Cestodes were taken from the small intestine of sheep and goats slaughtered at the slaughterhouses of Guelma (communal slauterhouse of Guelma, Oued Zenati and Hammam Debagh). The collection was made during a period from February to June 2022.
The impact of intrinsic factors influencing the prevalence and occurrence of cestodes were studied, such as: the influence of the sex of the hosts, their breeds and their age. The influence of other external factors such as the origin of the animals and the sampling season was also investigated.
2.1 Species of cestodes identified
Microscopic examination of intestinal Anoplocephalids of small ruminants in Algeria, showed morpho-anatomical variability, which allows to identify six species belonging to four genera: Moniezia expansa, Moniezia benedeni, Stilesia globipunctata, Stilesia sp, Avitellina centripunctata and Thysaniezia ovilla, closely related to descriptions by Euzeby (1982) and Beverigdge (1994).
2.1.1 Moniezia expansa
The scolex carries four suckers with linear opening. The segments are much wider than long. After staining, we observed on the mature segments : two horseshoe-shaped ovaries, two vitellogenic glands, several testes, two genital pores and a row of interproglottid glands that are aligned parallel to the posterior border of the proglottids (Fig. 2).
2.1.2 Moniezia benedeni
Species similar to Moniezia expansa but with wider proglottids (1.5 to 2cm), voluminous scolex carrying four suckers with circular opening. The interproglottid glands are diffuse at the posterior edge of the segments in their median part (Fig. 3).
2.1.3 Avitellina centripunctata
The neck is wide, the scolex is voluminous and spherical with suckers with a linear opening. External segmentation is barely visible. The genital pores are irregularly alternated. The uteri are arranged transversely in the middle of the proglottids. The ovigerous portion is cylindrical and contains a single paruterine organ (Fig. 4).
2.1.4 Stilesia globipunctata
These worms are curly with an inconspicuous external segmentation. The scolex bears four suckers. Two lateral canals and genital pores which are irregularly alternated (Fig. 5)
2.1.5 Stilesia sp
During our research on cestodes parasitizing the intestines of sheep, we found a sixth species. It is a curly worm 1m long and ≥ 1mm wide, carrying a scolex with 4 suckers and an inconspicuous external segmentation with a median canal (Fig. 6). To the naked eye it is similar to the genus Stilesia because the curly shape is a defining characteristic of this genus (Bussieras and Chermette 1995). We thought of the species Stilesia hepatica because this worm is morphologically similar to this species. However, the latter lives in the bile ducts and not in the intestines, this is why we named it Stilesia sp.
2.1.6 Thysaniezia ovilla
The scolex bears linear suckers. The mature segments contain irregularly alternate genital pores. Each ovigerous segment contains a large number of paruterine organs and numerous testes (Fig. 7).
All cestodes (except Stilesia sp) found in our work have already been reported in sheep and goats in several countries. Moniezia expansa has been reported in sheep and goats in Dahomey, Guinea Bissau, Chad, Ghana, Niger and Senegal (Aissatou 2000 ; Bastiaensen et al. 2003 ; Achi et al. 2003). In Ituri, intestinal cestodes are relatively uncommon. Four species of cestodes, 56% of which were from the genus Avitellina, were present in the small intestine (Chartier et al. 1990).
All previously reported species were described by Tamssar in 2016 on gastrointestinal helminthic parasitism of sheep slaughtered at the Dakar slaughterhouse.
2.2 Statistical study
2.2.1 General prevalence
According to Margolis and his colleagues (1982) prevalence is defined as the proportion of host individuals infected in a sample with a particular parasite, often expressed as a percentage.
The study was carried out on 116 samples, including 80 sheep and 36 goats. Data in Fig. 8 showed parasite prevalence of 14% in sheep and 8% in goats. This low prevalence of cestodes found could be explained by the indirect cycle because the biological evolution of the eggs continues in the intermediate host mite and lives in the pasture soil, which reduces the possibilities of reinfestation (Boullkaboul et al. 2006). These oribates are rare on cultivated land. In addition, desiccation and drought are unfavorable factors to their survival (Lefèvre et al. 2003).
