Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens

Abstract

SUMMARYBaseline data from an immuno-epidemiological study of hookworm infection in a rural village in Madang Province, Papua New Guinea are reported. Necator americanus was found to be the commonest helminth infection, with a prevalence of near 100% and intensity of 40 worms per host in adults. Enterobius vermicularis, Ascaris lumbricoides and Trichuris trichiura were also present, at prevalences of 53, 10 and 3% respectively; Ancylostoma duodenale was absent. The frequency distribution of N. americanus was highly over-dispersed, and was well described by a negative binomial distribution with aggregation parameter, k, of 0-370. Intensity of infection was significantly related to host age, but did not differ between the sexes. Haemoglobin levels and haematocrit values were indicative of anaemia in the community, but were unrelated to hookworm infection. Levels of antibodies (IgG, IgA and IgM combined) against adult Necator cuticular collagen and excretory-secretory (ES) products were determined. Serum concentrations of the two types of antibody were significantly correlated with each other. Significant positive correlations were found between anti-ES antibody levels and hookworm egg production, and between anti-collagen antibody levels and host age. It is suggested that the level of anti-collagen antibodies may reflect cumulative exposure to infection, whereas levels of anti-ES antibodies may be more dependent on current worm burden. No evidence was found to suggest that either antibody response is important in regulating parasite population growth. Similarly, the presence of a positive correlation between eosinophil concentration and infection intensity in adults indicates that eosinophilia reflects, rather than determines, the host's worm burden.

Immune Responses in Hookworm Infections

“…Most hookworm L3 cast their outer sheaths on skin penetration (85), but some seem to retain the sheath; antibodies from people infected with N. americanus recognize surface antigens of ensheathed but not exsheathed L3 by immunofluorescence (112). Antibodies have been detected to L3 exsheathing fluid, prompting the suggestion that the cast sheath and associated antigens diverted the immune response away from the potentially vulnerable larval surface (69).…”

“…Various methods have been used to identify these antibody responses, ranging from observation of immunoprecipitates around oral openings (102) to more detailed analyses of Ig subclasses against somatic and excretory/secretory (ES) products by enzyme-linked immunosorbent assay and Western blot analysis (79,80,112).…”

A new approach to morbidity risk assessment in hookworm endemic communities

“…These included studies in Puerto Rico [10]; Australia [11]; Brazil [12,13]; Papua New Guinea [14]; India [15,16]; and Sri Lanka [17].…”

Immunoepidemiology ofWuchereria bancroftiInfection: Parasite Transmission Intensity, Filaria-Specific Antibodies, and Host Immunity in Two East African Communities

“…The first approach was based on univariate statistical methods that essentially attempted to evaluate the effects of one antibody at a time to determine the role that each antibody played independently in regulating Wuchereria infection. This was accomplished via calculation of Pearson partial correlations between infection intensity and antibody variables within five age classes constructed to reflect the age structures of the two study communities (35), with tests for assessing heterogeneity in correlation coefficients between age classes carried out using methods described by Sokal and Rohlf (44). This was followed by an attempt to evaluate all the antibody effects simultaneously to determine their joint contributions to host regulation of worm intensity.…”

“…These studies unambiguously showed that W. bancrofti infection can induce strong antibody responses (4,29,32,42,47), but protective responses have not been conclusively identified yet. Recent theoretical analysis and evidence from other helminth infections (3,9,27,28,35,36) suggest that one reason for this situation in the study of filariasis could be the paucity of studies that have used an immunoepidemiological perspective to investigate the role of acquired immunity in influencing parasitic infection patterns in host communities in areas where the organism is endemic. In particular, this perspective, which attempts to link observed individual host immune responses to epidemiological patterns, has shown how observation of an increasingly negative correlation between the levels of an immune response and the intensities of infection with increasing host age could indicate a protective role for the response being examined (10,27,(48)(49)(50).…”