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. 2023;24(4):313–319. doi: 10.22099/IJVR.2023.48129.7006

Sarcocystosis among buffaloes from slaughterhouses in Nile Delta, Egypt: morphologic assessment and molecular confirmation

M El-Sayad 1, H El-Taweel 1, A Ahmed 2, N Abd El-Latif 1,*
PMCID: PMC11127730  PMID: 38799287

Abstract

Background:

Sarcocystis species are coccidian protozoan zoonotic parasites of the phylum Apicomplexa. There is a large diversity of Sarcocystis species. Some of them are pathogenic and dangerous to humans, domestic, and wild animals. Cattle are common intermediate hosts. The infection of meat with different species of Sarcocystis can be serious for public health.

Aims:

The current study aimed to determine the prevalence of sarcocystosis in slaughtered buffaloes in Tanta city abattoirs, Nile Delta, Egypt.

Methods:

Morphological and histological examinations and a molecular study were undertaken. A total of 517 locally bred buffaloes were slaughtered in Tanta city, Egypt. Each buffalo carcass was visually inspected for the presence of Sarcocystis macrocysts. Fifty tissue samples containing suspected cysts were examined by using different techniques including histology, transmission electron microscope (TEM), and PCR.

Results:

By visual inspection, the overall prevalence of suspected sarcocystosis was 26.5%. The highest infection rate was detected visually from the esophagus followed by skeletal muscles and diaphragm whereas the least was recorded in the tongue. Histological and TEM examination showed that the cysts were packed with bradyzoites separated by multiple septa. 100% of the sarcocysts diagnosed visually in the esophagus and muscles were confirmed by PCR, compared to only 25% of those detected in the tongue.

Conclusion:

These results highlight the high prevalence of sarcocystosis among buffaloes in Egypt, possibly due to widespread environmental contamination by Sarcocystis oocysts. The use of molecular methods should be encouraged to confirm the identity of the suspected cysts.

Key Words: Buffaloes, Egypt, Molecular, Sarcocystis spp., Ultrastructure

Introduction

Sarcocystis spp. is an intracellular zoonotic protozoan parasite belonging to the phylum Apicomplexa. There is a great Sarcocystis spp. diversity and over 220 species are widely distributed in man and many species of animals (Dubey et al., 2015a).

Sarcocystis spp. are cyst-forming sporozoan parasites with a complex obligatory heteroxenous cycle, involving a carnivore as a definitive host and a herbivore or an omnivore as an intermediate host. Cyst formation takes place in the intermediate hosts whereas sexual development gametogony and sporogony with oocyst formation take place in the definitive host (Dubey et al., 2015a). Sarcocystis spp. oocysts are passed and remain infective in the feces of the definitive host for two years. Intermediate hosts are mainly infected through ingestion of sporocysts (Savini et al., 1992). Vertical transmission was reported experimentally (Marques et al., 2018) and sporadically though rarely in natural infections (Moré et al., 2011).

Some species of Sarcocystis spp. sporocysts are pathogenic and dangerous to humans and domestic and wild animals. Pathogenicity depends on the species, intensity of infection, and localization in the body (Fayer, 2004). Pathogenic Sarcocystis spp. cause disease mainly in their intermediate, not in their definitive hosts (Tenter, 1995). Sarcocystis hominis, Sarcocystis cruzi, and Sarcocystis hirsuta are the main species infecting cattle whereas water buffaloes are intermediate hosts for Sarcocystis fusiformis, Sarcocystis levinei, Sarcocystis dubeyi, Sarcocystis sinensis, and Sarcocystis buffalonis (Lindsay and Dubey, 2020). Classification of Sarcocystis species is based on the shape and thickness of the cyst wall (Choi et al., 2018). Sarcocystis spp. infect skeletal cardiac, and smooth muscles of cattle (Koudela and Modrý, 2000; Fayer et al., 2004; Hu et al., 2011). The prevalence of sarcocystosis in adult bovine muscles may reach 70-100%, in many regions of the world (Choi et al., 2018; Ayazian et al., 2020). They may cause abortion in the acute form of sarcocystosis, while in chronic infection they may cause a decrease in weight gain, the reduction of wool quality, the low production of milk, and ultimately the death of animals. The losses caused by discarding the infected carcasses represent a serious economic problem (Tenter, 1995; Dubey et al., 2015a). Sarcocysts may also infect humans who become final hosts after eating infected raw or undercooked beef and pork (Fayer, 2004; Slesak et al., 2015; Dubey, 2015). Sarcocystis hominis, Sarcocystis heydorni, and Sarcocystis suihominis whose intermediate hosts are cattle, pigs, or wild boars, may elicit gastroenteritis in humans (Prakas and Butkauskas, 2012; Lindsay and Dubey, 2020). The cases of muscular sarcocystosis in which humans act as accidental intermediate hosts are rarely recorded (Fayer, 2004).

