptualization and design, R.M.F. and C.F.F.; experiments, formal analysis, and investigation, R.M.F., E.-S.E.-A., H.H.A., N.H.A.-H., A.M.M., A.M.S.M., M.A.K., M.E.-D., B.S.A. and C.F.F.; resources and shared materials, R.M.F., E.-S.E.-A., H.H.A., N.H.A.-H., A.M.M., A.M.S.M., M.A.K., M.E.-D., B.S.A. and C.F.F.; writing—original draft, R.M.F., E.-S.E.-A. and C.F.F.; writing—review and editing, R.M.F. and C.F.F. Project administration and funding acquisition; R.M.F. and C.F.F. All authors have read and agreed to the published version of the manuscript.

Funding

This study did not receive any special funds.

Institutional Review Board Statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study was approved by the Mansoura University Animal Care and Use Committee (MU-ACUC), approval code number: VM.R.23.07.116.

Informed Consent Statement

Verbal consent was obtained from animal owners before collection of samples after full explanation of the purposes of the study.

Data Availability Statement

All data generated and analyzed during this study are included in this published article. The raw data supporting the findings of this study are available from the corresponding author on request.

Acknowledgments

We thank all veterinarians who helped with collecting blood samples from the tested animals and the animal owners for their cooperation in providing animals and the required data and information for each animal. We would like to express our appreciation of the great help, cooperation, and technical assistance of our colleagues at the Department of Animal Medicine, Faculty of Veterinary Medicine, South Valley University, Qena.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. FAO. World Food and Agriculture—Statistical Yearbook 2021; FAO: Rome, Italy, 2021. [Google Scholar] [CrossRef]
  2. United Nations. Population Estimates and Projections; United Nations: New York, NY, USA, 2022; Available online: https://population.un.org (accessed on 13 June 2023).
  3. U.S. Department of State. International Religious Freedom Report for 2020: Egypt; United States Department of State, Office of International Religious Freedom: Washington, DC, USA, 2021. Available online: https://www.state.gov/reports/2020-report-on-international-religious-freedom/egypt/ (accessed on 23 June 2023).
  4. FAOSTAT. 2021. Available online: http://www.fao.org/faostat/en/#data/QA (accessed on 23 June 2023).
  5. Shalaby, E.A. Prospects of effective microorganisms technology in wastes treatment in Egypt. Asian Pac. J. Trop. Biomed. 2011, 1, 243–248. [Google Scholar] [CrossRef] [PubMed]
  6. Redding, R.W. The pig and the chicken in the Middle East: Modeling human subsistence behavior in the archaeological record using historical and animal husbandry data. J. Archaeol. Res. 2015, 23, 325–368. [Google Scholar] [CrossRef]
  7. Tenter, A.M.; Heckeroth, A.R.; Weiss, L.M. Toxoplasma gondii: From animals to humans. Int. J. Parasitol. 2000, 30, 1217–1258. [Google Scholar] [CrossRef] [PubMed]
  8. Dubey, J.P. Toxoplasmosis of Animals and Humans, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2010. [Google Scholar]
  9. Elmore, S.A.; Jones, J.L.; Conrad, P.A.; Patton, S.; Lindsay, D.S.; Dubey, J.P. Toxoplasma gondii: Epidemiology, feline clinical aspects, and prevention. Trends Parasitol. 2010, 26, 190–196. [Google Scholar] [CrossRef] [PubMed]
  10. Dubey, J.P.; Weigel, R.M.; Siegel, A.M.; Thulliez, P.; Kitron, U.D.; Mitchell, M.A.; Mannelli, A.; Mateus-Pinilla, N.E.; Shen, S.K.; Kwok, O.C.H.; et al. Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. J. Parasitol. 1995, 81, 723–729. [Google Scholar] [CrossRef] [PubMed]
  11. Dubey, J.P.; Cerqueira-Cézar, C.K.; Murata, F.H.; Kwok, O.C.; Hill, D.; Yang, Y.; Su, C. All about Toxoplasma gondii infections in pigs: 2009–2020. Vet. Parasitol. 2020, 288, 109185. [Google Scholar] [CrossRef] [PubMed]
