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Hyperendemic human and porcine Taenia solium

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Am. J. Trop. Med. Hyg., 68(3), 2003, pp. 268–275
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

HYPERENDEMIC HUMAN AND PORCINE TAENIA SOLIUM INFECTION IN PERÚ

HÉCTOR H. GARCÍA, ROBERT H. GILMAN, ARMANDO E. GONZALEZ, MANUELA VERASTEGUI,
SILVIA RODRIGUEZ, CESAR GAVIDIA, VICTOR C. W. TSANG, NESTOR FALCON, ANDRES G. LESCANO,
LAWRENCE H. MOULTON, TERESA BERNAL, MARCO TOVAR, AND THE CYSTICERCOSIS WORKING GROUP
IN PERÚ*
Departments of Microbiology and Pathology, Universidad Peruana Cayetano Heredia, Lima, Perú; Department of Transmissible
Diseases, Instituto Nacional de Ciencias Neurologicas, Lima, Perú; Departments of International Health and Biostatistics, Johns
Hopkins University School of Hygiene and Public Health, Baltimore; Asociacion Benefica PRISMA, Lima, Perú; School of
Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Perú; Parasitic Diseases Branch, Centers for Disease
Control and Prevention, Atlanta.

Abstract. The prevalence and characteristics of human taeniasis/cysticercosis and porcine cysticercosis were assessed
in an endemic area of the Peruvian highlands. Individuals from 10 communities had stool examinations (N ⳱ 2,951) and
serologic testing for Taenia solium antibodies (N ⳱ 2,583). The total porcine population present (N ⳱ 703) was also
examined by serology. Cysticercosis is hyperendemic in this area and is associated with an important number of seizure
cases. Human seroprevalence by village ranged from 7.1–26.9% (mean, 13.9%). Seroprevalence was higher among
individuals with a history of seizures but not in those reporting a history of headache or intestinal taeniasis. Prevalence
of taeniasis ranged from 0–6.7% (median, 2.5%). Coproantigen detection found 2.4 times more taeniasis cases than did
microscopy (direct and after concentration). Age distribution for taeniasis showed a peak at younger ages than for
seroprevalence. Porcine seroprevalence ranged from 42–75%. Random effects logistic regression models for human
seropositivity demonstrated both in-house clustering of cases and a large increase in risk associated with a tapeworm
carrier in the house. Besides confirming the close relationship between taeniasis and cysticercosis cases, this large-scale
field study demonstrated early age of tapeworm and cysticercosis infections in humans, and short duration of taeniasis
infections.

INTRODUCTION formed in a single selected endemic village and thus cannot be

Neurocysticercosis 1(NCC), the infection of the human cen-
tral nervous system by Taenia solium larvae, is an important
contributor to neurologic morbidity in developing countries1
and presumably is the major cause of acquired epilepsy in the
world.2 It also is increasingly diagnosed in industrialized
countries because of immigration from endemic areas, with
over 1,000 cases per year in the United States.3 The life cycle
of this zoonotic cestode includes the pig as the normal inter-
mediate host (harboring the larval vesicles or cysticerci), and
humans as the definitive host (harboring the adult form or
tapeworm). Humans also can be accidental intermediate
hosts and develop the larval stage of the disease by accidental
ingestion of T. solium eggs.3,4 Porcine cysticercosis is an im-
portant cause of economic losses in developing countries.5–7
In most developing countries, the cycle of T. solium be-
tween pigs and humans is sustained because of the coexist-
ence of poor sanitary conditions and domestic pig raising
without veterinary control or surveillance systems.6,7 Despite
multiple field epidemiologic studies in recent years,7–33 basic
data still are missing, especially regarding the interrelation-
ship between human tapeworm infections, porcine cysticer-
cosis, and human cysticercosis, and whether this relationship
varies in different conditions of endemicity.34
Although taeniasis/cysticercosis has been included in a
short list of diseases considered to be eradicable in the short
term,28,35 no sustainable eradication has been achieved.
