Ascaridia galli infection affects pullets differently when feed is contaminated with the Fusarium toxin deoxynivalenol (DON)

Abstract

The Fusarium mycotoxin deoxynivalenol (DON) is a common contaminant of cereal grains used as animal feed. DON is known for its cytotoxic and anti-proliferative properties and might adversely affect the health of poultry. The prevalence of the intestinal parasitizing roundworm Ascaridia galli is higher in outdoor housing systems and has been associated with maldigestion and malabsorption. It was hypothesized that ingested DON might not only affect the pullet itself but could also act on the nematode parasitizing in the ingesta. To examine these interactions between A. galli infection and DON contamination of feed 4 groups of 9 pullets in each were tested; non-infected groups were fed either an uncontaminated control (CON−) or a Fusarium toxin contaminated and mainly DON-containing diet (FUS−), and the corresponding A. galli inoculated groups were fed accordingly (CON+, FUS+).

A. galli infection significantly reduced the jejunal villi height and increased the thickness of the tunica muscularis with the effect being more pronounced when the DON-containing diet was fed (Group FUS+). Only in this group significantly increased weights of jejunal and ileal tissues and of livers were noticed. Moreover, DON was detected in plasma of the pullets at higher frequencies when they were infected suggesting a facilitated absorption of DON.

Group FUS+ was characterized by a significantly higher excretion of A. galli eggs and a concomitant lower proportion of pullets with detectable antibodies against a somatic antigen of A. galli while worm burden and worm characteristics were not affected by diet.

Other effects of feeding the FUS diet to the infected pullets included an increased mass per length of male worms.

In conclusion, infection of pullets with A. galli might increase the susceptibility towards DON as indicated by an increased DON absorption rate and a compromised antibody formation. The effects of DON on fecundity and worm morphology require further examination.

Introduction

The prevalence of endoparasitoses in gallinaceous poultry depends on the housing system. Hens kept on deep litter or outdoors might experience a higher infection pressure to the roundworm Ascaridia galli because of the permanent contact to parasite eggs present in excreta and soil, enabling the full A. galli infection cycle to run (Kaufmann et al., 2011).

In free ranging hens the prevalence of A. galli, Capillaria obsignata and Heterakis gallinarum was found to be 18, 28 and 16%, respectively, as reported for a screening of different production systems for the occurrence of various nematode species in Bavaria. In floor-kept hens the prevalence of these nematode infections varied between 5 and 7% while hens kept in cages were virtually free of these infections (Zeller, 1990).

This general trend was also confirmed for housing systems in Denmark where the prevalence of C. obsignata, A. galli and H. gallinarum infection were reported to be 54, 64 and 72% for free ranging hens, and 52, 42 and 19% for floor-kept hens, while cage kept hens were characterized by a low A. galli, prevalence of 5% (Permin et al., 1999).

In growing chickens an A. galli infection is manifested by an unspecific growth depression rather than by other overt clinical signs of an infection (Gauly et al., 2001).

It has been reviewed that this growth depression might also result from an infection related depression in feed intake (Chubb and Wakelin, 1963). Moreover, other host or nutrition derived factors might influence the overall outcome of an A. galli infection ranging from a pronounced growth depression via neutral effects to even a growth stimulation (e.g., Chubb and Wakelin, 1963). Based on the higher A. galli prevalence in housing systems which are increasingly practised today and on the uncertainties of the general outcome of an infection, the knowledge of infection influencing factors arising from feed is increasingly important.

A nutrition derived factor with the potential to affect both the host and the worm itself might be the presence of certain mycotoxins in feed. The Fusarium toxin deoxynivalenol (DON) is one of the most important feed contaminants worldwide as it occurs in diet concentrations high enough to adversely affect the health and performance of farm animals (EFSA, 2004). Gallinaceous poultry is generally regarded as relatively insensitive to DON as compared to other species, such as pigs, which is reflected by the different guidance levels for critical dietary DON concentrations of 5 and 0.9 mg DON/kg diet, respectively (EC, 2006).

DON acts as an immune-modulator in various species through interaction with ribosomes and transcription factors resulting in a disturbance of protein synthesis and deregulated cytokine interplay (Döll and Dänicke, 2011, Pestka, 2010). DON was shown to influence the synthesis of various proteins in broilers (Dänicke et al., 2011) and laying hens (Chowdhury and Smith, 2005), to affect white blood cells (Chowdhury et al., 2005) and decrease the antibody titres to the Newcastle disease virus in layers (Dänicke et al., 2002) and in broilers dose-dependently (Dänicke et al., 2003). Although in these experiments effects were observed mostly at DON concentrations higher than the mentioned guidance level of 5 mg DON/kg diet, it needs to be stressed that this critical dietary DON concentration applies for “normal” production conditions (EC, 2006). Additional stress factors might decrease the DON concentration in the diet for inducing adverse effects.

Thus, the aim of the experiment was to test the effects of DON on pullets which were either infected with A. galli or free from this helminth. Not only the consequences for various nutritional, morphological and pathophysiological characteristics of the pullets were examined but also the DON effects on the worms. Moreover, DON metabolism both in pullets and in worms was investigated.