  12. Foroutan, M.; Fakhri, Y.; Riahi, S.M.; Ebrahimpour, S.; Namroodi, S.; Taghipour, A.; Spotin, A.; Gamble, H.R.; Rostami, A. The global seroprevalence of Toxoplasma gondii in pigs: A systematic review and meta-analysis. Vet. Parasitol. 2019, 269, 42–52. [Google Scholar] [CrossRef] [PubMed]
  13. Maronpot, R.R.; Botros, B.A.M. Toxoplasma serologic survey in man and domestic animals in Egypt. J. Egypt. Public Health Assoc. 1972, 47, 58–67. [Google Scholar]
  14. Rifaat, M.A.; Morsy, T.A.; Sadek, M.S.M.; Azab, M.E.; Khaled, M.L.M.; Safar, E.H. Incidence of toxoplasmosis among farm animals in north coastal zone of Egypt. J. Egypt. Soc. Parasitol. 1979, 9, 193–197. [Google Scholar]
  15. Ghattas, S.S. Studies on Toxoplasma gondii Infecting Slaughtered Pigs in Egypt. MSc. Thesis, Cairo University, Cairo, Egypt, 1999. [Google Scholar]
  16. Barakat, A.M.; El Fadaly, H.A.; Shaapan, R.M.; Khalil, F.A.M. Occupational health hazard of Egyptian employees in contact with wastage nourished swine. J. Am. Sci. 2011, 7, 808–903. [Google Scholar]
  17. El Moghazy, F.M.; Kandil, O.M.; Shaapan, R.M. Toxoplasma gondii: Comparison of some serological tests for detection in sera of naturally infected pigs. World J. Zool. 2011, 6, 204–208. [Google Scholar]
  18. Hassanain, M.A.; El-Fadaly, H.A.; Hassanain, N.A.; Shaapan, R.M.; Barakat, A.M.; Abd El-Razik, K.A. Serological and molecular diagnosis of toxoplasmosis in human and animals. World J. Medical Sci. 2013, 9, 243–247. [Google Scholar]
  19. Abdel-Hafeez, E.H.; Kamal, A.M.; Abdelgelil, N.H.; Abdel-Fatah, M. Parasites transmitted to human by ingestion of different types of meat, El-Minia City, El-Minia Governorate, Egypt. J. Egypt. Soc. Parasitol. 2015, 45, 671–680. [Google Scholar] [PubMed]
  20. Ibrahim, M.H.S. Studies on Parasitic Infections among Egyptian pigs. MSc. Thesis, Benha University, Benha, Egypt, 1990. [Google Scholar]
  21. Abbas, I.E.; Villena, I.; Dubey, J.P. A review on toxoplasmosis in humans and animals from Egypt. Parasitology 2020, 147, 135–159. [Google Scholar] [CrossRef]
  22. Botros, B.A.M.; Moch, R.W.; Barsoum, I.S. Toxoplasmosis in Egypt: Isolation of Toxoplasma gondii from a pig. J. Trop. Med. Hyg. 1973, 76, 259–261. [Google Scholar]
  23. Dubey, J.P.; Schares, G.; Ortega-Mora, L. Epidemiology and control of neosporosis and Neospora caninum. Clin. Microbiol. Rev. 2007, 20, 323–367. [Google Scholar] [CrossRef]
  24. Dubey, J.P.; Hemphill, A.; Calero-Bernal, R.; Schares, G. Neosporosis in Animals; CRC Press: Boca Raton, FL, USA, 2017. [Google Scholar]
  25. Fereig, R.M.; Nishikawa, Y. From signaling pathways to distinct immune responses: Key factors for establishing or combating Neospora caninum infection in different susceptible hosts. Pathogens 2020, 9, 384. [Google Scholar] [CrossRef]
  26. Dubey, J.P.; Schares, G. Neosporosis in animals—The last five years. Vet. Parasitol. 2011, 180, 90–108. [Google Scholar] [CrossRef]
  27. Gui, B.Z.; Lv, Q.Y.; Ge, M.; Li, R.C.; Zhu, X.Q.; Liu, G.H. First report of Neospora caninum infection in pigs in China. Transbound. Emerg. Dis. 2020, 67, 29–32. [Google Scholar] [CrossRef]
  28. Snak, A.; Junior, G.S.; Pilati, G.V.T.; Kroetz, C.C.; Consoni, W.; Cristani, J.; de Moura, A.B. Does Neospora caninum cause reproductive problems in pigs? Vet. Parasitol. 2019, 275, 108934. [Google Scholar] [CrossRef]
  29. Snak, A.; Henrique, S.M.; Sebolt, A.P.R.; Cristani, J.; Sato, M.E.; Miletti, L.C.; de Moura, A.B. Experimental infection of tachyzoites of the NC1 strain of Neospora caninum in female swine. Parasitol. Res. 2021, 120, 1049–1057. [Google Scholar] [CrossRef]
  30. Dubey, J.P.; Schares, G. Diagnosis of bovine neosporosis. Vet. Parasitol. 2006, 140, 1–34. [Google Scholar] [CrossRef] [PubMed]
