Concurrent parasitic infections of sheep: depression of Trichostrongylus colubriformis populations by a subsequent infection with Oestrus ovis

Vet Parasitol. 2004 May 26;121(3-4):297-306. doi: 10.1016/j.vetpar.2004.01.013.

Abstract

Concurrent infections of sheep with Oestrus ovis and trichostrongyles of the digestive tract are common in the field. Previous results have shown that a previous infection with O. ovis adversely affects worm populations of either Trichostrongylus colubriformis or Haemonchus contortus. However, no information was available to determine the influence of the succession of infections on the expression of interactions between these parasites located in remote anatomical sites. In order to investigate the role of these modulating factors, an experimental study was conducted on four groups of naïve sheep, examining the consequences of a delayed infection with O. ovis on a pre-existing population of T. colubriformis. group T was infected four times with 4000 T. colubriformis larvae on days 0, 14, 28 and 42 of experiment; group O received multiple infections with O. ovis first instar larvae on days 42, 49, 56, 70 and 77; sheep from group TO received both infections and animals from group C remained as uninfected controls. Faecal egg counts and eosinophilia were measured weekly throughout the study. At necropsy (day 91), the mucosal cellular responses in the nasal cavities (septum, turbinates, ethmoid and sinus) and in the digestive tract (stomach and small intestine) from all animals were analysed from histological sections. Infection of the digestive tract with nematodes did not modify the biology of Oestrus populations, as measured by the number and weight of larvae. In contrast, infections with O. ovis after T. colubriformis infection was related to significant reductions (P < 0.01) in nematode egg excretion and worm burdens. These changes were associated with significant modifications in populations of mast cells, globule leucocytes and eosinophils in the respiratory and digestive tracts. These results indicate that an antagonistic interaction exists between the populations of O. ovis in the nasal cavities and T. colubriformis in the small intestine but that the order of succession of infections with the two parasites is not a major modulating factor for expression of interactions. They also confirm that parasitic infection in one particular anatomical site induces "at distance" inflammatory reactions of the whole mucosal system.

MeSH terms

  • Animals
  • Blood Cell Count / veterinary
  • Diptera / growth & development*
  • Eosinophilia / parasitology
  • Eosinophilia / veterinary
  • Feces / parasitology
  • Female
  • Gastrointestinal Diseases / parasitology
  • Gastrointestinal Diseases / veterinary
  • Intestinal Mucosa / parasitology
  • Male
  • Myiasis / complications
  • Myiasis / parasitology
  • Myiasis / veterinary*
  • Nasal Mucosa / parasitology
  • Parasite Egg Count / veterinary
  • Respiratory Tract Infections / parasitology
  • Respiratory Tract Infections / veterinary
  • Sheep
  • Sheep Diseases / parasitology*
  • Trichostrongylosis / complications
  • Trichostrongylosis / parasitology
  • Trichostrongylosis / veterinary*
  • Trichostrongylus / growth & development*