We note that the number of infected sheep is higher than that of infected goats with a difference of 6%. Indeed, This difference in host infestation rates was interpreted by Chartier et al (1990) and Achi et al (2003), by the difference in the feeding behavior of the hosts. Indeed, sheep prefer herbaceous plants while goats make more use of woody pastures rich in tannins, whose natural anthelmintic effects were known. According to Vasiliu et al. (1980) oribates, which are the intermediate hosts of Anoplocephalidae, are generally found in grassland vegetation, so this positioning favors the sheep infestation.
2.2.2 Specific prevalence of infestation in sheep and goats
Data of Fig. 9 show the percentages of infestation of each species : For sheep, we noted the following species with their respective prevalences: M. expansa (54%), M. benedeni (21%), S. globipunctata (13%), S. sp (3%), A. centripunctata (6%) and T. ovilla (4%). For goats we found: M. expansa (47%), M. benedeni (31%), S. globipunctata (11%), A. centripunctata (8%) and T. ovilla (3%).
According to Vassiliades (1981), the infestation by Anoplocephalids is generally considered benign, however it should not be neglected, because if the infestation is strong as is often the case, it can cause serious dystrophic conditions which could affect profitability of productions.
According to the experimental study by Hansen and Perry (1995), helminthiasis inhibits the improvement of sheep production. In fact, in the case of heavy infestation by Stilesia globipunctata, death can occur within few days after diarrhea followed by muscle wasting. In our work we noted a low rate of infestation by Stilesia globipunctata, so the infestation in our study region is considered benign.
2.2. 3 Prevalence of infestation according to sex
The results presented in Fig. 10 show that the prevalence of infestation by Anoplocephalids is higher in female sheep (60%) than in males (40%). Similar research has noted higher infestation frequencies in females than in males. In fact, females slaughtered are those with poor health or those which are elderly and/or have other defects. This seems to be common for many slaughterhouses and for all pathologies (Mwabonimana et al. 2016).
Concerning the relationship of the occurrence of Anoplocephalid species and the sex of infected animals, it was noted from the data in Fig. 11 that Moniezia expansa is the parasite most encountered in small ruminants, whether in sheep (male 50%, female 49%) or in goats (male: 43%, female: 53%), it has been around three times more common than Moniezia benedeni. The latter is found at a prevalence of 22% in females and 19% in males for sheep, and 18% in females and 38% in males for goats. Boulkaboul et al (2006) reported that it was approximately three times more frequent, and that Moniezia benedeni is less common observed more often in cattle than sheep.
Chartier et al (2000) stated that the distribution of species is not uniform although Anoplocephalidosis is a cosmopolitan affection, in addition these species are more likely to be seen in warm and dry regions. According to studies by Abassa in 1995, A. centripunctata avitelliniosis is a condition frequently encountered in adult ruminants while monieziosis is more common in younger ones.
2.2.4 Prevalence of infestation according to age
Data presented in Fig. 12 show the prevalence of Anoplocephalid infestation according to the age of infested animals. In sheep, the rate of young is higher (54%) than adults (46%). Similarly, for goats the young recorded a percentage of 71% and the adults a percentage of 29%.
A great receptivity of the young is marked in both host species. In the study by Benmarce et al. (2018) carried out in the same region (Guelma), the percentage of infestation is higher in young than in adult animals. In addition, the work of Boulkaboul and Moulaye (2006) showed that the rate of infested adults is low in comparison with young animals. This high receptivity to parasites can be attributed to the immaturity of the immune system of young ruminants which makes them more vulnerable to parasitism (Vlassoff et al. 2001). According to research by Boucheikhchoukh et al. (2012) in eastern Algeria (El-Tarf), age is a risk factor. Colditz et al. (1996) showed that parasites belonging to the genus Moniezia constitute a serious danger for young animals, it would seem that Avitellina and Stilesia play the same role.
2.2.5 Prevalence of infestation according to the origin of the animals
The animals slaughtered in the slaughterhouses of Guelma originate from several regions of Algeria.
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In sheep : data of Table 1 show that the infestation rates are different depending on the parasitic species and the origin of the slaughtered animals, so we see a strong infestation by M. expansa (21%) in Guelma and Oum El Bouaghi. For M. benedeni, the highest rate was observed in Guelma (17%); S. globipunctata in Tiaret which is a wilaya in western Algeria (33%), and S. sp (50%) in Guelma and Oum El Bouaghi; the highest infestation by A. centripunctata was recorded in Oum El Bouaghi (60%); T. ovilla in Guelma and Tiaret (33%).