  31. Sinnott, F.A.; Monte, L.G.; Collares, T.F.; Silveira, R.M.; Borsuk, S. Review on the immunological and molecular diagnosis of neosporosis (years 2011–2016). Vet. Parasitol. 2017, 239, 19–25. [Google Scholar] [CrossRef] [PubMed]
  32. Pozio, E.; Zarlenga, D.S. New pieces of the Trichinella puzzle. Int. J. Parasitol. 2013, 43, 983–997. [Google Scholar] [CrossRef] [PubMed]
  33. Murrell, K.D.; Pozio, E. Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerg. Infect. Dis. 2011, 17, 2194. [Google Scholar] [CrossRef]
  34. La Rosa, G.; Pozio, E.; Rossi, P.; Murrell, K.D. Allozyme analysis of Trichinella isolates from various host species and geographical regions. J. Parasitol. 1992, 78, 641–646. [Google Scholar] [CrossRef] [PubMed]
  35. Mohammed, E.S.; Youseef, A.G.; Mubarak, A.G.; Mawas, A.S.; Khalifa, F.A.; Felefel, W. Epidemiological perspective associated with principal risk factors of Trichinella spiralis infection in pigs and humans in Egypt. Vet. World 2022, 15, 1430. [Google Scholar] [CrossRef]
  36. Loutfy, N.F.; Awad, O.M.; El-Masry, A.G.; Kandil, G.M. Study on rodents infestation in Alexandria and prevalence of Trichinella spiralis infection among them. J. Egypt. Soc. Parasitol. 1999, 29, 897–909. [Google Scholar]
  37. Mikhail, E.M.; Mansour, N.S.; Awadalla, H.N. Identification of Trichinella isolates from naturally infected stray dogs in Egypt. J. Parasitol. 1994, 80, 151–154. [Google Scholar] [CrossRef]
  38. Yassien, M.; Abd EL-Rahman, H.; Ibrahim, A.; Mousa, M. Prevalence of encysted larvae of Trichinella spiralis in pork and beef meat products with special reference to the effect of rapid heat treatment on their viability. Assiut Vet. Med. J. 1989, 21, 84–92. [Google Scholar]
  39. Morsy, T.A.; Ibrahim, B.B.; Haridy, F.M.; Rifaat, M.M. Trichinella encysted larvae in slaughtered pigs in Cairo (1995–1999). J. Egypt. Soc. Parasitol. 2000, 30, 753–760. [Google Scholar] [PubMed]
  40. Sayed, A.S.; Hussein, A.A.; Arafa, M.I.; Abdo, B.R.N. Epidemiological study on trichinellosis in pigs and man in Upper Egypt. Assiut Vet. Med. J. 2010, 56, 280–287. [Google Scholar]
  41. Dyab, A.K.; Ahmed, M.A.; Abdelazeem, A.G. Prevalence and histopathology of Trichinella spiralis larvae of slaughtered pigs in Cairo governorate, Egypt. J. Egypt. Soc. Parasitol. 2019, 49, 439–442. [Google Scholar] [CrossRef]
  42. Azab, M.E.; Morsy, T.A.; Abdel-Aal, T.M.; Safar, E.H.; Makaram, S.S.; El Hady, H.M.; Kamel, A.A. Current prevalence of trichinosis in pigs in Egypt. J. Egypt. Soc. Parasitol. 1988, 18, 383–389. [Google Scholar] [PubMed]
  43. OIE/World Organisation for Animal Health. Trichinellosis (Infection with Trichinella spp.), Chapter 2.1.20 Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, World Organization for Animal Health. 2017. Available online: https://www.oie.int/eng/normes/mmanual/A_00013.htm (accessed on 13 June 2023).
  44. Fereig, R.M.; Abdelbaky, H.H.; El-Alfy, E.S.; El-Diasty, M.; Elsayed, A.; Mahmoud, H.Y.; Ali, A.O.; Ahmed, A.; Mossaad, E.; Alsayeqh, A.F.; et al. Seroprevalence of Toxoplasma gondii and Neospora caninum in camels recently imported to Egypt from Sudan and a global systematic review. Front. Cell. Infect. Microbiol. 2022, 12, 1042279. [Google Scholar] [CrossRef] [PubMed]
  45. Fereig, R.M.; Wareth, G.; Abdelbaky, H.H.; Mazeed, A.M.; El-Diasty, M.; Abdelkhalek, A.; Mahmoud, H.Y.; Ali, A.O.; El-Tayeb, A.; Alsayeqh, A.F.; et al. Seroprevalence of specific antibodies to Toxoplasma gondii, Neospora caninum, and Brucella spp. in sheep and goats in Egypt. Animals 2022, 12, 3327. [Google Scholar] [CrossRef]
  46. Montoya, J.G. Laboratory diagnosis of Toxoplasma gondii infection and toxoplasmosis. J. Infect. Dis. 2002, 185, S73–S82. [Google Scholar] [CrossRef]
  47. de Barros, R.A.M.; Torrecilhas, A.C.; Marciano, M.A.M.; Mazuz, M.L.; Pereira-Chioccola, V.L.; Fux, B. Toxoplasmosis in human and animals around the world. Diagnosis and perspectives in the one health approach. Acta Trop. 2022, 231, 106432. [Google Scholar] [CrossRef]
