Introduction

Production animals generally harbor a series of parasites in the gastrointestinal (GI) tract, particularly helminths, causing clinical or subclinical parasitism, negatively affecting their health status, causing enormous economic losses to the livestock industry, and also affecting productive performance and reproductive of livestock¹. Helminths are endoparasites classified into 2 main groups: nematodes (roundworms) and platyhelminths (flatworms), the latter are subdivided into trematodes (trematodes) and cestodes (tapeworms) that can exhibit complex life cycles involving one or more intermediate hosts that house juvenile stages and a definitive host where the sexually mature parasites are found².

The genus Moniezia belongs to the family Anoplocephalidae in the Order Cyclophyllidea, characterized by the absence of hooks and rostellum, its body consists of a small anterior scolex, neck, followed by a long chain strobile with a specific pattern for each species³. Moniezia species are included in cestodes and they show a worldwide distribution; causing intestinal diseases in ruminant species characterized by a decrease in animal production and, in some cases, death⁴.

Since the description of the genus by Blanchard in 1891, 11 species were included, but later 6 species were added; however, regardless of the number of species recorded, Moniezia benedeni (Moniez, 1879) and Moniezia expansa (Rudolphi, 1810) remain the 2 most important species, with prevalence levels ranging from 1 to 21 % in various geographic regions or different seasons of the same regions⁵.

M. expansa is commonly located in the small intestine of cattle, sheep, goats, deer, among others, however, frequently mature animals do not generally present clinical symptoms, while young animals are more susceptible and develop soft feces, which then become diarrheal accompanied by mucus, segments of the parasite and can suffer intestinal obstruction, intestinal torsion and even intestinal rupture⁶. M. benedeni primarily a livestock parasite, like M. expan-sa, occur more frequently in animals less than 6 to 8 months old, while older animals tend to be less susceptible; after 2 years, they rarely have more than one or a few worms⁷.

This article presents a review on the importance of M. expansa and M. benedeni as gastrointestinal parasites (GIP) in ruminants, and also presents a discussion on the taxonomic problems in both species with the contributions that molecular biology has had to elucidate the identification confusions of both species.

Materials and methods

The present article was based on a systematic bibliographic review on the current information on M. expansa and M. benedeni in GI infections in ruminants, it was approached under a qualitative approach of narrative design and descriptive scope⁸. According to Cesário et al.⁹, the bibliographic review is a type of research based on already constructed material, such as monographs or articles published in scientific journals.

For the search, the main scientific databases were consulted, including Scopus, Web of Science, Taylor & Francis, PubMed, Latindex, SciELO, Dialnet, among others, using the Boolean logical operator “AND” and “OR”. The criteria for selecting the articles to be analyzed included those publications that contain the following key words in Spanish: GI diseases, M. benedeni, M. expansa, moneziosis, taeniasis of ruminants, ruminants with their equivalents in Spanish and Portuguese. In the first search, 390 articles were obtained, of which 27 articles were selected, which were analyzed for the review. For this selection, only open access articles were taken into account, related to topics related to the species M. expansa and M. benedeni, written in English, Portuguese or Spanish.

In addition, a restriction was made in the search for scientific articles to the last 5 years in order to carry out the analysis of the most up-to-date information on the current status of M. expansa and M. benedeni in GI infections in ruminants.

Finally, the review followed the inclusion, selection, identification and review criteria Figure 1.

Figure 1 Flowchart for the selection of articles included in the review 

Development

GI diseases in ruminants. In general, livestock can be affected by different types of parasites that include species of nematodes, trematodes, cestodes and coccidia. Zooparasitic helminths lodge in their digestive tract, are usually associated with subclinical infections and can occasionally cause direct mortality in affected animals¹⁰. In tropical and subtropical areas, GIP are one of the main threats that limit the development and profitability of the livestock industry¹¹.

These types of GIP cause a significant impact on the health of production animals, causing a reduction in the rate of growth, reproduction, milk/meat production and, ultimately, death, causing considerable economic losses¹². According to Charlier et al.¹³, the decrease in productivity is due to the fact that helminths cause alterations in metabolic functions, resulting in a low level of utilization and assimilation of food and consequently results in delayed growth, weight gain, malnutrition, decreased appetite, loss of body weight, emaciation, and increased susceptibility to other pathogens.

