© 2008 The Authors 293
Journal compilation © 2008 Blackwell Publishing Ltd
Parasite Immunology , 2008, 30, 293–303 DOI: 10.1111/j.1365-3024.2008.01023.x
Blackwell Publishing Ltd ORIGINAL ARTICLES Mucosal antibodies in hookworm infection
Mucosal antibody responses in experimental hookworm infection
R. D. BUNGIRO JR,
1
T. SUN,
1
L. M. HARRISON,
1
C. B. SHOEMAKER
2
& M. CAPPELLO
1
1
Program in International Child Health, Departments of Pediatrics and Epidemiology and Public Health, Yale University School of Medicine,
New Haven, CT 06520, USA,
2
Department of Biomedical Sciences, Tufts Cummings School of Veterinary Medicine, North Grafton,
MA 01536, USA
SUMMARY
Hookworms are bloodfeeding nematodes that reside in the
intestinal mucosa. These parasites secrete proteins that induce
robust systemic immune responses in humans and experimental
animals. By contrast, mucosal immune responses in and
around the site of attachment are not described as well. This
paper presents data from studies aimed at examining hookworm-
specific mucosal antibody responses in a hamster model of
Ancylostoma ceylanicum infection. Intestinal flush prepared
from infected hamsters was analysed by ELISA and shown to
be enriched in IgA-specific for A. ceylanicum excretory–
secretory (ES) products. Evaluation of mucosal IgA responses
by immunoblot demonstrated that infected hamsters recognized
a broad range of ES proteins. Hamsters repeatedly exposed to
drug-terminated infections were shown to have enhanced
serum IgG and mucosal IgA responses, as well as a high level
of protection from challenge infection. Parasite-specific IgA
was also detected in the faeces of hamsters undergoing a
primary infection, and increasing faecal IgA responses were
coincident with significant reductions in intestinal worm
burdens and faecal ES output over time. Together these results
suggest that secretory IgA may act in concert with other
components of the mucosal and systemic immune response to
promote protective immunity against hookworm infection and/
or disease.
Keywords Ancylostoma ceylanicum, hamster, hookworm,
IgA, mucosal immunity
INTRODUCTION
Hundreds of millions of persons worldwide continue to
harbour hookworm infections (1). These bloodfeeding soil
transmitted nematodes are a major cause of anaemia and
malnutrition, and as such rank among the foremost agents
of global morbidity (2), especially among children and women
of childbearing age (3–6). It has been suggested that the
immunomodulatory influence of hookworms and other
helminth infections may exacerbate the clinical course of
globally significant infectious diseases such as tuberculosis
and HIV-AIDS, and also reduce the efficacy of vaccines (7–10).
Although effective anthelminthic agents for hookworm are
available, rapid reinfection (11,12), and the possibility of
emerging drug resistance (13), suggest that existing control
methods may become less effective in the future. Consequently
new strategies to control hookworm disease, such as vaccines
(14) and novel therapeutics (15) are needed to augment
currently available control options. Such efforts will be aided
by a thorough understanding of host immune response pheno-
types that are germane to protection and susceptibility.
The immune response to hookworms has been the subject
of numerous studies in both humans and animals (as reviewed
in Refs (16–18)), with considerable attention focusing on
the Syrian golden hamster (Mesocricetus auratus) model of
Ancylostoma ceylanicum infection. In contrast to mice, which
do not permit the development of Ancylostoma spp. hook-
worms upon larval infection (19,20) and do not support
extended parasite survival following adoptive transfer of
adult worms (21), immunocompetent hamsters are fully
permissive hosts for A. ceylanicum (22,23). Furthermore,
when infected with a sublethal dose of A. ceylanicum larvae,
weanling hamsters exhibit the delayed growth and anaemia
which typify human disease (24–26). These findings, coupled
with the inherent advantages of rodent models as compared
to larger species, have made the hamster model of A. ceylanicum
infection ideal for studies of hookworm pathogenesis and
vaccine development (24,27–36). A limitation of the hamster
model, however, has been the relative paucity of commercially
available immunological reagents, which has hampered the
detailed study of immune responses in this species (16).
Correspondence: Richard D. Bungiro Jr., Yale Child Health
Research Center, 464 Congress Avenue, New Haven, CT 06520,
USA (e-mail: richard.bungiro@yale.edu).
Received: 29 October 2007
Accepted for publication: 4 February 2008