Whereas endemic taeniasis/cysticercosis occurs in very differ-
ent scenarios (highlands, tropics, arid coast, etc.), and at dif-
ferent intensities of prevalence, most field studies are per-
* Other members of the Cysticercosis Working Group in Perú are H.
Mayta, J. Jimenez, P. Castillo (Universidad Peruana Cayetano
Heredia, Lima, Perú); M. Martinez (Instituto Nacional de Ciencias
Neurologicas, Lima, Perú); C .A. W. Evans (Cambridge University,
England).
268
extrapolated to regional or country settings. The transmission
dynamics of T. solium need to be better understood to design
a rational control program that can be applied in various
settings. As part of an interventional study on the control of
T. solium, we used the best available diagnostic tools (en-
zyme-linked immunoelectro transfer blot [EITB] assay for
the detection of anti-cysticercus antibodies36,37 and coproan-
tigen detection by enzyme-linked immunosorbent assay
[ELISA]21,38) in a large-scale, comprehensive, cross-sectional
survey in a wide area of the Peruvian highlands to quantify
baseline infection parameters for human taeniasis and human
and porcine cysticercosis.
MATERIALS AND METHODS
Study site. The central highlands area of Perú was selected
because of demonstrated endemicity7 and accessibility by
road. The area is cold and has at least two clearly defined
seasons: dry from June to November, and rainy from Decem-
ber to May. Paved access highways are passable all year, al-
though secondary roads may not be used during the rainy
season. A preliminary trip was made to select an adequate
study area on the basis of accessibility and the willingness of
communities to cooperate in a longitudinal project on the
control of porcine cysticercosis. In this trip, several villages
less than 50 miles from Huancayo (population 300,000), the
main city in the department, were inspected. Communities
near Huancayo were selected because of the convenience of a
city-based location for specimen-handling, centrifugation, and
storage.
Nine villages of the Quilcas district, located 12 miles west
from Huancayo at altitudes of 3,200–3,600 meters above the
sea level, were selected for the study. They were Veintisiete
de Mayo, Santa Cruz, Pampas, Llacta, Colpar, Rangra, Casa-
cancha, Progreso, and Centro. Canchayllo, a village in an-
 HYPERENDEMIC T. SOLIUM IN PERÚ
other district, also was included to increase sample size (Fig-
ure 1). The houses in these villages are adobe and have no
sanitation facilities (10–50% have latrines). Most of the vil-
lages also lack potable water or electricity. After the study
communities were chosen, a second visit was made to meet
key village leaders to evaluate their interest in the project and
willingness to participate. Census and mapping were initiated
after the leaders consulted the communities and confirmed
their consent. Before starting the project, the field personnel
gave several talks to groups of villagers about the project and
the disease. During these talks, villagers identified the pres-
ence of intestinal parasites as one of their principal health
concerns; thus, free detection and treatment of geohelminthi-
asis was offered as part of the study. Human and veterinary
medical attention, including animal vaccinations for porcine
hog cholera, also were offered free during each field trip.
Data collection. The census form for villagers included
identification (last name, first name, age, sex) and simple,
direct questions in local terms about a history of passing tape-
worm proglottids, headaches, or seizures. The questionnaire
was applied to all individuals present, including children, and
the head of the family gave information about members who
were absent. An individual who slept two or more nights each
week in a village was considered as living there. The cross-
sectional sampling of humans and pigs for the study was per-
formed from March–May 1996.
Samples. Approximately 5 mL of venous blood was drawn
by venipuncture from all consenting villagers age 5 or older.
Some samples were taken from children younger than 5 at
their parents’ request. Samples were centrifuged in Huancayo
the same day, coded with consecutive numbers according to
the collection lists, aliquoted in two sets of 1.5-mL vials,
stored at −4°C, and sent frozen to a laboratory in Lima (Labo-
FIGURE 1. Study area and village distribution.
269
ratorio de Patologia, Universidad Peruana Cayetano
Heredia) to be assayed by EITB.
