Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth.
This study tested the hypothesis that a host mucogenic response to an intestinal coccidial infection promotes the onset of necrotic enteritis (NE). A chick NE model was used in which birds were inoculated with Eimeria acervulina and E. maxima and subsequently with Clostridium perfringens (EAM/CP). A second group of EAM/CP-infected birds was treated with the ionophore narasin (NAR/EAM/CP). These groups were compared to birds that were either non-infected (NIF), or infected only with E. acervulina and E. maxima (EAM), or C. perfringens (CP). The impact of intestinal coccidial infection and anti-coccidial treatment on host immune responses and microbial community structure were evaluated with histochemical-, cultivation- and molecular-based techniques. Barrier function was compromised in EAM/CP-infected birds as indicated by elevated CFUs for anaerobic bacteria and C. perfringens in the spleen when compared to NIF controls at day 20, with a subsequent increase in intestinal NE lesions and mortality at day 22. These results correlate positively with a host inflammatory response as evidenced by increased ileal interleukin (IL)-4, IL-10 and IFN-gamma RNA expression. Concurrent increases in chicken intestinal mucin RNA expression, and goblet cell number and theca size indicate that EAM/CP induced an intestinal mucogenic response. Correspondingly, the growth of mucolytic bacteria and C. perfringens as well as alpha toxin production was greatest in EAM/CP-infected birds. The ionophore narasin, which directly eliminates coccidia, reduced goblet cell theca size, IL-10 and IFN-gamma expression, the growth of mucolytic bacteria including C. perfringens, coccidial and NE lesions and mortality in birds that were co-infected with coccidia and C. perfringens. Collectively the data support the hypothesis that coccidial infection induces a host mucogenic response providing a growth advantage to C. perfringens, the causative agent of NE.
Collier
C T
CT
Department of Animal Sciences, University of Illinois at Urbana-Champaign, IL 61801, USA.
Hofacre
C L
CL
Payne
A M
AM
Anderson
D B
DB
Kaiser
P
P
Mackie
R I
RI
Gaskins
H R
HR
D000818:Animals; D001427:Bacterial Toxins / Q000096:biosynthesis; D002135:Calcium-Binding Proteins / Q000096:biosynthesis; D002645:Chickens; D003016:Clostridium perfringens / Q000254:growth & development*; D003044:Coccidia / Q000472:pathogenicity*; D016207:Cytokines / Q000096:biosynthesis; D004751:Enteritis / Q000209:etiology* / Q000276:immunology / Q000473:pathology; D008297:Male; D009077:Mucins / Q000235:genetics; D009093:Mucus / Q000502:physiology*; D009336:Necrosis; D010738:Type C Phospholipases / Q000096:biosynthesis
D001427:Bacterial Toxins; D002135:Calcium-Binding Proteins; D016207:Cytokines; D009077:Mucins; D010738:Type C Phospholipases; C040649:alpha toxin, Clostridium perfringens