Abstract
Ascaris suum is one of the most prevalent nematode parasites in pigs and causes significant economic losses, and also serves as a good model for A. lumbricoides, the large roundworm of humans that is ubiquitous in developing countries and causes malnutrition, stunted growth and compromises immunity to other pathogens. New treatment options for Ascaris infections are urgently needed, to reduce reliance on the limited number of synthetic anthelmintic drugs. In areas where Ascaris infections are common, ethno-pharmacological practices such as treatment with natural plant extracts are still widely employed. However, scientific validation of these practices and identification of the active compounds are lacking, although observed effects are often ascribed to plant secondary metabolites such as tannins. Here, we extracted, purified and characterised a wide range of condensed tannins from diverse plant sources and investigated anthelmintic effects against A. suum in vitro. We show that condensed tannins can have potent, direct anthelmintic effects against A. suum, as evidenced by reduced migratory ability of newly hatched third-stage larvae and reduced motility and survival of fourth-stage larvae recovered from pigs. Transmission electron microscopy showed that CT caused significant damage to the cuticle and digestive tissues of the larvae. Furthermore, we provide evidence that the strength of the anthelmintic effect is related to the polymer size of the tannin molecule. Moreover, the identity of the monomeric structural units of tannin polymers may also have an influence as gallocatechin and epigallocatechin monomers exerted significant anthelmintic activity whereas catechin and epicatechin monomers did not. Therefore, our results clearly document direct anthelmintic effects of condensed tannins against Ascaris and encourage further in vivo investigation to determine optimal strategies for the use of these plant compounds for the prevention and/or treatment of ascariosis.
Highlights
The closely related worms Ascaris suum and A. lumbricoides are among the most prevalent nematode parasites in pigs and humans, respectively
The use of plant compounds such as Condensed tannins (CT) as anthelmintics has received renewed interest due to the on-going threat of parasite resistance to the small number of synthetic drug classes currently available, as well as concerns about drug residues arising from prophylactic use of synthetic drugs in food production systems
Whilst the potential of CT to be used as anthelmintics has been repeatedly demonstrated in parasites from ruminant livestock, as well as in some rodent models, evidence of direct anthelmintic effects against the pig parasite A. suum has been lacking
Summary
The closely related worms Ascaris suum and A. lumbricoides are among the most prevalent nematode parasites in pigs and humans, respectively. Ascaris suum has a high prevalence in pigs in both developed and developing countries, resulting in significant economic penalties for pig farmers [2,3]. Ascaris control is based mainly on mass treatment with synthetic anthelmintic drugs. In the long-term this is not sustainable – re-infection after annual or bi-annual drug treatment is more or less unavoidable due to the long-lived and resistant eggs which survive for many years in the environment [7], and the reliance on a limited number of related compounds (mainly albendazole and mebendazole) for mass drug administration against A. lumbricoides means that the threat of drug resistance is an on-going concern [1]. There is an urgent need to investigate alternative and/or complementary options for the control of these parasites
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