  48. Rostami, A.; Karanis, P.; Fallahi, S. Advances in serological, imaging techniques and molecular diagnosis of Toxoplasma gondii infection. Infection 2018, 46, 303–315. [Google Scholar] [CrossRef]
  49. Salama, D.B.; Fereig, R.M.; Abdelbaky, H.H.; Shahat, M.S.; Arafa, W.M.; Aboelhadid, S.M.; Mohamed, A.E.; Metwally, S.; Abas, O.; Suo, X.; et al. Toxoplasma gondii and Neospora caninum antibodies in dogs and cats from Egypt and risk factor analysis. Pathogens 2022, 11, 1464. [Google Scholar] [CrossRef]
  50. Metwally, S.; Hamada, R.; Sobhy, K.; Frey, C.F.; Fereig, R.M. Seroprevalence and risk factors analysis of Neospora caninum and Toxoplasma gondii in cattle of Beheira, Egypt. Front. Vet. Sci. 2023, 10, 1122092. [Google Scholar] [CrossRef] [PubMed]
  51. Gerges, A.A.; MONA, S.; Fathi, A.; Mohamed, H.; Abou-gazia, K.H.A.; Mohamed, H.F. Detection of Neospora caninum and Coxiella burnetii antibodies in milk and serum of infected dairy cattle. Assiut Vet. Med. J. 2018, 64, 49–57. [Google Scholar]
  52. El-Mohamady, R.S.; Gerges, A.M.; Abd-Elhafeiz, Y.G.M. Investigation of the association between bovine viral diarrhea virus and Neospora caninum as a cause of abortion in cattle. J. Applied Vet. Sci. 2022, 7, 11–17. [Google Scholar] [CrossRef]
  53. Selim, A.; Abdelhady, A. Neosporosis among Egyptian camels and its associated risk factors. Trop. Anim. Health Prod. 2020, 52, 3381–3385. [Google Scholar] [CrossRef] [PubMed]
  54. Bartova, E.; Sedlak, K. Seroprevalence of Toxoplasma gondii and Neospora caninum in slaughtered pigs in the Czech Republic. Parasitology 2011, 138, 1369–1371. [Google Scholar] [CrossRef]
  55. Lopes, L.M.; Minervino, A.H.H.; Monger, S.D.G.B.; Soares, H.S.; Portela, J.M.; Ferreira, J.I.G.D.S.; Gennari, S.M.; Pereira, W.L.A. Occurrence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in pigs in the State of Pará, Brazil. Rev. Bras. Parasitol. Vet. 2021, 30, e017520. [Google Scholar] [CrossRef]
  56. Villa, L.; Gazzonis, A.L.; Allievi, C.; Zanzani, S.A.; Mortarino, M.; Manfredi, M.T. Prevalence of Neospora caninum antibodies in fattening pigs and sows from intensive farms in northern Italy. Parasitol. Res. 2022, 121, 1033–1040. [Google Scholar] [CrossRef]
  57. Qi, T.; Ai, J.; Yang, J.; Zhu, H.; Zhou, Y.; Zhu, Y.; Zhang, H.; Qin, Q.; Kang, M.; Sun, Y.; et al. Seroepidemiology of Neosporosis in various animals in the Qinghai-Tibetan Plateau. Front. Vet. Sci. 2022, 9, 953380. [Google Scholar] [CrossRef]
  58. Dubey, J.P.; Romand, S.; Hilali, M.; Kwok, O.C.H.; Thulliez, P. Seroprevalence of antibodies to Neospora caniuum and Toxoplasma gondii in water buffaloes (Bubalus bubalis) from Egypt. Int. J. Parasitol. 1998, 28, 527–529. [Google Scholar] [CrossRef]
  59. Hilali, M.; Romand, S.; Thulliez, P.; Kwok, O.C.H.; Dubey, J.P. Prevalence of Neospora caninum and Toxoplasma gondii antibodies in sera from camels from Egypt. Vet. Parasitol. 1998, 75, 269–271. [Google Scholar] [CrossRef]
  60. Ibrahim, H.M.; Huang, P.; Salem, T.A.; Talaat, R.M.; Nasr, M.I.; Xuan, X.; Nishikawa, Y. Prevalence of Neospora caninum and Toxoplasma gondii antibodies in Northern Egypt. Am. J. Trop. Med. Hyg. 2009, 80, 263–267. [Google Scholar] [CrossRef] [PubMed]
  61. Fereig, R.M.; AbouLaila, M.R.; Mohamed, S.G.; Mahmoud, H.Y.; Ali, A.O.; Ali, A.F.; Hilali, M.; Zaid, A.; Mohamed, A.E.A.; Nishikawa, Y. Serological detection and epidemiology of Neospora caninum and Cryptosporidium parvum antibodies in cattle in southern Egypt. Acta Trop. 2016, 162, 206–211. [Google Scholar] [CrossRef] [PubMed]
  62. Ibrahim, H.M.; Abdel-Rahman, A.A.; Bishr, N.M. Seroprevalence of Neospora caninum and Toxoplasma gondii IgG and IgM antibodies among buffaloes and cattle from Menoufia Province, Egypt. J. Parasit. Dis. 2021, 45, 952–958. [Google Scholar] [CrossRef] [PubMed]
