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. 2021 Apr 15;45(4):952–958. doi: 10.1007/s12639-021-01386-x

Seroprevalence of Neospora caninum and Toxoplasma gondii IgG and IgM antibodies among buffaloes and cattle from Menoufia Province, Egypt

Hany M Ibrahim 1,✉, Adel A H Abdel-Rahman 2,✉, Nora M Bishr 2
PMCID: PMC8556423  PMID: 34789977

Abstract

The main reasons behind performing the current study were the high distribution of the water buffaloes Bubalus bubalis and cattle in Menoufia province, the veterinary importance of Neospora caninum and Toxoplasma gondii and the limited information on the seropositivity of these parasites in Menoufia province, Egypt. Therefore, the current study was conducted to estimate the distribution of anti-N. caninum and anti-T. gondii antibodies (IgM and IgG) in water buffaloes and cattle from Menoufia province. ELISA methods based on the surface antigen 1 of N. caninum (NcSAG1t) and the surface antigen 2 of T. gondii (TgSAG2t) were utilized to detect both specific IgM and IgG for these parasites. The overall seroprevalence of N. caninum and T. gondii in cattle of Menoufia Province were (12.21% and 1.91% for IgM) and (14.89% and 3.05% for IgG), respectively. In water buffaloes, seroprevalences of N. caninum and T. gondii were (6.97% and 9.02% for IgM) and (13.52% and 8.2% for IgG), respectively. The mixed infection rate was 1.5% in cattle and 4.92% in buffaloes. No significant differences were detected regarding age or gender. Statistically significant changes in the prevalence of both parasites were demonstrated in relation to a period of the year. In conclusion, seroprevalence of neosporosis was more than toxoplasmosis in cattle and buffaloes in Menoufia Province, Egypt.

Keywords: Diagnosis, Toxoplasmosis, Neosporosis, Cattle, Water buffalo, Menoufia

Introduction

Neospora caninum and Toxoplasma gondii are related coccidian protozoan parasites capable of infecting a variety of warm-blooded animals, including cattle and water buffaloes (Lindsay and Dubey 2020). Cats and dogs (definitive hosts) shed T. gondii and N. caninum oocysts, respectively, in their feces resulting in wide-ranging environmental contamination (De Marez et al. 1999; Hill and Dubey 2002). In the hosts, another route of the infection is vertical transmission of T. gondii and N. caninum between mother and its fetus (Schares et al. 1998; Fricker-Hidalgo et al. 2013). Tissue cysts of both parasites are commonly seen in different meat-producing animals (Tenter et al. 2000; Dubey 2003). Therefore, ingestion of raw or poorly-cooked meat by carnivorous animals or humans is representing a potential hazard. While toxoplasmosis is considered as a zoonotic disease, neosporosis is suggested to be a potential zoonotic disease since anti-N. caninum antibodies are detected in humans (Lobato et al. 2006; Ibrahim et al. 2009).

In cattle and water buffaloes, N. caninum can affect animal productivity (Chryssafidis et al. 2011), resulting in reproductive losses such as abortions and neonatal mortality (Dubey et al. 2007; Chryssafidis et al. 2015). Moreover, viable T. gondii was isolated from naturally infected aborted bovine fetuses (Canada et al. 2002). Cattle and water buffaloes are the main source of red meat in Egyptian markets (Alboghdady and Alashry 2010). The Egyptian bovine sector is well-integrated with crop-land since the country has limited natural pastures. In Egypt, cattle and buffalo are well-distributed in the Delta and around the River Nile. As one of the Delta provinces, Menoufia province occupied the second rank in the water buffalo and cattle distribution in Lower Egypt (FAO 2018).