Stool samples were collected from all consenting individu-
als in disposable 500 mL plastic boxes. When the collection
materials for stool samples were distributed, villagers were
carefully instructed about adequate hygiene to avoid contami-
nation, and were given toilet paper and soap.
Pig sampling. All pigs in the village (excluding pregnant
sows to avoid the risk of miscarriage, and piglets less than 2
months old) were identified and ear-tagged with consecutive
numbers. The age of the pigs was established by asking the
owner and corroborated using conventional teeth-eruption
indicators in young animals.39–41 At the same time, a 5-mL
blood sample was taken from the pig’s cava vein using
vacuum tubes. Samples were processed as described above
for human serum. All pigs were vaccinated against hog chol-
era.
Processing. Serum samples were processed by EITB as
originally described.36 In brief, this assay uses a semipurified
fraction that contains seven T. solium glycoprotein antigens
(diagnostic bands GP50, GP42-39, GP24, GP21, GP18, GP14,
and GP13, the number indicating the respective molecular
weight in kDa) in an immunoblot format to detect infection-
specific antibodies. Reactions to at least one band are con-
sidered positive. After a macroscopic examination for worms
or proglottids in the field, stool samples were sent to the
reference laboratory in Lima and examined by both direct
microscopy and a concentration (sedimentation) method.42
No further efforts at species identification were made. Indi-
viduals with a positive parasitologic examination were revis-
ited at the end of the study and offered antiparasitic treat-
ment. Stool samples were also examined by coproantigen de-
tection ELISA, as originally described.21,38 This assay has a
270
FIGURE 2. Sampling coverage for blood and stools (total residents
in the study area, N ⳱ 5,658). Huancayo, Perú, 1996.
reported sensitivity of 87.5% and a specificity of 96%.43 Co-
proparasitologic and coproantigen assays were performed
with samples taken at different times.
Data management and analysis. Databases were analyzed
using Stata 6.0 (Stata Corp., College Station, TX, 1999). Di-
rect age and sex standardization was used to compare preva-
lences among villages. Associations among categorical vari-
ables were tested by ␹2 or Fisher’s exact test, and among
continuous variables by Student’s t test. Bivariate correlations
were tested using Spearman’s rho. A series of random effects
logistic regression models was fitted to evaluate the presence
of in-house clustering of seropositive cases (by estimating the
cluster-level variance as a proportion of the total variance)
and the contribution of selected covariates. All confidence
intervals (CIs) are at the 95% level.
The study was approved by the institutional review boards
of the Johns Hopkins Bloomberg School of Public Health, the
Centers for Disease Control and Prevention, and the Univer-
sidad Peruana Cayetano Heredia.
RESULTS
Population and sampling. The total population resident in
the study area at the time of the survey was 5,658 individuals,
2,696 males (47.6%), and 2,962 females. Mean age (SD) was
24.51 (20.82) years, range 0 to 99. Age distribution was typical
of rural areas in developing countries, with predominance of
younger age groups.
Blood sampling. Blood samples were obtained from 2,545
of 4,850 residents age 5 or older (mean sampling coverage
52.5%, Figure 2), and 38 children younger than 5.
TABLE 1
Characteristics of the population according to whether they were sampled for blood, collected stool samples, or both (all residents, n ⳱ 5658).
Huancayo, Perú, 1996
Both samples
(n ⳱ 1,749)
Male 710 (40.6%)*
Mean age (SD) 25.2 (19.7)
History of taeniasis 179/1,749 (10.2%)*
History of headache 244/1,749 (14.0%)*
History of seizures 43/1,749 (2.5%)
* P < 0.001, ** P ⳱ 0.057, *** P ⳱ 0.015, or **** P ⳱ 0.052, compared with the not-sampled group
GARCÍA AND OTHERS
Stool sampling. Stool samples were collected from 2,607
residents age 5 or older (53.7%) and 345 children under 5 who
were not in the original sampling frame. Most people who had
blood samples taken (1,749, 68%) also provided stool
samples.