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In goats : In the following Table 2, we see that M. expansa has the highest rates in Guelma, Oum El Bouaghi and El Bayed (19%), M. benedeni (40%) in Batna, S. globipunctata (50%) in Tiaret and Tebessa, A. centripunctata (67%) in Guelma and T. ovilla (100%) in Guelma.
According to our results, the majority of the wilayas from which our samples were taken belong to a sub-arid bioclimatic domain. Indeed, intestinal Anoplocephalidosis of small ruminants constitutes a parasitosis which, although cosmopolitan, particularly affects the dry areas of the African continent (Saidi et al. 2009).
2.2.6 Prevalence of infestation according to parasitic association
Data in Fig. 13 indicate that the prevalence of polyparasitism in both host species is similar.
According to data in Table 3, it appears that in sheep, polyparasitism was observed in both sexes (two males and two females), on the other hand we noticed in goats a total absence of polyparasitism in females.
Polyparasitism is the association of two cestode worms belonging to different species in the same host. In our study we reported a high rate for the M. expansa - S. globipunctata association (50%), compared to the parasitic associations of M. expansa - T. ovilla (16.67%), A. centripunctata - S. globipunctata (16.67%) and A. ovilla - M. benedeni (16.67%). The results of the work of Mallé and his collaborators (2018) show a greater frequency of Avitellina - Stilesia associations and an absence of a Moniezia - Thysaniezia co-infestation.
In the majority of cases, parasitic associations are composed of M. expansa with another species (T. ovilla or S. globipunctata). We also noticed an association between M. benedeni-S. globipunctata and between A. centripunctata -S. globipunctata. The most common association is M. expansa- S. globipunctata.
The cause of the choice of parasitic associations can be interpreted by the size of the worms. In fact, in the majority of association cases we have noted the presence of a large worm (like Moniezia) with a small one (like Stilesia and Avitellina).
2.2.7 Prevalence of infestation according to month
According to the results in Fig. 14, we noticed a strong infestation of sheep in the months of April (50%), May (52%) and June (54%) compared to the months of February (15%)and March (29%). There is also a very high infestation rate among goats in April (29%), May and June (50%) compared to the months of February (14%) and March (21%).
The study by Mwabonimana et al. (2016) showed that the infestation increased in the month of August (17.8%) followed by the month of September (16%), the month of June (15%) and finally the month of July (14.8%). In Morocco, in the Middle Atlas Mountains, the infestation is maximum between February and April (Ouhilli et al. 1981). Losson et al. (2003) reported that Anoplocephalid infestation occurs mainly during the dry season (the short and long seasons) just after the rainy period.
Given that the abundance of oribates is favored by climatic conditions (humid and overcast weather), the nature of the soil, etc., we believe that the infestation occurs most often after the rainy period, which is close to the remarks de Chartier et al. (2000). According to all this research works, this activity presents variations between countries and within the same country depending on the climatic conditions of each region.
2.2.8 Prevalence of infestation according to host race
Analysis of the data in Figure show that sheep belonging to the Berber and Rembi breeds are the most infested by anoplocephalids with the following respective prevalences : 45.5% and 27%, while sheep of the Ouled Djellal, Ouled Nail and Kabylie breeds are less infested (successively : 9.5%, 12% and 6%).
In a study carried out in Tiaret (western Algeria) on the Ouled Djellal breed, Boulkaboul and Moulaye (2006) reported the presence of 334 heads infested with intestinal cestodes, out of a total of 423 heads. Another study on internal parasitism was carried out by Saidi et al. (2009) in sheep of the Rembi breed in a steppe region of Algeria (Ain D'hab) showed a low prevalence of infestation by intestinal cestodes (Moniezia sp) compared to other internal parasites. The low prevalence of intestinal cestodes found in sheep in the Ain D’hab region could be attributed to the indirect cycle of parasites. In fact, the eggs of the Anoplocephalidae continue their development in the oribate mite which lives in the pasture soil, where the drought of these regions is unfavorable for their survival (Lefèvre et al., 2003).