Both apicomplexan parasites are prevalent in Egypt. Previous studies from Egypt demonstrated anti-T. gondii and N. caninum antibodies in asymptomatic pregnant women (Ibrahim et al. 2009; Kamal et al. 2015; El-shqanqery et al. 2017), chickens (Ibrahim 2013; Ibrahim et al. 2016), sheep (Ibrahim 2016; Ibrahim et al. 2017), camels (Hilali et al. 1998; Ahmed et al. 2017), bovines (Dubey et al. 1998; Ibrahim et al. 2009), ducks and pigeons (AbouLaila et al. 2011; Ibrahim 2016; Ibrahim et al. 2018).

Enzyme linked immunosorbent assay (ELISA) is characterized by its reproducible and quantifiable data. A highly specific and sensitive ELISA based on TgSAG2 was previously described (Ibrahim et al. 2009, 2017, 2018). Several bovine surveys have proved that NcSAG1 is an important candidate antigen to detect specific N. caninum antibodies during acute and chronic infections (Chahan et al. 2003; Wilkovsky et al. 2011; Takashima et al. 2013; Ichikawa-seki et al. 2016; Pagmadulam et al. 2018). Therefore, the objective of the current study was carried out to investigate the distribution of Neospora caninum and Toxoplasma gondii IgM and IgG antibody seropositivity among cattle, and water buffaloes in Menoufia province using ELISAs based on the recombinant antigens TgSAG2 and NcSAG1.

Materials and methods

Serum samples

From June 2017 to May, 2018, a total 506 blood samples from cattle (262) and water buffaloes (244) were collected from open public markets in Qewaisna and Birket Al Saba, Menoufia Province, Egypt (Fig. 1). The cattle and buffaloes are usually kept in farmer's stables in the evening and used in the fields in the daytime. Cattle from 1 month to 8 years old were divided into two groups based on their age; young (2 years or less) and aged (more than 2 years). Buffaloes from 1 month to 10 years old were divided into two groups based on their age; young (3 years or less) and aged (more than 3 years). Blood samples were collected from the jugular or the caudal vein by local veterinary practitioners. Then the samples were incubated at room temperature for 1 h, and centrifuged at 3000 rpm for 15 min. Sera were collected, aliquoted and stored at − 20 °C until use.

Fig. 1.

Fig. 1

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Map of Menoufia Province sampling sites

Serology

In the current study, purified recombinant proteins of NcSAG1 and TgSAG2 fused with glutathione S transferase (GST) were prepared and utilized for detection of N. caninum and T. gondii specific (IgG and IgM) antibodies by ELISA (Ibrahim et al. 2009). Horseradish peroxidase (HRP)-conjugated anti-bovine IgG (Bethyl Laboratories, Montgomery, TX, USA) and HRP-conjugated anti-bovine IgM (Chongqing Biospes Co., China) were used as secondary antibodies. Absorbance values of each reaction were measured at 405 nm using a micro-plate reader (Seac, Radim Company, Italy). The ELISA results for recombinant antigens (TgSAG2 or NcSAG1) were subtracted from those of GST protein. The cut-off points were calculated as the OD405 value for N. caninum or T. gondii negative sera plus 3 standard deviations (Ibrahim et al. 2009) (n = 20); for IgG; TgSAG2: 0.015 and NcSAG1: 0.018 in cattle, TgSAG2: 0.018 and NcSAG1: 0.018 in buffaloes, for IgM; TgSAG2: 0.018 and NcSAG1: 0.018 in cattle, TgSAG2: 0.019 and NcSAG1: 0.020 in buffaloes. The Standard negative sera from our sera stock were tested and confirmed negative were used to calculate the cut off values.

Statistical analysis

The logistic regression test was used to evaluate significant differences (P < 0.05) of infection rate in animals of a different location, age, sex, and season using SPSS version 11.