Unsampled individuals. Individuals who did not have a
blood sample taken were more frequently male, reflecting
lower presence or cooperation in male adults. (Data not
shown.) Those who did not provide stool samples were older,
and similar to the blood sampling, most of them were male. In
general, individuals who were not sampled for blood or did
not turn in stool samples were less prone to have a history of
headaches, seizures, or having passed proglottids (Table 1).
One-third of the population (1,873, 33.1%) was not sampled
for blood and did not turn in stool samples.
Serology. Three hundred fifty-five individuals age 5 or
older were seropositive to cysticercosis (13.7%). In the whole
study population, seroprevalence was similar for males and
females, with an early increase at age 10, a later decrease, and
a rise again to a higher peak at age 40–60 (Figure 3). Children
younger than 5 had lower seroprevalence (2/38, 5.3%; odds
ratio [OR] 0.34; P ⳱ 0.196). The only two seropositive chil-
dren in this group were 4 years old.
Human seroprevalence per village ranged from 7.1% in
Canchayllo to 26.9% in 27 Veintisiete de Mayo (Table 2).
Seroprevalence increased with age in the two villages with
lower prevalence levels, but all others showed homogeneous
hyperendemicity levels across age groups. (Data not shown.)
Distribution of seroprevalence by sex was extremely variable
among villages. We observed a trend for higher human sero-
prevalence in villages farther from the main road (Spearman’s
rho 0.48, P ⳱ 0.18). This trend was more evident in relation
to porcine seroprevalence (Spearman’s rho 0.597, P ⳱ 0.090).
Taeniasis—parasitology. Baseline pretreatment stool
samples were collected from 1,317 individuals. No proglottids
were found at macroscopic examination, but eight cases had
Taenia sp eggs detected by microscopy (0.6%). Post-
treatment stool samples were collected from 2,471 individuals
(836 individuals provided both pretreatment and post-
treatment samples). Taenia proglottids were found in post-
treatment samples of 13 individuals, and Taenia eggs were
detected by microscopy in 21 cases (0.8%). More taeniasis
cases were detected in the intervention (praziquantel-treated)
than in the comparison (pyrantel-treated) areas, although the
proportions were not significantly different (17/1,626 ⳱ 1.0%
versus 4/845 ⳱ 0.5%; OR 2.22; P ⳱ 0.142). Prevalence of tae-
niasis by microscopy in the study villages ranged from 0–1.9%.
Taeniasis—coproantigen detection. Coproantigen detec-
tion ELISA was performed in post-treatment stool samples
Only stool samples Only blood samples Not sampled
(n ⳱ 1,203) (n ⳱ 834) (n ⳱ 1,872)
562 (46.8%)* 426 (51.1%) 998 (53.3%)
22.9 (22.7)** 25.2 (17.7) 24.4 (21.8)
80/1,200 (6.7%)* 39/833 (4.7%) 59/1,832 (3.2%)
95/1,200 (7.9%) 85/833 (10.2%)*** 134/1,832 (7.3%)
33/1,200 (2.8%) 28/834 (3.4%)**** 37/1,832 (2.0%)
 HYPERENDEMIC T. SOLIUM IN PERÚ 271

FIGURE 3. Age-stratified prevalence of serum antibodies to Taenia solium and intestinal taeniasis by either coproantigen or microscopy.
Huancayo, Perú, 1996.

from 1,620 individuals, almost all of them (1,611) from the
intervention areas. Forty-five (2.8%) were positive. Only 17
of 45 (37.8%) also were positive in microscopy. In general,
coproantigen-positive individuals were younger than those
who tested negative (mean age 19.6 [SD 20.6] and median 9
years versus mean 24.5 years [SD 20.8] and median 16 years),
although the difference did not reach statistical significance
(P ⳱ 0.12). However, most coproantigen-positive individuals
were 10 years old or younger, with a significantly higher
prevalence in this age group (23/595, 3.9%, versus 22/1,025,
2.1%, OR 1.83, P ⳱ 0.042). Prevalence of taeniasis by co-
proantigen detection in the study villages tested ranged from
0–6.7%.
