Parasitic infections are considered a significant and very common problem in relation to animal health, particularly for grazing ruminants. As veterinarians, when we refer to internal parasites we mainly think of gastro-intestinal worms, lung worms and liver flukes. We rarely, if ever, consider paramphistomatidae or rumen flukes. Nevertheless, these flatworms – that settle in the rumen of grazers (ruminants) – are found the world over. Where they previously primarily caused disease in ruminants in tropical and sub-tropical regions, it appears that infections in Western Europe are more common than we thought. Opinion is divided about the effect of these parasites on animal health and technical results.
Paramphistomosis, an infection caused by a parasite in the genus Paramphistomum, has been known for many years. Where paramphistomosis was previously described as a disease that occurred mainly in tropical regions, in recent years we have seen an increase in the prevalence in Western Europe too (Huson et al., 2017). Calicophoron daubneyi (formerly known as Paramphistomum daubneyi) is the most common of the various Paramphistomum species found in Europe. France, Great Britain, Ireland, Belgium, Portugal and Spain have seen a tremendous increase in the occurrence of this parasite and these countries emphasise the importance of control measures (Malrait et al., 2015). In the Netherlands, routine testing of all faeces samples received by the Animal Health Department in the period 2009-2014 revealed an incidence of 15.8% in cattle and 8% in sheep (H.W. Ploeger, 2017).
The spread through purchasing of infected animals across continents, improved diagnostic methods such as faeces inspection by a modified McMaster technique, climatological changes with increased rainfall and increased temperatures and switching to a more targeted treatment of liver fluke (not effective against rumen fluke) were all suggested as possible reasons for the increased prevalence. A recent study performed by Edinburgh University using the deep amplicon sequencing method revealed how extensive the impact of intense movements of animals is on the spread of the infection (Sargison et al., 2019). Based on this result, proper parasite control is required, in addition to preventative measures of course, such as combating the intermediate host through lowering the water level.
The life cycle of the rumen fluke Calicophoron daubneyi is very similar to that of the liver fluke Fasciola hepatica. In addition to having the same final host, the rumen fluke also has an indirect cycle, with the fresh water snail / mud snail Galba Truncatula acting as intermediate host (Kaufmann et al., 1996).
However, there are also clear differences between the two trematodes. Following ingestion of the infectious metacercaria by the final host, the excysted larvae are released in the abomasum from where they migrate to the duodenum. There they attach to the mucosa and continue to develop for 3 to 6 weeks. Their presence in and migration through the small intestines can cause significant amounts of damage. The immature stages can absorb large sections of intestinal wall, resulting in necrosis (Hendrix et al., 2006). Once the rumen fluke has fully matured, the parasite migrates back to the rumen and reticulum, where it attaches to the rumen papillae. After being present in the rumen and the reticulum for several weeks, the adult rumen fluke is able to start producing eggs. These eggs end up in the pasture via the faeces. Miracidia emerge from the eggs only in an aqueous environment and if the temperature is above 10 ˚C. These miracidia can survive for a maximum of 24 hours in the outside world. They spend this time searching for the intermediate host Galba Truncatula. After several developments in the intermediate host, the cercaria are excreted. The cercaria that are released undergo fairly rapid encystation to form metacercaria in a suitable location (such as a patch of grass near water). They can survive for up to 6 months in a temperate climate. The final host becomes infected when it eats the grass on which the metacercaria are present.
Life cycle of the rumen fluke, Calicophoron daubneyi (Huson et al., 2017)
We can distinguish between the symptoms in the final host caused by the immature stages on the one hand and the adult stages on the other hand.
Paramphistomosis can manifest in two ways in cattle:
Acute form caused by the immature stages
The migration of the juvenile rumen flukes and the migration in the mucosa of the small intestines can result in the destruction of the gastro-intestinal glands. Erosion of the intestinal epithelium, with haemorrhagic damage and mucosal oedema, becomes evident quite soon after infection with rumen fluke. The resulting acute haemorrhagic enteritis can be associated with significant diarrhoea, reduced appetite, dehydration, weight loss, anorexia and even death. Repeat infection of animals is often associated with type 1 hypersensitivity reactions, which can increase the severity of the symptoms.
Chronic form caused by adult stages
Relatively mild infestations of adult worms in the rumen rarely cause clinical symptoms.
However, large numbers of rumen flukes – preferably grouped near the ruminal folds – can cause tympanites, ruminal atrophy and oedema formation in the mucosal folds of the rumen. This can be associated with thinner faeces and reduced appetite.
Histopathological examination of infected cattle has revealed that a correlation exists between the number of rumen flukes and the damage to the rumen, such as hyperkeratosis and infiltration of inflammatory cells (Fuertes et al., 2015). However, it is not certain whether the presence of rumen flukes has a significant effect on the health, growth and performance of the final host. In contrast, a study at abattoir level found a clear negative association between rumen fluke infection and the carcass weight and the fat coverage of the animal (Bellet et al., 2016).
Most parasites induce a certain degree of immunity in their final host, resulting in a balance between the parasitic population and the host. It is not one hundred percent clear yet whether this phenomenon also applies to trematode infestations. According to Chauvin et al, 2012 this is not entirely the case for rumen fluke. Ferreras et al 2014 also suggest that repeated exposure to rumen flukes does not offer any protection against repeat infection. Repeated, severe infestations of rumen flukes can result in an accumulation of the number of rumen flukes.