As the infection of meat with different species of Sarcocystis can be serious for public health, the identification and differentiation of Sarcocystis spp. are very important (Hoeve-Bakker et al., 2019; Ayazian et al., 2020). The current study aimed to detect and determine the prevalence of Sarcocystis spp. in slaughtered buffaloes in the Tanta city abattoir, Egypt. Morphological, histological as well as molecular studies were undertaken.

Materials and Methods

Ethics statement

The study was approved by the Research Ethics Committee of the Medical Research Institute (MRI), Alexandria University (AU 01219091512). All samples used in the study were collected postmortem. No animal was killed for the purpose of the study.

The study included 517 locally bred buffaloes slaughtered in Tanta city, Egypt during the period between May 2018 and April 2019. The age and sex of animals were recorded.

Macroscopic examination

Parts of the buffalo carcass, especially tongues, diaphragms, esophagus, and skeletal muscles were visually examined for Sarcocystis spp. macrocysts. The organs were cut into small pieces and examined, using a hand lens, for the presence of whitish macrocysts of different sizes as described by Lam et al. (1999). Fifty tissue samples containing visually suspected macrocysts were collected from tongues, diaphragms, esophagus, and skeletal muscles and divided into four parts to be studied by different methods.

Microscopic examination

Pieces of the organs of animals with macrocysts were sampled into separate bags to study the presence of microcysts. Small parts of the organs/tissues were compressed between two glass slides, stained with 1% Giemsa and examined microscopically (Latif et al., 1999).

Histological examination

Parts of the collected tissue samples were fixed in 10% neutral buffered formalin and then dehydrated by different concentrations of ethanol. They were then embedded in paraffin. Sections, about 5 μm thickness, were prepared, stained with hematoxylin and eosin (H&E), and examined under a light microscope (×40) (Bancroft, 1990).

Transmission electron microscope (TEM ( examination

Suspected macrocysts that were examined by light microscope were fixed in 2.5% glutaraldehyde solution in 0.1 M phosphate buffer (pH 7.4) for 4 h. After buffer wash, specimens were post-fixed with 1% osmium tetroxide at 4°C for 4 h. Afterward, the specimens were dehydrated in a graded ethyl alcohol series, passed in two changes of propylene oxide and embedded in an epon mixture. Ultra-thin sections were prepared and stained with uranyl acetate and lead citrate before examination on a Tecnai G2 TEM at 120 kV (FEI, Hillsboro, Oregon, USA) (Lam et al., 1999).

Molecular study

Suspected cysts (N=50) from muscles, esophagus, tongue, and diaphragm were washed with PBS and preserved at -20°C for DNA analysis. Genomic DNA was extracted using DNeasy Blood and Tissue Kit (QIAGEN, Germany) according to the manufacturer’s instructions. Genomic DNA was used as a template to amplify 18S ribosomal subunit DNA using the following pair of primers as described by Rubiola et al. (2020): Sar-F1: 5´GCA CTT GAT GAA TTC TGG CA3´ and Sar-R1: 5´CAC CAC CCA TAG AAT CAA G3´.

PCR reactions were performed using MyTaq™ Red Mix (Bioline) according to the manufacturer’s instructions. PCR cycles were as follows: An initial denaturation step at 95°C for 3 min, followed by 35 cycles of denaturation at 94°C for 1 min, annealing at 50°C for 1 min, and extension at 72°C for 40 s, with a final extension step at 72°C for 10 min. Nuclease-free water (without genomic DNA) was included in each run as a negative control. The PCR products were then run on a 1.5% agarose gel stained with ethidium bromide.

Statistical methods

Data were analyzed using the Statistical Package for Social Sciences (SPSS ver. 20 Chicago, IL, USA). Pearson Chi-square was used for testing the association between categorical variables. The level of significance was set at P<0.05.

Results

A total of 517 buffaloes were slaughtered, and their carcasses were visually examined. Of them, 170 (32.9%) were <2 years, 215 (41.6%) ranged from 2 to 5 years, and 132 (25.5%) ranged from 5 to 10 years. As regard to the sex; 342 (66.2%) were males and 175 (33.8%) were females.

Macroscopic detection

The overall prevalence of suspected sarcocystosis was 26.5% (137/517). There was a statistically significant increase in the prevalence of Sarcocystis macrocysts concerning age. The prevalence was 15.3% among buffaloes aged under 2 years, 21.9% in the age category 2-5 years, and 48.5% among the age category 5-10 years (P<0.001). it was found that 19.9% of males had positive results compared to 39.4% of females (Tables 1 and 2).

Table 1.