Results

The seroprevalence of T. gondii and N. caninum in cattle from Qewaisna and Birket Al Saba regions of Menoufia Province, Egypt were summarized in Table 1. The overall prevalence of T. gondii in Menoufia Province was 1.91% and 3.05% for acute infection (IgM) and chronic infection (IgG), respectively. T. gondii seropositivity for IgM and/or IgG antibodies was not significant between Qewaisna and Birket Al Saba areas. Seropositivity of N. caninum for IgM and IgG antibodies was 12.21% and 14.89% respectively, with a significant (P < 0.05) increase in the IgM level in the area of Qewaisna (16.11%) compared to Birket Al Saba (7.08%) area. A mixed infection of T. gondii and N. caninum was (1.5%) in the cattle sera from Menoufia Province.

Table 1.

Seroprevalence of Toxoplasma gondii and Neospora caninum infections in cattle from Menoufia province

Regions Total T. gondii N. caninum Mixed
IgM IgG IgM IgG
Qewaisna 149 2 (1.34%) 6 (4.03%) 24 (16.11%) 24 (16.11%) 2 (1.34%)
Birket Al Saba 113 3 (2.65%) 2 (1.77%) 8 (7.08%)* 15 (13.27%) 1 (0.88%)
Total 262 5 (1.91%) 8 (3.05%) 32 (12.21%) 39 (14.89%) 3 (1.5%)
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Data are expressed as: number of animal (%).

*Indicates that prevalence is significantly different (P < 0.05)

In buffaloes from Menoufia Province, the overall seroprevalence of T. gondii was 9.02% and 8.2% for IgM and IgG, respectively. While the overall seroprevalence of N. caninum was 6.97% and 13.52% respectively. Both parasites seropositivity for IgM antibodies was significantly (P < 0.05) increased in the area of Birket Al Saba compared to Qewaisna area. The mixed infection of T. gondii and N. caninum was 4.92% in the buffalo sera from Menoufia Province. Although the mixed infection is higher in Birket Al Saba area compared to Qewaisna area, but the difference was non-significant (Table 2).

Table 2.

Seroprevalence of Toxoplasma gondii and Neospora caninum infections in water buffaloes from Menoufia province

Regions Total T. gondii N. caninum Mixed
IgM IgG IgM IgG
Qewaisna 135 6 (4.44%) 9 (6.66%) 0 (0%) 20 (14.81%) 4 (2.96%)
Birket Al Saba 109 17 (15.6%)* 11(10.09%) 17(15.6%)* 13(11.93%) 8 (7.34%)
Total 244 22 (9.02%) 20 (8.20%) 17 (6.97%) 33(13.52%) 12 (4.92%)
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Data are expressed as: number of animal (%).

*Indicates that prevalence is significantly different (P < 0.05)

During chronic infection, the percentages of infection of both parasites in aged animals (cattle and water buffaloes) were higher than those in the young ones without any significant difference. Moreover, during acute infection in cattle, only the percentage of N. caninum infection was higher in aged animals (14.29%) than that of the young animals (9.57%) (Table 3). In contrast, in the water buffaloes, IgM positive samples for T. gondii were higher in younger animals (10.23%) than the aged ones (8.97%) without any significant difference (Table 4). Gender-wise, no significant differences were detected in infection percentages of both parasites. In female buffaloes, the prevalence (8.55%) and (13.68%) was demonstrated only during the chronic infection of T. gondii and N. caninum, respectively (Table 4). In female cattle, the prevalence (3.45%) was demonstrated during the chronic infection of T. gondii (Table 3).

Table 3.

Seroprevalence of Toxoplasma gondii and Neospora caninum infections in cattle according to gender, season and age

Characteristics Total T. gondii N. caninum
IgM IgG IgM IgG
Age
2 years or less 115 2 (1.74%) 1 (0.65%) 11 (9.57%) 18 (11.61%)
More than 2 years 147 3 (2.04%) 7 (4.76%) 21(14.29%) 21 (14.29%)
Gender
Male 30 1 (3.33%) 0 3 (10.00%) 5 (16.66%)
Female 232 4 (1.72%) 8 (3.45%) 29 (12.5%) 34 (14.66%)
Season
Spring 75 3 (4.00%) 2 (2.66%) 8 (10.67%) 6 (8.00%)
Summer 42 0 3 (7.14%) 3 (7.14%) 10 (23.81%)*
Autumn 69 0 1 (1.45%) 13 (18.84%) 12 (17.39%)
Winter 76 2 (2.63%) 2 (2.63%) 8 (10.53%) 11 (14.47%)
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Data are expressed as: number of animal (%).