In contrast, Knubben-Schweizer found in her research that successive small infections in older animals result in partial immunity.
Clinical symptoms are usually not very specific and therefore will not result in a clear diagnosis.
If the case history refers to animals with severe diarrhoea that graze in areas that are frequently flooded, then rumen fluke infection should certainly be taking into consideration when making the diagnosis.
At the moment, the presence of adult worms (egg-producing stage) can only be demonstrated by faeces inspection.
We can distinguish between qualitative and quantitative faeces examinations. Qualitative examination is usually sufficient for routine examinations. This is performed to check whether an animal is infected or not.
To obtain a clear impression of the degree of infection, it is better to perform a quantitative determination. The quantitative determination can include determination of the number of eggs per gram of faeces (=EPG) (Vercruysse, 1992). One of the quantitative methods used to determine the EPG of various types of parasites is the McMaster method. This method uses a counting chamber for this process. As the eggs of trematodes are relatively heavy, a flotation liquid with a specific gravity over 1.35 must be used.
Rieu et al. (2007) studied the degree of reliability of faeces testing for rumen fluke. A significant correlation was observed between EPG counts and the severity of the infection. Finding more than 100 eggs per gram of faeces was an indication that the rumen or reticulum contained more than 100 adult paramphistomatidae.
The Master’s thesis by Karen Malrait from the University of Ghent used a cut-off value of 200 EPG to distinguish a severe infection (more than 201 adult rumen flukes in the rumen) from milder infections. However, the amount of eggs in the faeces says nothing about the pathogenicity of the infection, as symptoms are primarily caused by the immature stages.
Faeces inspection during immature stages can yield a false negative result. This is due to the fact that immature stages do not excrete eggs. In severely infected animals, it is possible to detect red immature rumen flukes in the faeces.
Autopsy of dead animals can provide quite a lot of information.
For the acute form of the infection, the opening of the intestines will reveal the presence of red immature rumen flukes measuring one to two millimetres (depending on their stage of development), small superficial ulcers and oedema of the mucosa.
In the case of a chronic infection, opening of the rumen will reveal the adult parasites attached to the wall.
Research into serological and molecular techniques is ongoing and this may result in improved diagnostics in future.
As is the case with liver fluke infection, treatment is based on two pillars.
A sound pasture management plan, which ensures that cows are not left in marshy areas, is one of the most important things that can be implemented. Not allowing young, susceptible animals to graze with older animals, or not allowing young animals to graze during the most dangerous period of the pasture season can significantly reduce the infection pressure. Drastically reducing the survival chances of the fresh water snail by ensuring good drainage of pastures with a high water level will also significantly reduce rumen fluke infections.
Taking into account the information about the effect of the mass movement of infected animals on the spread of Calicophoron in the UK and Ireland (from the study performed under the supervision of Edinburgh University), it would seem sensible to treat infected animals too. Knowledge of the infection status of newly purchased animals is therefore certainly important.
But what to do with infected animals?
There are currently no anthelmintics registered in Europe for the treatment of rumen fluke infections.
Many in vitro and in vivo studies examined the efficacy of various de-worming agents to combat rumen fluke. No generally accepted criteria have been established to evaluate successful treatment with flukicides in the treatment of trematode infections. Therefore, as is the case with the treatment of nematode infections, we will also look at the reduction in the number of eggs present in the faeces.
A study by Arias et al., 2013 looked at the efficacy of albendazole, netobimin, closantel and oxyclozanide in the treatment of the rumen fluke Calicophoron daubneyi in naturally infected cows. Oxyclozanide and closantel, both administered orally, were deemed effective in this study.
The literature recommends oxyclozanide – registered for the treatment of liver fluke – as “the” molecule of choice for treatment of mature rumen fluke. The dosage of oxyclozanide used in the treatment of rumen fluke infections is higher than the registered dosage for liver fluke infections. Rolfe & Boray (1987) and Alzieu et al. (1999) studied the effect of various dosages of oxyclozanide on mature and immature rumen flukes.
The high dosage of 18.7 mg/kg twice, with three-day interval yields a good efficacy against both mature and immature stages. Side effects, such as diarrhoea and lethargy, have been reported in treated animals at such high doses. These side effects disappeared 24-48 hours after the treatment. For fear of the above-mentioned side effects, veterinarians in the field prefer to work with the dose of 10 mg/kg BW (without stop dose) twice with 3 days in between and this with good results.
As rumen fluke infection does not form an indication for the veterinary medicinal products containing oxyclozanide, the treatment of paramphistomosis with this active ingredient can only take place via the cascade. If dosages exceeding those listed in the package leaflet are used, then the veterinarian must prescribe a withdrawal period that is sufficiently long to ensure that products derived from the animal will not contain unwanted residues.
Although rumen fluke infection has been discussed extensively in the literature, we have observed that rumen fluke is diagnosed in practice, but that an infection with severe clinical symptoms in cows occurs only sporadically. A recent study has revealed that – in addition to changing weather conditions – the mass movement of positive animals is a major contributor to the increased prevalence in recent years. Treatment with a de-worming agent is only recommended if the faeces inspection warrants this. Unnecessary treatments can contribute to resistance. No products have been registered to date for the treatment of paramphistomosis. Oxyclozanide has been described in the literature as effective.
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