  63. Selim, A.; Khater, H.; Almohammed, H.I. A recent update about seroprevalence of ovine neosporosis in Northern Egypt and its associated risk factors. Sci. Rep. 2021, 11, 14043. [Google Scholar] [CrossRef]
  64. Abbas, I.; Al-Araby, M.; Elmishmishy, B.; El-Alfy, E.S. Gastrointestinal parasites of cats in Egypt: High prevalence high zoonotic risk. BMC Vet. Res. 2022, 18, 420. [Google Scholar] [CrossRef]
  65. 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. [Google Scholar] [CrossRef]
  66. Ramadan, M.Y.; Abou-EL-Roos, M.E.A.; El-Madawy, R.S. An approach for detection of Neospora caninum infection in aborted bovine fetuses in Egypt. Benha Vet. Med. J. 2009, Feb., 266–281. [Google Scholar]
  67. Gazzonis, A.L.; Garcia, G.A.; Zanzani, S.A.; Mora, L.M.O.; Invernizzi, A.; Manfred, M.T. Neospora caninum infection in sheep and goats from north-eastern Italy and associated risk factors. Small Rumin. Res. 2016, 140, 7–12. [Google Scholar] [CrossRef]
  68. Udonsom, R.; Supanta, J.; Tanglakmankhong, O.; Ngoenphisutsin, K.; Nishikawa, Y.; Fereig, R.M.; Jirapattharasate, C. Toxoplasma gondii and Neospora caninum prevalence and risk factors on goat farms in Kanchanaburi province, Thailand. Vet. Integr. Sci. 2021, 19, 65–74. [Google Scholar] [CrossRef]
  69. Quintanilla-Gozalo, A.; Pereira-Bueno, J.; Tabares, E.; Innes, E.A.; González-Paniello, R.; Ortega-Mora, L.M. Seroprevalence of Neospora caninum infection in dairy and beef cattle in Spain. Int. J. Parasitol. 1999, 29, 1201–1208. [Google Scholar] [CrossRef]
  70. Pozio, E. Searching for Trichinella: Not all pigs are created equal. Trends Parasitol. 2014, 30, 4–11. [Google Scholar] [CrossRef] [PubMed]
  71. Murrell, K.D. The dynamics of Trichinella spiralis epidemiology: Out to pasture? Vet. Parasitol. 2016, 231, 92–96. [Google Scholar] [CrossRef] [PubMed]
  72. Gamble, H.R.; Bessonov, A.S.; Cuperlovic, K.; Gajadhar, A.A.; Van Knapen, F.; Noeckler, K.; Schenone, H.; Zhu, X. International Commission on Trichinellosis: Recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Vet. Parasitol. 2000, 93, 393–408. [Google Scholar] [CrossRef] [PubMed]
  73. Van Knapen, F. Control of trichinellosis by inspection and farm management practices. Vet. Parasitol. 2000, 93, 385–392. [Google Scholar] [CrossRef] [PubMed]
  74. Alban, L.; Petersen, J.V. Ensuring a negligible risk of Trichinella in pig farming from a control perspective. Vet. Parasitol. 2016, 231, 137–144. [Google Scholar] [CrossRef] [PubMed]
  75. Eslahi, A.V.; KarimiPourSaryazdi, A.; Olfatifar, M.; de Carvalho, L.M.M.; Foroutan, M.; Karim, M.R.; Badri, M.; Ketzis, J.K. Global prevalence of Trichinella in pigs: A systematic review and meta-analysis. Vet. Med. Sci. 2022, 8, 2466–2481. [Google Scholar] [CrossRef]
  76. Therizol, M.; Levy, R.; Coulbois, J.; Brochard, C.; Berque, A.; Betourne, C. Trichinose aigue. A propos de quelques cas récents importés d’Egypte. Bull. Soc. Pathol. Exot. 1975, 68, 407–415. [Google Scholar]
  77. Antonios, S.N.; Salem, S.A. A case report of human trichinosis in Tanta. J. Egypt. Soc. Parasitol. 1989, 19, 363–364. [Google Scholar]
  78. Pozio, E. World distribution of Trichinella spp. infections in animals and humans. Vet. Parasitol. 2007, 149, 3–21. [Google Scholar] [CrossRef]
  79. Gamble, H.R.; Anderson, W.R.; Graham, C.E.; Murrell, K.D. Diagnosis of swine trichinosis by enzyme-linked immunosorbent assay (ELISA) using an excretory—secretory antigen. Vet. Parasitol. 1983, 13, 349–361. [Google Scholar] [CrossRef]
  80. Nöckler, K.; Serrano, F.J.; Boireau, P.; Kapel, C.M.O.; Pozio, E. Experimental studies in pigs on Trichinella detection in different diagnostic matrices. Vet. Parasitol. 2005, 132, 85–90. [Google Scholar] [CrossRef] [PubMed]
