Abstract
Parasites may significantly affect the functioning of the host organism including immune response and gut-brain-axis ultimately leading to alteration of the host behavior. The impact of intestinal worms on the host central nervous system (CNS) remains unexplored. The aim of this study was to evaluate the effect of intestinal infection by the tapeworm Hymenolepis diminuta on behavior and functions of the CNS in rats. The 3 months old animals were infected, and the effects on anxiety, exploration, sensorimotor skills and learning processes were assessed at 18 months in Open Field (OF), Novel Object Recognition (NOR) and the Water Maze (WM) tests. After completing the behavioral studies, both infected and non-infected rats were sacrificed, and the collected tissues were subjected to biochemical analysis. The levels of neurotransmitters, their metabolites and amino acids in selected structures of the CNS were determined by HPLC. In addition, the gene expression profile of the pro- and anti-inflammatory cytokines (TNF-α, IL-1β, IL-6 and IL-10) was evaluated by Real-Time PCR to determine the immune response within the CNS to the tapeworm infection. The parasites caused significant changes in exploratory behavior, most notably, a reduction of velocity and total distance moved in the OF test; the infected rats exhibited decreased frequency in the central zone, which may indicate a higher level of anxiety. Additionally, parasite infestation improved spatial memory, assessed in the WM test, and recognition of new objects. These changes are related to the identified reduction in noradrenaline level in the CNS structures and less pronounced changes in striatal serotonergic neurotransmission. H. diminuta infestation was also found to cause a significant reduction of hippocampal expression of IL-6. Our results provide new data for further research on brain function during parasitic infections especially in relation to helminths and diseases in which noradrenergic system may play an important role.
Highlights
The small intestine is a hostile environment for parasitic worms including Hymenolepis diminuta, being subject to digestive enzymes, immune response components, bacteria and active peristaltic movements
Recent advances in the research on parasitic manipulation and/or control of the nervous system of their host resulted in the development of neuro-parasitology, a new and emerging branch of science
Behavioral changes were related to the reduction in noradrenaline level in the central nervous system (CNS) structures, and less pronounced changes in striatal serotonergic neurotransmission
Summary
The small intestine is a hostile environment for parasitic worms including Hymenolepis diminuta, being subject to digestive enzymes, immune response components, bacteria and active peristaltic movements. Adult parasites utilize their scolex and tegumental microtiches to anchor to the intestinal epithelium, allowing parasite-derived molecules like excretory-secretory, surface, and tegumental proteins to interact with the host immune system [1–2]. Many of these molecules are proteins involved in the parasite metabolism and survival strategies, and can play significant roles in the parasite-host relationship. The eggs pass into the external environment along with the feces of the definitive host and, when eaten by the beetle, the hexacanth larva hatches and penetrate into the beetle haemocoel and undergoes transformation into a cysticercoid. Tapeworms settle into the small intestine of the definitive hosts and mature sexually in 2–3 weeks [3]
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