In four cases, taeniasis was diagnosed by other means, but
coproantigen testing was negative: One person was positive
for Taenia eggs at microscopy, and proglottids were seen
post-treatment; two were positive for eggs only by micros-
copy, and in one, proglottids were reported post-treatment,
but microscopy was negative.
TABLE 2
Prevalence of serum antibodies to Taenia solium in human and por-
cine populations, and human taeniasis infection. Huancayo,
Perú, 1996
Human cysticercosis Porcine cysticercosis
Village (seroprevalence) (seroprevalence)
Porcine seroprevalence. Porcine seroprevalences ranged
from 42.3–75.0% (total prevalence 62.4%), and increased
monotonically with age (Table 3). There were no differences
in seroprevalences between male and female pigs.
Human versus porcine seroprevalence at village level. There
was a statistically significant positive correlation between hu-
man and porcine seroprevalence for each village (Spearman’s
rho 0.799, P ⳱ 0.006) that persisted after direct standardiza-
tion by age and sex. Significant positive correlations also ex-
isted between porcine seroprevalence and human taeniasis by
coproantigen (Spearman’s rho 0.866, P ⳱ 0.005) and between
human seroprevalence and taeniasis prevalence by coproan-
tigen detection (Spearman’s rho 0.800, P ⳱ 0.017) (Figure 4).
Factors related to seropositivity: Neurologic symptoms. Se-
roprevalence was higher among individuals with a history of
seizures (16/71, 22.5% versus 339/2,512, 13.5%; OR 1.86; 95%
CI ⳱ 1.01, 3.39; P ⳱ 0.029 − ␹2 test, 40.1% attributable risk
in exposed individuals44) but not in those who had a history of
headache (51/329, 15.5% versus 304/2,253, 13.5%; OR 1.18;
CI ⳱ 0.84, 1.64; P ⳱ 0.323). Seizure complaints were more
frequent in older people, particularly in seropositive individu-
als (Figure 5). The association between a history of seizures
and a positive EITB was stronger in individuals older than 40
(8/87, 9.2% versus 15/451, 3.3%; OR 2.94; CI ⳱ 1.10, 7.70;
P ⳱ 0.021, 63.8% attributable risk in seropositive individuals).
Human taeniasis
(coproantigen)

Canchayllo 33/474 (7.0%) 30/71 (42.3%) 1/217 (0.5%) TABLE 3

Colpar 13/174 (7.5%) 31/48 (64.6%) Not done* Porcine seroprevalence by age groups. Huancayo, Perú, 1996
Centro 19/198 (9.6%) 24/52 (46.2%) 0/97 (0%)
Progreso 26/254 (10.2%) 21/42 (50.0%) 0/94 (0%) Age group (months) Seroprevalence
Llacta 27/201 (13.4%) 57/78 (73.1%) 9/259 (3.5%)
Pampa 53/419 (12.6%) 51/102 (50.0%) 0/164 (0%) 2–4 94/201 (46.8%)
Santa Cruz 56/372 (15.1%) 47/66 (71.2%) 10/339 (2.9%) 5–6 65/114 (57.0%)
27 de Mayo 74/275 (26.9%) 78/104 (75.0%) 19/279 (6.8%) 7–8 75/122 (61.5%)
Rangra 29/113 (25.7%) 28/43 (65.1%) Not done 9–10 52/79 (72.2%)
Casacancha 25/103 (24.3%) 72/97 (74.2%) 6/170 (3.5%) 11–12 72/93 (77.4%)
Total 355/2,583 (13.7%) 439/703 (62.4%) 45/1,619 (2.8%) > 12 76/94 (80.9%)
Total 439/703 (62.4%)
* One negative sample corresponding to a resident of Colpar is not included.
272 GARCÍA AND OTHERS

FIGURE 4. Prevalence of human and porcine cysticercosis infection and human intestinal taeniasis by village. Huancayo, Perú, 1996.