  81. Kapel, C.M.O.; Gamble, H.R. Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. Int. J. Parasitol. 2000, 30, 215–221. [Google Scholar] [CrossRef] [PubMed]
  82. Kapel, C.M. Sylvatic and domestic Trichinella spp. in wild boars; infectivity, muscle larvae distribution, and antibody response. J. Parasitol. 2001, 87, 309–314. [Google Scholar] [CrossRef] [PubMed]
  83. Pozio, E.; Merialdi, G.; Licata, E.; Della Casa, G.; Fabiani, M.; Amati, M.; Cherchi, S.; Ramini, M.; Faeti, V.; Interisano, M.; et al. Differences in larval survival and IgG response patterns in long-lasting infections by Trichinella spiralis, Trichinella britovi and Trichinella pseudospiralis in pigs. Parasites Vectors 2020, 13, 520. [Google Scholar] [CrossRef]
  84. Thi, N.V.; Dorny, P.; La Rosa, G.; Long, T.T.; Van, C.N.; Pozio, E. High prevalence of anti-Trichinella IgG in domestic pigs of the Son La province, Vietnam. Vet. Parasitol. 2010, 168, 136–140. [Google Scholar] [CrossRef]
Vetsci 10 00675 g001
Figure 1. Geographical locations of sample origins. Serum samples were collected from pigs during slaughtering in the El-Bassatin abattoir, Cairo. These animals originated from three main slums of pig raising in three parts of Cairo, the capital governorate of Egypt: Ezbet El Nakhl (eastern Cairo), Manshiyat Naser (western Cairo), and 15 May city (southern Cairo).
Figure 1. Geographical locations of sample origins. Serum samples were collected from pigs during slaughtering in the El-Bassatin abattoir, Cairo. These animals originated from three main slums of pig raising in three parts of Cairo, the capital governorate of Egypt: Ezbet El Nakhl (eastern Cairo), Manshiyat Naser (western Cairo), and 15 May city (southern Cairo).
Vetsci 10 00675 g001
Table 1. Commercially available ELISA test kits used for detecting antibodies against T. gondii, N. caninum, and Trichinella species #.
Table 1. Commercially available ELISA test kits used for detecting antibodies against T. gondii, N. caninum, and Trichinella species #.
Infectious AgentELISA Test Kit $AntigenSerum DilutionConjugate Sensitivity *Specificity *
Toxoplasma gondiiID Screen® Toxoplasmosis Indirect MultispeciesP30 antigen1:10Anti-multi-species IgG-HRP98.36% (95% CI: 95.29–99.44) 99.42% (95% CI: 98.8–100)
Neospora caninumID Screen® Neospora caninum competition MultispeciesPurified extract of Neospora caninum1:2Anti-N. caninum-HRP
(detects IgG or IgM)		100% (95% CI: 98.8–100) 100% (95% CI: 99.63–100)
Trichinella speciesID Screen® Trichinella Indirect MultispeciesTrichinella E/S antigen1:20Anti-multi-species-HRP (detects IgG or IgM)90.7% (95% CI: 89.1–92.4)100% (95% CI: 98.95–100)
$ All ELISA kits were manufactured by ID.vet Innovative Diagnostics, Grabels, France. * The sensitivity and specificity of the diagnostic kits were provided by the manufacturer of the kits. # detects antibodies to T. spiralis, T. pseudospiralis, T. britovi and T. nativa.
Table 2. Seroprevalence of T. gondii, N. caninum, Trichinella spp. and mixed infections in pigs from Egypt.
Table 2. Seroprevalence of T. gondii, N. caninum, Trichinella spp. and mixed infections in pigs from Egypt.
Type of Infection No. TestedNo. Negative (%)No. Doubtful (%)No. Positive (%)95% CI *
T. gondii332152 (45.8)28 (8.4)152 (45.8)40.4–51.3
N. caninum332217 (65.4)22 (6.6)93 (28.0)23.3–33.2
Trichinella spp.332327 (98.5)1 (0.3)4 (1.2)0.4–3.3
T. gondii + N. caninum332251 (75.6)19 (5.7)62 (18.7)14.7–23.4
* 95% CI calculated according to the method described by http://vassarstats.net/, accessed on 22 July 2023.
Table 3. Risk factors for T. gondii antibodies in pigs, Cairo, Egypt.
Table 3. Risk factors for T. gondii antibodies in pigs, Cairo, Egypt.
Analyzed FactorNo. TestedNo. Negative (%) No. Positive (%)OR (95% CI) *p-Value #
Sex
Female200105 (52.5)95 (47.5)Ref. Ref.
Male13275 (56.8)57 (43.2)0.8 (0.5–1.3)0.499
Breeding place
Ezbet El Nakhl184119 (64.7)65 (35.3)3.8 (1.8–7.9)0.0003
