The Relative Influence of Polyparasitism, Environment, and Host Factors on
Schistosome Infection
Rita de Cássia Ribeiro Silva, Maurício Lima Barreto, Ana Marlúcia Oliveira Assis, Mônica Leila Portela de Santana,
Isabel M. Parraga, Mitermayer Galvão Reis, and Ronald E. Blanton*
School of Nutrition, Federal University of Bahia, Salvador, Bahia, Brazil; Institute of Collective Health, Federal University of Bahia,
Salvador, Bahia, Brazil; Department of Nutrition, Case Western Reserve University, Cleveland, Ohio, USA; Oswaldo Cruz
Foundation, Fiocruz, Salvador, Bahia, Brazil; Center for Global Health and Diseases, Case Western Reserve University,
Cleveland, Ohio, USA
Abstract. Where prevalence of geohelminths and schistosomes is high, co-infections with multiple parasite species
are common. Previous studies have shown that the presence of geohelminths either promotes or is a marker for greater
prevalence and intensity of Schistosoma mansoni infections. Some of this apparent synergy may simply represent shared
conditions for exposure, such as poor sanitation, and may not suggest a direct biologic interaction. We explored this
question in a study of 13,279 school children in Jequié, Bahia, Brazil, with a survey of demographic characteristics and
stool examinations. Cross-sectional analysis revealed a statistically significant increase in the prevalence and intensity of
S. mansoni infection with increasing numbers of geohelminth species (OR 2.5, 95% CI 1.38–3.64). Less than 20% of the
strength of this association was contributed by socioeconomic status or environmental conditions. Thus, polyparasitism
itself, as well as intrinsic host factors, appears to produce greater susceptibility to additional helminth infections.
INTRODUCTION
Among helminth infections, schistosomiasis is considered
one of the most important health problems, not only for its
high prevalence but also for its potential to develop into se-
vere clinical forms precisely at a time of greatest human pro-
ductivity.
1
More than 200 million people are infected with
schistosomes according to the World Health Organization,
and 500–600 million are at risk because of inadequately pro-
tected water supplies and precarious sanitary conditions.
2
In most areas, schistosomiasis is not the only chronic para-
sitic infection found. It is estimated that 26–68% of the indi-
viduals with schistosomiasis are carriers of an additional hel-
minthic infection, such as hookworms, Ascaris lumbricoides,
or Trichuris trichiura.
3
These parasites can aggravate the mor-
bidity due to schistosome infection, especially in young chil-
dren.
4
Various authors have demonstrated a synergism between
simultaneous infection with geohelminths and the burden of
schistosomiasis,
5–8
but whether this effect was the result of
shared environments, host factors, intrinsic parasite biology,
or a combination of these factors is usually not explored. This
study will address the relative contribution of these different
factors by evaluating correlations between prevalence and in-
tensity of Schistosoma mansoni infection and co-infection
with hookworms, A. lumbricoides, and T. trichiura. We fur-
ther evaluated the influence of socioeconomic status and en-
vironmental conditions.
MATERIALS AND METHODS
Population and study area. The study was located in the
city of Jequié, a district center in the southern region of the
state of Bahia, Brazil. The total population of the municipal
district was 120,396 in 1991. This city is situated in one of the
most prosperous districts in the State, and it constitutes an
economic pole of regional attraction for surrounding cities
and rural areas. The Contas River flows through the district.
This river is highly polluted with raw sewage from homes and
businesses present along its banks. It is fed by equally pol-
luted streams flowing from the rest of the city.
In the course of 2 months, some 13,279 individuals 7–17
years of age were examined for intestinal helminths. This
corresponds to 40% of individuals in this age range who were
resident in the city.
Informed consent. Informed consent was obtained for all
study subjects before clinical and parasitologic studies. This
study was approved by the Human Investigation Committees
of University Hospitals of Cleveland and of the Oswaldo Cruz
Foundation, Salvador, Bahia, Brazil. Individuals infected with
intestinal helminths were treated with albendazole, and indi-
viduals infected with S. mansoni were treated with oxam-
niquine at WHO-recommended doses.
Stool examination. The collection of stool samples was car-
ried out by house-to-house distribution of lidded plastic con-
tainers that were collected on the following day. The Kato–
Katz quantitative stool exam,
9
carried out by laboratory staff
trained by the National Health Foundation (FNS), was used
to determine parasite species and intensity of infection. Iden-
tification of hookworm eggs was performed 2 hours after pre-
paring the slides. Quality control for the stool examinations
was carried out by a technician hired independently for this
job who re-examined 10% of all slides.
Index of socioeconomic and environmental conditions. An
indicator of the environmental and household conditions was
constructed from demographic information obtained by inter-
views with childcare providers. A questionnaire was admin-
istered for a sample of 1,766 schoolchildren infected with a
low or moderate intensity of at least 1 species of helminth.
The sample was obtained in areas of the city with the highest
prevalence of S. mansoni infections. Variables describing
household conditions and sanitation were dichotomized as
favorable (0) or unfavorable (1) and tested for statistically
significant associations with the presence or absence of ane-
mia in a logistic regression model. Those that remained sig-
nificant (P < 0.05) were included in the index (Table 1). Thir-
teen variables were found to be significant, and the sum of
* Address correspondence to Ronald Blanton, Center for Global
Health and Diseases, 2103 Cornell Road, Case Western Reserve Uni-
versity, Cleveland, OH. E-mail: reb6@case.edu
Am. J. Trop. Med. Hyg., 77(4), 2007, pp. 672–675
Copyright © 2007 by The American Society of Tropical Medicine and Hygiene
672