Even though parasitic diseases represent an important challenge in livestock farms worldwide, knowledge about the epidemiology of GIP is still limited, mainly in low-income countries¹⁰. Therefore, it is necessary to investigate the morbidity of diseases caused by GIP, both in production and domestic animals, to establish strategies that ensure welfare and management.

Moniezia species and their impact on livestock farming worldwide. Causative agents of the disease known as monieziasis, characterized by the ability to produce a gastrointestinal disorder in ruminants, which is generally considered to have mild pathogenicity, especially in adult cattle, the effects on calves and lambs can cause significant economic losses³.

Moniezia spp., infections have become a major concern in the livestock industry, although the damage caused by cestodes is generally minor compared to the damage caused by gastrointestinal nematodes, the former has shown that they are capable of causing significant economic losses. worldwide in some types of livestock such as buffaloes and sheep¹⁴.

Moniezia have been described, however, given that identification at the species level has been based on the use of morphological characters, its taxonomy is currently quite controversial and there are authors who recognize up to 17 species^3,15. On the other hand, there is only information on genetic sequencing for the 3 main species; M. expansa, M. benedeni and M. monardi¹⁶. In that sense, morphologically, the differentiation between M. expansa and M. benedeni is based on the shape of the interproglottid glands, which have a rosette pattern in M. expansa, while in M. benedeni it has a short and continuous linear pattern³. However, this characteristic is difficult to observe in some specimens, making them not morphologically distinguishable⁵, which is why other biochemical and molecular techniques have been developed for the differentiation of these 2 species. Additionally, in Australia the existence of cryptic species in M. benedeni has been pointed out through multilocus enzyme electrophoresis^15,17, which highlights the need to investigate genetic variation between geographical populations for the establishment of an accurate identification, as well as for re-evaluation of conventional taxonomy.

M. benedeni and M. expansa. Moniezia spp., infections are included among those that affect the small intestine in sheep and goats, although it also includes a wide range of definitive hosts, including cattle and other wild ruminants, with M. expansa being the most important species due to its high frequency of occurrence in sheep and goats compared to other ruminants⁴.

Moniezia species have an indirect biological cycle, in which 2 host species are required, including ruminants as definitive or final host, where occurs sexual reproduction and the eggs produced pass from the intestine of the ruminant into the gravid proglottids and are expulsed through the feces to the soil where they penetrate the oribatid mites that become intermediate hosts (where asexual reproduction occurs)¹⁸.

M. benedeni are widely distributed parasites and are commonly associated with wild and domestic ruminants, although they are generally considered to be of low pathogenicity, because the host does not present specific or serious symptoms, however, a decrease in the growth rate has been observed. in infected animals, therefore, with a reduced value at the time of sale¹⁹. In one study, the prevalence of M. benedeni in European bison from 3 months to 26 years of age in a primeval forest in Białowieża, infection was reported to be 42.3 %, with infection intensity ranging from 2 to 25 tapeworms (average 5.8 specimens), being higher in calves (50 %) than in adult bison (33.3 %)²⁰. According to the authors, the high prevalence of this parasitosis in European bison could be due to poor condition or weak immunity of infected animals.

Although it is uncommon, coinfections of M. benedeni and M. expansa have been verified. In this sense, in Romania Iacob et al.²¹ reported that Carpathian goat kids (aged 6 to 8 months) with acute digestive syndrome presented infection with both species, 56.1 % corresponded to M. expansa, 43.9 % M. benedeni, with a mean infection intensity of 7.5 M. expansa per animal, compared to 4.5 M. benedeni per animal. Infection with both species caused severe pathological lesions in the small intestine such as occlusion, intestinal obstruction, total intestinal villous atrophy and ulcerations.

Therefore, research has indicated that even when the pathogenicity is low, it is necessary to apply control, such as the use of praziquantel at doses of 3.75 and 5.0 mg kg^-1, which can be effective for the complete deworming of sheep and goats, respectively, but there is no information on the optimal dose for the control of M. benedeni in cattle¹⁹. In Bolivia, praziquantel was applied in combination with albendazole resulting in 100 % efficacy and even a high level of control was observed with the use of albendazole. On the other hand, the use of Fenbendazole caused a 60 and 75 % reduction in infections with M. expansa and M. benedeni, while albendazole also achieved a 75 and 95 % reduction in oviposition in M. expansa and M. benedeni, respectively, although the authors do not specify the administered dose of Fenbendazole and albendazole²².