Seizures were reported in 4.5% (16/355) of seropositive and
2.5% (55/2,228) of seronegative individuals, corresponding to
a population attributable risk of 10% of all seizures related to
cysticercosis seropositivity.44
History of having passed proglottids. Seroprevalence
among individuals with a history of having passed proglottids
was similar to that in individuals without such antecedent
(36/218 versus 319/2,364; OR 1.27; CI ⳱ 0.85, 1.88; P ⳱ 0.22).
This lack of association led to further analysis of this variable.
We observed increased odds for seropositivity related to a
history of passing proglottids in individuals younger than 25
(OR 2.76; CI 1.82, 4.08; P < 0.001) but not in older subjects
(OR 0.66; CI 0.21, 2.08; P ⳱ 0.779).
Current intestinal taeniasis. There were 917 individuals who
had both serum samples taken and post-treatment stool
samples processed by microscopy and coproantigen detec-
tion. A comparative analysis was performed in this subgroup
to evaluate the association between intestinal taeniasis and
seropositivity to EITB. Most Taenia carriers in this group
(23/30) were seropositive, including all seven cases with pro-
glottids seen at macroscopical examination, 14 of 16 cases
with Taenia eggs at microscopy (87.5%), and 22 of 28 cases
with positive coproantigen examination (78.6%). Five of the
seven seronegative taeniasis cases corresponded to coproan-
tigen-positive individuals with negative parasitologic results
(microscopy and macroscopic examination). After excluding
the tapeworm carriers, the association between a positive
EITB and living in a house with a Taenia carrier was exam-

FIGURE 5. Age-stratified prevalence of seizures in individuals seropositive and seronegative to Taenia solium. Huancayo, Perú, 1996.
 HYPERENDEMIC T. SOLIUM IN PERÚ
ined in this same subgroup (N ⳱ 887). Forty percent of in-
dividuals living in a house with a tapeworm carrier were se-
ropositive, compared with 13% of individuals in houses where
no tapeworms were detected (22/55, 40.0% versus 111/832,
13.3%; OR 4.33; CI ⳱ 2.34, 7.98; P < 0.001).
Other risk factors associated with seropositivity. Raising
pigs, irrespective of the number, was associated with being
seropositive (232/1,562, 14.9% versus 123/1,021, 12.0%; OR
1.27; CI 1.01, 1.61; P ⳱ 0.043). A similar association existed
between having infected pigs and being seropositive (190/
1,224, 15.5% versus 165/1,359, 12.1%; OR 1.33; CI 1.06, 1.66;
P ⳱ 0.013). Age, sex, the number of people living in the
house, and having a history of passing proglottids were not
associated with positive EITB in bivariate analysis. Using ran-
dom effects logistic regression (RELR) models for seroposi-
tivity, raising pigs, and having seropositive pigs failed to sig-
nificantly increase the explained deviance according to the
likelihood-ratio test (LRT). We also tested interaction terms
between the presence of tapeworm carriers and pig raising as
well as having seropositive pigs, failing to observe significant
effect modification. The maximum amount of deviance was
explained by considering the presence of a tapeworm carrier
in the house and fitting dummy variables for the seropreva-
lence levels, although a large amount of the variability still
remained unexplained in this model.
Household clustering of cases seropositive for cysticercosis.
Using a RELR model, we confirmed the presence of cluster-
ing at the household level both before and after considering
the presence of tapeworm carriers in the house. Cluster-level
effects explained highly significant amounts of the total vari-
ance in each case, 63.4 and 52.1%, respectively (P < 0.001 for
both cases, LRT). Significant differences were observed be-
tween odds ratios estimated at the cluster level and the
pooled estimates. The clustering effects remained significant
when fitting individual models for groups of communities
with different seroprevalence levels (high > 20%, intermedi-
ate 10–20%, and low < 10%). Less clustering was observed in
communities with high seroprevalence. The percentage of the
variance accounted for by clustering in those communities
was only 32.5%, while it exceeded 50% in communities with
intermediate and low seroprevalence.
Clustering of seropositive cases around tapeworm carriers.