Prevalence of Sarcocystis spp. (macrocysts) among 517 buffaloes according to age

Age of animals Examined No. Positive No. (%) Negative No. (%) P-value
<2 170 26 (15.3) 144 (84.7) X2=46
P<.001*
2 to <5 215 47 (21.9) 168 (78.1)
5 to ≤10 132 64 (48.5) 68 (51.5)
Total 517 137 (26.5) 380 (73.5)
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X2: Pearson Chi-square test, and * Statistically significant

Table 2.

Prevalence of Sarcocystis spp. (macrocysts) among 517 buffaloes according to sex

Sex of animals Examined No. Positive No. (%) Negative No. (%)
Males 342 68 (19.9) 274 (80.1)
Females 175 69 (39.4) 106 (60.6)
Total 517 137 (26.5) 380 (73.5)
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X2=21.7, and P<.001*

As to the distribution of Sarcocystis macrocysts in the different organs in the 137 infected animals, 83.2% of infected animals showed macrocysts in the esophagus, 78.8% in their muscles, 59.1% in the diaphragm, 35% in the tongues, and 14.1% animals had macrocysts in more than one site (Table 3, Fig. 1).

Table 3.

Anatomical distribution of sarcocystis (macrocysts) in the 137 infected animals

Organs No. of positive animals Positive percentage
Esophagus 114 83.2
Muscles 108 78.8
Diaphragms 81 59.1
Tongues 48 35.0
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73 animals had cysts in esophagus, muscles, and diaphragms simultaneously

Fig. 1.

Fig. 1

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Macroscopic Sarcocystis spp. (A) Sarcocystis in diaphragm, and (B) Isolated macrocysts

Cyst morphology

Sarcocystis cysts with thin walls were isolated from the esophagus, diaphragm, and muscles; while thick-walled cysts were all detected in tongues. Observed under light microscopy, thin-walled cysts were ovoid and larger in size, measuring 225 ± 34.7 μm × 431.3 ± 82.4 μm whereas thick-walled cysts isolated from tongues were spindle-shaped and smaller in size (141.6 ± 51.4 μm × 263 ± 82.3 μm). Sarcocystis macrocysts pressed between two slides and stained with Giemsa stain showed many bradyzoites (Figs. 1 and 2).

Fig. 2.

Fig. 2

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Light microscopic photograph of pressed macrocysts showing huge number of mature bradyzoites stained by toluidine stain (×400)

Histological examination

Histopathological examination (Figs. 3 and 4) illustrates that among 50 macrocysts examined, Sarcocystis with thin wall was more prevalent (n=37, 74%) compared to thick-walled species (n=13, 26%). Microcysts were detected in 23 animals inside tissues of the tongue and esophagus.

Fig. 3.

Fig. 3

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The intact thin wall around the S. fusiformis cysts was positively stained with H&E technique (arrow). Cyst was packed with bradyzoites separated by multiple septa dividing the cyst into chambers (star)

Fig. 4.

Fig. 4

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Intact Sarcocysts stained with H&E impacted with numerous bradyzoites. The intact thick wall around the cysts was positively stained with H&E technique (thin blue arrow). Cyst was packed with bradyzoites separated by multiple septa dividing the cyst into chambers (thick black arrow)

Transmission electron microscopy (TEM)

TEM showed that cysts contained fully formed bradyzoites (Fig. 5) measuring 4.52-10.33 μm × 2.3-3.39 μm. Bradyzoites were separated by multiple septa dividing the cyst into chambers (Fig. 6).

Fig. 5.

Fig. 5

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TEM ultra-photograph of Sarcocystis macrocysts A: Bradyzoites containing amylopectin (am) as white granules and dense plagues (dp), B: Larger magnification of a bradyzoite showing the ground substance (gs), C: Enlarged part of a bradyzoite showing its membrane (m), and D: Enlarged apical part of a bradyzoite showing the conoid (co), rhoptry (rh), and micronemes (mn)

Fig. 6.

Fig. 6

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TEM picture of mature bradyzoites in Sarcocystis macrocysts

Molecular analysis

PCR amplification of the 18S rRNA gene revealed a specific band at 600 bp in 41 out of the 50 examined samples (82%). Negative samples were tested molecularly and were found to be Cysticercus bovis (El-Sayad et al., 2021).

All DNA extracted from cysts within the esophagus, diaphragm, and muscles gave the specific distinctive band for Sarcocystis spp., while DNA extracted from tongue samples gave no bands in 9 out of the 12 samples examined (75%) (Table 4).

Table 4.