*Indicates that prevalence is significantly different against the spring season (P < 0.05)

Table 4.

Seroprevalence of Toxoplasma gondii and Neospora caninum infections in water buffaloes according to gender, season and age

Characteristics Total T. gondii N. caninum
IgM IgG IgM IgG
Age
3 years or less 88 9 (10.23%) 5 (5.68%) 3 (3.41%) 11 (12.5%)
More than 3 years 156 14 (8.97%) 15 (9.62%) 14(8.97%) 22 (14.10%)
Gender
Male 10 2 (20.00%) 0 2 (20.00%) 0
Female 234 21 (8.97%) 20 (8.55%) 16 (6.84%) 32 (13.68%)
Season
Spring 33 4 (12.12%) 1 (3.03%) 2 (6.06%) 2 (6.06%)
Summer 40 2 (5.00%) 4 (10.00%) 0 8 (20.00%)
Autumn 101 4 (3.96%) 6 (5.95%) 1 (0.99%) 13 (12.87%)
Winter 70 13 (18.57%)* 9 (12.86%) 14(20.00%)* 10 (14.29%)
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Data are expressed as: number of animal (%).

*Indicates that prevalence is significantly different against the summer or autumn seasons (P < 0.05)

According to the season, no significant changes were demonstrated during acute infection of both parasites in cattle. During spring, the prevalence (8%) was significantly (P < 0.05) reduced compared to the summer season, (23.81%) in cattle during the chronic infection of N. caninum (Table 3). The prevalence of T. gondii and N. caninum showed significant (P < 0.05) increase during the winter season when compared to the summer or the autumn seasons during the acute infection in water buffaloes (Table 4).

Discussion

Among the livestock sector, cattle and water buffaloes play a major role in the economy of Egypt because meat and milk products derived from these livestock are daily consumed in the Egyptian markets mainly in the delta of Egypt and Menoufia Province. Although N. caninum or T. gondii infection are manifested as stillbirth and abortion in adult animals and neurological symptoms in calves, only limited data is available on the prevalence of these protozoan parasites in Menoufia Province. Therefore, in the present study, sera from water buffaloes and cattle from two areas of Menoufia Province were examined for seropositivity to T. gondii and N. caninum.

Detectable seroprevalence of N. caninum and T. gondii in cattle and water buffaloes of Menoufia Province was demonstrated in the current study. The mixed infection rates were 1.5% and 4.92%, among the cattle and water buffaloes, respectively. The significant elevation in the level of the seropositivity for IgM antibodies among areas indicates the high frequency of the recent infection of these parasites in Menoufia Province. In cattle (n = 93) of neighboring Sharkia Province, one of the Egypt delta Provinces, 20.43% anti- N. caninum and 10.75% anti- T. gondii antibodies were detected (Ibrahim et al. 2009). In southern Provinces (Qena and Sohag) of Egypt, the prevalence of N. caninum and T. gondii in cattle (n = 301) were 18.9% and 23.6%, respectively (Fereig et al. 2016a; 2016b). While only one previous survey reported that 68% anti- N. caninum and 1.3% anti- T. gondii antibodies were found in sera in water buffalo (n = 75) from Cairo Province the capital of Egypt (Dubey et al. 1998).