Most tapeworm carriers were seropositive (22/28, 78.6% of
coproantigen-positive individuals) while their household con-
tacts had a rate 3.4 times higher than individuals living in
households with no tapeworm carriers (45/112, 40.1% versus
288/2,443, 11.8%; P < 0.001). RELR models showed that the
presence of a tapeworm carrier was significantly associated
with higher rates of seropositive cases in the house (OR, 9.21;
CI 5.38, 15.76; P < 0.001, LRT) after taking into account
clustering of cases within the household. In all analyses by
prevalence levels, clustering around carriers remained highly
significant (P < 0.005, LRT). Communities with higher rates
showed less clustering around carriers (OR 5.43) than com-
munities with intermediate and lower prevalence rates (OR
7.31 and OR 14.11, respectively).
DISCUSSION
This comprehensive, large-scale study demonstrates the hy-
perendemicity of Taenia solium infection in a widespread
area of the Peruvian central highlands. Most residents in 10
273
typical villages had either serology or stool examination per-
formed, and an important proportion of them had both. All
study villages showed human seroprevalences of antibodies to
T. solium above 7%, reaching 25% in three of the 10 com-
munities. Impressively, porcine seroprevalences were all
above 40%, reaching 75% in two villages, and there was a
strong correlation between human and porcine seropreva-
lence by village. As opposed to most epidemiologic studies in
taeniasis/cysticercosis (performed in one or two selected vil-
lages), this study looked at all villages in a district to provide
a comprehensive overview of the situation in the area.
The study also has estimated the extent of in-house clus-
tering of cases, as well as the high risk involved for both
tapeworm carriers and their household contacts. Marked clus-
tering occurs despite the high background seroprevalence,
largely in houses with tapeworm carriers. Given the ultimate
goal of controlling or eradicating transmission, identifying
and characterizing the sources of infection is crucial. The cu-
mulative effect of a tapeworm carrier in in-house transmission
will depend on the duration of the infection. In this series, the
age-prevalence curve of intestinal taeniasis peaks at an earlier
age than do human cysticercosis antibodies. This would not
support the classic theories of a long tapeworm life span of 20
years and corroborates recent studies in Guatemala18,22,23
which suggested that the life span is much shorter than sus-
pected, probably below 5 years in most cases. Symptomatic
neurocysticercosis is known to appear years after exposure.45
Recent data have shown that the frequency of taeniasis in
patients with neurocysticercosis may reach 15%, and that pa-
tients with more cerebral cysticerci have a higher probability
of carrying a tapeworm at the time of diagnosis.46,47 We pos-
tulate that many seropositive individuals, including many
NCC patients, once were tapeworm carriers (i.e., that auto-
infection plays a much more important role in NCC than
previously suspected) or household contacts.
The coproantigen-detection test consistently detected two
times more tapeworm carriers than microscopy alone did.
Thus, microscopy underestimates the real prevalence of tae-
niasis and would be a poor monitoring tool for control pur-
poses. Almost all tapeworm carriers in this area were EITB
positive, whether they were diagnosed by microscopy or co-
proantigen detection. However, it is not clear whether intes-
tinal taeniasis leads to antibody formation by itself, being a
different stage of the same species, or whether the antibodies
represent contamination of the carrier with Taenia eggs from
its own source by external autoinfection. In young individuals,
there was a significant association between T. solium antibod-
ies and a history of having passed proglottids, but this effect
disappears at older ages. This can be explained by young age
of infection, short life span of the tapeworm, and later sero-
conversion to negative (transient seropositive cases).48 Short-
lived intestinal tapeworm infections at younger ages can help
explain the early peak in the bimodal seroprevalence curve in
the human population.