Site of PCR results of S. macrocysts (n=50). Conventional PCR analysis was carried out on fifty macrocysts from different organs

PCR results Esophagus No. (%) Muscles No. (%) Diaphragm No. (%) Tongues No. (%)
Positive 13 (100) 13 (100) 12 (100) 3 (25)
Negative 0 (0) 0 (0) 0 (0) 9 (75)
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Discussion

Diagnosis of Sarcocystis cysts in animals is a prerequisite for survey and surveillance of sarcocystosis in endemic re-emergent or emergent transmission zones (WHO, 2005). Visual inspection method revealed that the overall Sarcocystis spp. infection rate among slaughtered buffaloes was 26.5%. This high infection rate may be due to the climatic conditions in the Northern Delta of Egypt which are favorable for the survival of the parasite. Moreover, bovines are frequently exposed to infection as they are often bred in areas where stray dogs and cats are observed. Environmental contamination by the infective forms exposes all animals to infection with Sarcocystis. Data from various studies showed prevalences that ranged from 25-100% in different countries (Beyazit et al., 2007; Tinak, 2009; Saleh et al., 2022). Differences may be attributed to the sample size, studied organs, diagnostic methods, and especially to the presence of infective stages in the environment. A high prevalence of sarcocystosis is related to close contact between the final and intermediate hosts (Tinak, 2009, Dong et al., 2018).

In the current study, a greater proportion of infection was detected in older buffaloes. This may be attributed to the longer exposure over the years and the time needed for the development of macrocysts inside the carcasses. Similarly, a gradual increase in infection with age was reported in previous studies in Egypt (El-Dakhly et al., 2011; Metwally et al., 2014; Gareh et al., 2020) and other countries (Fayer et al., 2015; Mounika et al., 2018; Imre et al., 2019).

In the present study, infection rate in buffaloes was 39% in females and 19.9% in males with statistically significant difference (X2=21.7, P<.001*). Some studies found a significant association between the rate of Sarcocystis infection and the sex of cattle (More et al., 2008; Nourani et al., 2010). All infected females in the present study were more than five years old, which is under the Egyptian regulations stipulating slaughtering females after that age and this may explain the higher infection rate.

In the current study, the anatomical distribution of Sarcocystis macrocysts by visual examination of organs revealed preferential localization to the esophagus followed by muscles and diaphragm; the least number of macrocysts was detected in tongues. The esophagus may seemingly be an earlier station in the migration route of Sarcocystis. For this reason, the esophagus may be considered more helpful in detecting the infection at an earlier stage than the tongue and muscles. This result was supported by a former studies that recorded the esophagus to be the organ more often affected (Ahmed et al., 2016; JyothiSree et al., 2017; Elshahawy et al., 2022). On the contrary, they disagreed with other reports (Beyazit et al., 2007; Tinak, 2009).

Advances in diagnostic approaches for livestock are very important (WHO, 2005). In the present work, various diagnostic methods other than visual inspection were applied to cysts collected from the carcasses of slaughtered buffaloes. Microscopic examination showed the presence of microcysts inside the tissues of the tongue and esophagus only. These results were in agreement with various studies on different hosts, that recorded the presence of microscopic cysts in organs of buffaloes mainly tongues (Dafedar et al., 2008; Morsy et al., 2011).

Sarcocystis species are diverse. Some are thin-walled such as S. cruzi and S. heydorni, others have thick walls such as S. hominis, S. hirsuta, and S. rommeli (Dubey et al., 2015b; Choi et al., 2018). Depending on histological examination, morphologically different forms of Sarcocystis spp. were found in the examined animals; thin-walled species and thick-walled sarcocysts which produce macrocysts and microcysts with separated chambers. Similar findings were reported by Beyazit et al. (2007) and Ayazian Mavi et al. (2020). Previous studies showed that S. fusiformis and S. dubeyi are the predominant species infecting buffaloes in Egypt (Hilali et al., 2011; Morsy et al., 2018; Ras et al., 2021).

In the present study, PCR amplification of the 18S rRNA gene confirmed infection with Sarcocystis spp. in 82% of the examined macrocysts. All PCR-negative cysts were found in the samples of the tongue. This emphasizes the importance of molecular diagnosis in differentiating Sarcocystis spp. from other cyst-forming lesions.

The present study has revealed a high prevalence of bovine Sarcocystis in the slaughterhouses in Tanta abattoirs, Northern Delta, Egypt which suggests that the environment is heavily contaminated. The use of molecular methods in slaughterhouses should be encouraged to confirm the identity of suspected cysts.

Other studies are recommended to determine the true prevalence of sarcosporidiosis in other herbivores in different regions of Egypt. Further molecular and biochemical studies are required for differentiation between Sarcocystis spp., isolated from different hosts in various geographic localities. Strict control measures should be applied on stray dogs and cats in Egypt, as they possibly represent a serious source of infection.

Conflict of interest

No conflict of interest to declare.

Acknowledgements

We would like to sincerely thank the staff of Veterinary Doctors in Tanta city, the laboratory of the Pathology Department of the Medical Research Institute, and the staff of TEM Unit at Alexandria University. No fund was obtained for execution of the study.

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