Maternal transmission of immunity to Eimeria maxima: enzyme-linked immunosorbent assay analysis of protective antibodies induced by infection

Abstract

Vaccination of broiler chickens against Eimeria infection is problematic because of the need to ensure that birds are protected from the time of hatching. We have therefore investigated the feasibility of protecting hatchling broilers via maternal transfer of protective antibodies from hens to their offspring. Oral infection of broiler breeder hens with 20,000 sporulated Eimeria maxima oocysts caused production of antibodies which were passed into the egg yolk and subsequently to hatchlings. The level of specific antibodies in the yolks to unsporulated oocysts, sporulated oocysts, merozoites, and gametocytes was assessed by enzyme-linked immunosorbent assays. The levels in yolks of antibodies to all developmental stages peaked 3 to 4 weeks after infection of the hens. Groups of 10 hatchlings were challenged at 3 days of age by oral infection with 100 sporulated E. maxima oocysts. In the first experiment, the mean 4-day (days 6 to 9 post-infection) total number of oocysts excreted in the feces of chicks from eggs collected 3 weeks after infection of the hens was (0.6 +/- 0.4) x 10(6) (mean +/- standard error) compared with (9.9 +/- 1.4) x 10(6) for the progeny of uninfected hens, which represents a greater than 90% reduction. However, oocyst excretion by chicks from eggs collected 7 or 8 weeks after infection of the hens was only 47 or 68% lower than control values, reflecting declining levels of protective antibodies. In a second experiment, in which the hens were somewhat older and pretreated by intramuscular injection of saline in the emulsifying agent, Arlacel A, the period for which protective antibodies were transferred to hatchlings was prolonged. Thus, oocyst excretion by challenged hatchlings from eggs collected for an 8-week period after infection of the hens was more than 90% lower than oocyst excretion by control chicks, and even hatchlings of eggs collected 19 weeks after infection of the hens showed a 60% reduction in oocyst output. In both experiments, the levels of immunoglobulin G (IgG) antibodies to all developmental stages in yolks or hatchling sera were very strongly correlated with maternally derived immunity to E. maxima. In contrast, parasite-specific IgM or IgA was not detectable, either in egg yolk or egg white. These results demonstrate the ability of IgG antibodies to protect against E. maxima in poultry, thus raising the possibility of using protective maternally derived IgG antibodies to identify potentially protective parasite antigens and indicating the feasibility of using maternal immunization as a means for parasite control.

Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica)

“…Females also transfer immunoglobulins to eggs, and they serve to confer protective immunity to the offspring in the critical posthatching period, when their immune system is immature (e.g. Naqi et al, 1983;Smith et al, 1994;Ahmad & Siddique, 1998;Gasparini et al, 2000;Buechler et al, 2002;Saino et al, 2003). Decline of immune response with age may therefore reflect this specific kind of cost entailed by reproduction, an interpretation which is corroborated by the lack of age effect on primary immune response in males and a smaller secondary immune response, that was measured after first clutch completion, in females compared with males.…”

Maternal immunoglobulin concentration in Collared Flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order

“…The transfer of maternally derived antibodies is assumed to be highly beneficial, since it reduces the susceptibility of nestlings to local diseases and pathogens by allowing them to apply a highly specific and efficient acquired immune defence even at the first encounter with a pathogen (Fadly & Nazerian 1989;Graczyk et al . 1994;Smith et al . 1994;Gasparini et al .…”

“…2003). Furthermore, several other factors may affect the immunoglobulin transfer to the eggs, such as the age (Barua, Yoshimura, & Tamura 1998) and health of the mother (Smith et al . 1994;Gasparini et al .…”

Immunity, growth and begging behaviour of nestling Barn Swallows Hirundo rustica in relation to hatching order

“…Consideration of immunity as a crucial component of offspring fitness soon after hatching is therefore likely to be of pivotal importance in studies of avian breeding ecology, although poorly investigated to date. In particular, a neglected aspect of field studies on birds is that females can deliver immunoglobulins to their offspring via the egg, which may confer protection against parasites during crucial life stages following hatching (Naqui et al 1983, Tizard 1991, Smith et al 1994a, b, Kaspers et al 1996, Ahmad and Siddique 1998, Pastoret et al 1998, Saino et al 2001.…”