It has been suggested that pigs get infected only at early
ages.49 In this study, however, porcine seroprevalence in-
creased monotonically with the age of the animal. This may
indicate either that older animals are as susceptible as
younger pigs or that some pigs are protected through the
initial exposure period, perhaps via maternal transfer of an-
tibodies, but become susceptible later. Maternal antibodies
are protective for other larval cestode infections34 and have
274 GARCÍA AND OTHERS
been shown to slowly decrease in piglets born to cysticercosis-
infected sows.50
The prevalence of individuals complaining of seizures (30/
1,000) was somewhat higher than expected for developing
countries.51 These individuals had almost twice the sero-
prevalence as individuals who did not complain of seizures.
Even though the simple questionnaire that we used may have
resulted in non-specific or false-positive answers, a strong as-
sociation between seizures and seropositivity to T. solium was
found in this study. The estimate of 10.2% for population-
attributable risk of seizures due to cysticercosis is most likely
an extremely conservative estimate. Only calcified brain cys-
ticerci are found in over half the cases of symptomatic
NCC,52–54 as in almost all asymptomatic individuals examined
by neuroimaging in endemic villages.20,26,27 All these NCC
cases may have become seronegative over time. Another
group of cases with a single viable or degenerating parasite
also may be seronegative.55 Thus, some—or many—seizures
in seronegative individuals also will result from cysticercosis.
The high frequency of individuals with seizures in older age
strata in this population and its strong association with serum
antibodies to T. solium probably reflect the cumulative effect
of infections that occurred some time ago but only become
clinically manifest years later. A history of headache was
three times more frequent in women than men, as expected
for general population.56 Probably because of the low speci-
ficity of the symptom, there was no association between com-
plaining of headache and seropositivity.
Taeniasis/cysticercosis is an important public health prob-
lem in endemic areas, as demonstrated by its hyperendemic
conditions in the study area and the association between se-
ropositivity and seizures. While improvements in sanitation in
poor rural zones are not to be expected in the near future,
control programs are needed to deal with this endemic dis-
ease in the short and medium terms.
Received November 15, 2001. Accepted for publication June 27, 2002.
Acknowledgments: We thank the residents of Quilcas who made it
possible to perform this study. Help from the personnel of the Labo-
ratory of Cysticercosis of the Instituto Nacional de Ciencias Neuro-
logicas, Laboratory of Pathology of the Universidad Peruana Cayet-
ano Heredia, and the Facultad de Medicina Veterinaria of the Uni-
versidad Nacional Mayor de San Marcos, J. B. Phu and D. Sara in
sample management and data collection is also acknowledged.
Financial support: This study was funded by grants number 1-U-19-
A145431-01, ABC and ITREID from the National Institutes of
Health and the Fogarty Foundation.
Authors’ addresses: H. H. Garcia and M. Verastegui, Department of
Microbiology, Universidad Peruana Cayetano Heredia, Av. H. Delgado
430, S.M.P., Lima 31, Peru, E-mail: hgarcia@terra.com.pe. R. H. Gil-
man, L. M. Moulton and A. G. Lescano, Department of International
Health, Johns Hopkins University Bloomberg School of Public Health,
615 N. Wolfe St, Room 3501, Baltimore, MD 21205. A. E. Gonzalez, C.
Gavidia, N. Falcon and T. Bernal, School of Veterinary Medicine, Uni-
versidad Nacional Mayor de San Marcos, Av. Circunvalacion s/n, Sala-
manca de Monterrico, Lima, Peru. S. Rodriguez, Cysticercosis Unit,
Instituto de Ciencias Neurologicas, Jiron Ancash 1271, Barrios Altos,
Lima 1, Peru. M. Tovar, A. B. PRISMA, C. Gonzalez 251, Maranga, San
Miguel, Lima, Peru. V. C. W. Tsang, Immunology Branch, Division of
Parasitic Diseases, National Center for Infectious Diseases, Centers for
Disease Control and Prevention, 4770 Buford Highway, Mail Stop F-13,
Atlanta, GA 30333.
Reprint requests: Robert H. Gilman, Department of International
Health, Johns Hopkins University School of Hygiene and Public
Health, 615 N. Wolfe Street, Room 3501, Baltimore, MD 21205.
Phone: 410-614-3639, Fax: 410-614-6060, E-mail: rgilman@jhsph.edu
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