The taxonomic problem in some species within the genus Moniezia. The taxonomy of this genus has been based mainly on morphological characters, making the status of the species uncertain. Taxonomic confusion could be derived from the fact that the description of the species has been based on a limited number of morphological characteristics that are often convergent, which generates controversy about the taxonomy of the genus^3,16. In this sense, there have been confusions and errors in the identification of the 2 main species of Moniezia, M. expansa and M. benedeni, which have been differentiated based on the shape of their interproglottid glands and eggs^3,16. M. expansa has a short continuous linear pattern of interproglottid glands, while M. benedeni has a row of small circular patterns on the interproglottid glands. Regarding the eggs, these have a triangular shape in M. expansa and a tetragonal shape in M. benedeni²³. However, there are problems in identification when specimens lack interproglottid glands or when the eggs have an altered shape^3,16. Additionally, the morphological recognition of these species is also based on features related to the scolex, neck and strobile and the presence of transparent anterior, posterior, mature and gravid segments¹⁵.

Furthermore, Chilton et al.¹⁴ pointed out, through the use of multilocus enzyme electrophoresis techniques, the existence of cryptic species in M. benedeni, which highlights the limitations of identifying Moniezia species solely based on morphological characters. On the other hand, the use of molecular techniques to elucidate the DNA sequence (ITS1 and 5.8S) have been used to distinguish these 2 species^16,25. According to Chilton et al.²⁴, a greater num-ber of genetic markers must be developed to accura-tely identify Moniezia species and serve as a basis for taxonomic investigations.

Also, ribosomal ITS2 is considered a very useful marker for establishing relationships between helminth species²⁶. Yan et al.⁵ amplified and sequenced the 18S rDNA regions of M. benedeni and M. expansa for precise species identification, obtaining that the lengths and GC contents of the sequenced regions were 2476-2487 bp and 51.9-52.1 % for M. benedeni and 2473 bp and 51.9-52.0 % for M. expansa, respectively, in addition the alignment and comparison of the 18S sequences in both species revealed a homology of 92.5 to 93.3 %. Finally, the results suggest no matches in the 18S regions of M. benedeni and M. expansa with other species using the BLAST search, suggesting that the 18S sequences are appropriate markers for the design of distinctive primers for the 2 species of Moniezia.

Similarly, Gao et al.²⁷ characterized, for the first time, the complete mitochondrial genome of M. sichuanensis and noted that the total length of the circular genome was 13652 bp, which consisted of 12 protein-coding genes (PCGs), 22 transfer RNA genes, and 2 ribosomal RNA genes, which are typical of Moniezia mitochondrial genomes.

Additionally, an increasing number of complete mitochondrial (mt) genome sequences provides the opportunity to optimize the selection of molecular markers for studies in ecology, evolutionary biology, and population genetics²³. Complete mt genomes provide individual markers with different levels of sequence variation, as well as combined mtDNA molecular markers for intra-and interspecies studies²⁷.

In conclusion, phylogenetic analysis using the concatenated amino acid sequences suggests that M. benedeni and M. expansa represent close but distinct taxa and, furthermore, the data support the view of the existence of cryptic species in M. benedeni and M. expansa. According to Guo²³ the complete mt genomes of these 2 species will be useful not only to infer phylogenetic relationships between cestodes, but also to identify suitable molecular markers for future studies on diagnosis, population genetics and molecular ecology in Moniezia species.

Conclusion

Among GIP species, Moniezia species, causal agents of the disease known as monieziasis, occur most frequently in cattle, sheep and goats, being characterized by the presence of a gastrointestinal disorder in the host and, although they generally produce symptoms with mild pathogenicity, especially in adult cattle, the effects on calves and lambs can cause significant economic losses.

The taxonomy of the genus Moniezia has been based mainly on morphological characters, making the status of the species uncertain, and consequently the exact number of species in the genus is not known. Concomitantly, errors have been made in the identification of the 2 main species of Moniezia, M. expansa and M. benedeni, which have been differentiated based on the shape of their interproglottid glands and eggs. Therefore, the use of molecular techniques has served as a basis to distinguish these two species; however, it is necessary to obtain a greater number of genetic markers to accurately identify Moniezia species and serve as a basis for taxonomic research. Finally, the correct identification of parasite species associated with production animals is a crucial step in establishing management strategies for infections in livestock, so the present review presents relevant information that contributes to the elucidation of the taxonomic problems among Moniezia species.