The high prevalence of N. caninum and T. gondii infection in cattle and water buffaloes not only affects the development of the livestock industry but is also an important infectious source of human toxoplasmosis. In general, the possible routes by which the hosts become infected with N. caninum or T. gondii could be (1) ingestion of bradyzoite cysts in the tissues of intermediate hosts (including cattle and water buffaloes), (2) ingestion of sporulated oocysts, or (3) vertical transmission (Dubey and Beattie 1988). In Egypt, consumption of grilled or undercooked bovine or bubaline meat is frequent and could result in a high infection rate among humans. But the major risk factor associated with the high seropositivity and infection rates among the bovine or bubaline themselves is contact with soil-harboring the indicated parasites oocysts excreted by wild homeless cats and dogs. Birds such as chickens, ducks, and pigeons have been used as important indicators of soil contamination with N. caninum and T. gondii oocyst (Dubey 2010; Ibrahim 2013, 2016; Ibrahim et al. 2018). In Egypt, the soil contamination with these parasites oocysts was previously indicated (Ibrahim 2013, 2016; Ibrahim et al. 2016, 2018). Furthermore, T. gondii has been reported in goats (Fereig et al. 2016b), horses (Ghazy et al. 2007), donkeys (El-Ghaysh 1998), and both T. gondii and N. caninum have been reported in sheep and camels in Egypt (Hilali et al. 1998; Ibrahim 2016; Ibrahim et al. 2017).

We also compared the seropositivity of N. caninum and T. gondii with ages, gender, and periods of the year among the examined cattle and water buffaloes population. Although higher seropositivity was detected in aged animals than young populations, no significant differences were demonstrated in the current study. Several previous reports in cattle suggested that the risk of being seropositive for N. caninum and T. gondii may increase with age (Rinaldi et al. 2005; Lopes et al. 2013; Holec-Gąsior et al. 2013). In the present study, no significant changes were detected among male and female animals. These results were in agreement with previous studies carried out on cattle in Egypt (Fereig et al. 2016a; 2016b). Although studies recorded that the prevalence of these parasites becomes lower in cold weather, the current study showed high N. caninum prevalence among buffaloes during the winter season when compared with the summer or the autumn seasons during the acute infection. On the other hand, during spring the prevalence was significantly reduced compared to the summer season in cattle during the chronic infection of N. caninum. The highest prevalence of N. caninum in water buffaloes from Pakistan was detected in the summer season (Nasir et al. 2011). Dubey et al. (2007) reported that in the area surrounding the cattle populations' high temperature might facilitate faster sporulation of N. caninum oocytes.

In conclusion, our results indicated that neosporosis and toxoplasmosis present the threat of an epidemic in Menoufia Province, with reasonable seropositivity in cattle and buffaloes. The use of ELISA based on recombinant NcSAG1t and TgSAG2t is a suitable diagnostic method to diagnose neosporosis and toxoplasmosis. This is the first report investigating the seroprevalence of N. caninum and T. gondii antibodies in cattle and buffaloes from Menoufia Province, Egypt, using NcSAG1t- and TgSAG2t -based ELISA.

Acknowledgements

The authors would like to thank Prof. Dr. Xuenan Xuan, and Prof. Dr. Yoshifumi Nishikawa (National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido, Japan) for providing the recombinant NcSAG1t and TgSAG2t. The authors also thank local veterinary practitioners for collecting blood samples.

Author contributions

HMI designed the study. NMB and HMI performed the experiments, analyzed and interpreted the data. HMI wrote the first version of the manuscript. HMI, AAHA and NMB assisted during the analysis and interpretation of data and revised the manuscript. All authors reviewed and approved the final version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The animal owners gave consent for collection of samples. This study was performed after getting permission from the Institutional Animal Ethical Committee, Menoufia University, Egypt (approval ID: MUFS/F/IM/2/17).

Footnotes

Publisher's Note

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Contributor Information

Hany M. Ibrahim, Email: hany.mohamed@science.menofia.edu.eg, Email: hanyibrahimeg@gmail.com

Adel A. H. Abdel-Rahman, Email: adelnassar63@yahoo.com

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