Manshiyat Naser10848 (44.4)60 (55.6)0.6 (0.3–1.3)0.259
15 May city4013 (32.5)27 (67.5)Ref.Ref.
* Odds ratio and 95% confidence interval calculated by http://vassarstats.net/ (accessed on 22 July 2023). # p value was evaluated by Fisher’s exact test using online statistics software http://vassarstats.net/ (accessed on 22 July 2023) and GraphPad Prism version 5. Ref. is the value used as a reference.
Table 4. Risk factors for N. caninum antibodies in pigs, Cairo, Egypt.
Table 4. Risk factors for N. caninum antibodies in pigs, Cairo, Egypt.
Analyzed FactorNo. of TestedNo. of Negative (%) No. of Positive (%)OR (95% CI) *p-Value #
Sex
Female200124 (62)76 (38)Ref Ref
Male132115 (87.1)17 (12.9)4.1 (2.3–7.4)<0.0001
Breeding place
Ezbet El Nakhl184160 (87)24 (13)Ref. Ref.
Manshiyat Naser10850 (46.3)58 (53.7)7.7 (4.4–13.7)<0.0001
15 May city4029 (72.5)11 (27.5)2.5 (1.1–5.7)0.031
* Odds ratio and 95% confidence interval calculated by http://vassarstats.net/ (accessed on 22 July 2023). # p value was evaluated by Fisher’s exact test using online statistics software http://vassarstats.net/ (accessed on 22 July 2023) and GraphPad Prism version 5. Ref. is the value used as a reference.
Table 5. Seroprevalence of N. caninum antibodies in animals in Egypt.
Table 5. Seroprevalence of N. caninum antibodies in animals in Egypt.
AnimalsLocationStudy YearNo. TestedNo. Positive (%)Diagnostic MethodHistoryReference
BuffaloesCairo slaughterhouse19957551 (68)NATNS[58]
CamelsCairo slaughterhouse19951616 (3.7)NATNS[59]
CattleSharkiaNS9319 (20.43)ELISANS[60]
CattleQena and Sohag2014–201530157 (18.9)ELISANS[61]
CattleFayoum, Giza, Beni-Swief, and Menia201710029 (29) 1ELISAInfertility and abortion[51]
CamelsRed Sea, Qalyubia, Kafr, and El Sheikh2018–201928231 (11)ELISA150 camels had a history of abortion[53]
CattleMenoufia2017–201826232 (12.21) 1
39 (14.89) 2
3 (1.5) 3		ELISANS[62]
Buffaloes24417 (6.97) 1
33(13.52) 2
12 (4.92) 3
SheepAlexandria, Gharbia, Menofia, and Qalyubia2017–201843037 (8.6)ELISANS[63]
CattleGiza, El Fayoum, and Beni Suef 11635 (30.17)ELISAAborted bovine fetuses[52]
CamelsAswan2018–202146018 (3.9)ELISANS[44]
Sheep and GoatsDakahlia, Beni Suef, Qena, and Red Sea2016–2021239
121		37 (15.5)
6 (5)		ELISANS[45]
Dogs and CatsVariable2019–2022172
51		10 (5.8)
2 (3.9)		ELISA-[49]
CattleBeheira 35888 (24.6)ELISANS[50]
1 IgM-ELISA positive, 2 IgG-ELISA positive, 3 mixed IgM, IgG-ELISA positive. Abbreviations: ELISA, enzyme-linked immunosorbent assay; NAT, neospora agglutination test; NS, not stated.
Table 6. Prevalence of Trichinella sp. larvae in pigs in Egypt.
Table 6. Prevalence of Trichinella sp. larvae in pigs in Egypt.
Sample TypesGovernoratesStudy YearNo. TestedNo. Positive (%)Diagnostic MethodsSpeciesReference
pork sausageAlexandriaNS1006 (6)
4 (4)		Trichinoscope
Digestion method		T. spiralis[38]
abattoir meatAssiut and Sohag2006–20071506 (4)
5 (3.33)		Trichinoscope
Digestion methods		T. spiralis[40]
abattoir meatEl-Minia2014–20151000Muscle squash and digestion methods-[19]
abattoir meatCairo2018–20191842 (1.08)Trichinoscopic and histopathological examinationT. spiralis[41]
abattoir inspectionCairo202033,812 *359 (1.06)Trichinoscopic examinationTrichinella sp.[35]
abattoir meatCairo20201706 (3.35)
4 (2.35)		Digestion methods
Trichinoscope		T. spiralis#[35]
* Data were collected through a standard form from the Al-Basateen abattoir archives. # Trichinella spiralis was identified based on PCR of the GAPDH gene.
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Fereig, R.M.; El-Alfy, E.-S.; Abdelbaky, H.H.; Abdel-Hamid, N.H.; Mazeed, A.M.; Menshawy, A.M.S.; Kelany, M.A.; El-Diasty, M.; Alawfi, B.S.; Frey, C.F. Seroprevalence of Toxoplasma gondii, Neospora caninum and Trichinella spp. in Pigs from Cairo, Egypt. Vet. Sci. 2023, 10, 675. https://doi.org/10.3390/vetsci10120675

AMA Style

Fereig RM, El-Alfy E-S, Abdelbaky HH, Abdel-Hamid NH, Mazeed AM, Menshawy AMS, Kelany MA, El-Diasty M, Alawfi BS, Frey CF. Seroprevalence of Toxoplasma gondii, Neospora caninum and Trichinella spp. in Pigs from Cairo, Egypt. Veterinary Sciences. 2023; 10(12):675. https://doi.org/10.3390/vetsci10120675

Chicago/Turabian Style

Fereig, Ragab M., El-Sayed El-Alfy, Hanan H. Abdelbaky, Nour H. Abdel-Hamid, Amira M. Mazeed, Ahmed M. S. Menshawy, Mohamed A. Kelany, Mohamed El-Diasty, Bader S. Alawfi, and Caroline F. Frey. 2023. "Seroprevalence of Toxoplasma gondii, Neospora caninum and Trichinella spp. in Pigs from Cairo, Egypt" Veterinary Sciences 10, no. 12: 675. https://doi.org/10.3390/vetsci10120675

APA Style

Fereig, R. M., El-Alfy, E. -S., Abdelbaky, H. H., Abdel-Hamid, N. H., Mazeed, A. M., Menshawy, A. M. S., Kelany, M. A., El-Diasty, M., Alawfi, B. S., & Frey, C. F. (2023). Seroprevalence of Toxoplasma gondii, Neospora caninum and Trichinella spp. in Pigs from Cairo, Egypt. Veterinary Sciences, 10(12), 675. https://doi.org/10.3390/vetsci10120675

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