922

Am. J. Trop. Med. Hyg., 59(6), 1998, pp. 922927

Copyright 1998 by The American Society of Tropical Medicine and Hygiene
BALANTIDIASIS IN AYMARA CHILDREN FROM THE NORTHERN BOLIVIAN
ALTIPLANO
JOSE

-GUILLERMO ESTEBAN, CARLOS AGUIRRE, RENE

ANGLES, LAWRENCE R. ASH, AND SANTIAGO MAS-COMA

Departamento de Parasitolog a, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain; Unidad de Parasitolog a,
Instituto Nacional de Laboratorios de Salud Nestor Morales Villazon (INLASA), La Paz, Bolivia
Abstract. Balantidium coli infection was coprologically studied in 2,124 Aymara children 519 years of age from
the schools of 22 communities of the northern Bolivian Altiplano over a ve-year period. Infection with B. coli was
found in 11 of the communities surveyed, with prevalences of 1.05.3% (overall prevalence 1.2%). The prevalences
observed are some of the highest reported and did not differ signicantly among the various age groups or between
boys and girls. These prevalences, the apparent absence of symptoms or signs of illness due to this parasite in the
schoolchildren surveyed at the time of stool sampling, and the consistency of stool samples of the infected students
suggest that they are apparently asymptomatic carriers. Infection with B. coli must be considered as an endemic
anthropozoonosis in the area studied. A relationship between B. coli infection and Altiplanic pigs is suggested.
Balantidium coli (Malmsten, 1857) (Ciliophora: Balanti-
idae) is the largest protozoan and the only ciliate parasite of
humans. Although numerous animal species are known to
harbor B. coli, pigs have a particularly high rate of infection
(20100%) and consequently are generally considered the
main natural reservoir of this parasite.
1
Although B. coli infection in humans has a worldwide
distribution, it is considered an uncommon infection. Prior
to 1988, less than 1,000 human cases had been reported.
24
A review of the literature has shown that the majority of
reports are concerned only with individual symptomatic and
fatal or complicated cases. Only a few reports of outbreaks
or epidemiologic surveys have been published.
58
On the oth-
er hand, in several reports on community-based or epide-
miologic surveys of intestinal parasites in different countries
worldwide, data on human balantidiasis are rarely found.
9
In many large series, estimates of worldwide prevalence
are only 0.020.1%.
1
Nevertheless, rates up to 6%,
1012
with
very high prevalences (up to 29%) in certain areas,
7,8
have
been found. However, although known for more than a cen-
tury, the pathogenicity of the organism and how it is ac-
quired by humans remains controversial.
1
In Bolivia, there have been only three reports of B. coli
in two (Santa Cruz and La Paz) of the nine Departments in
this country. In the rst, a prevalence of 1.8% among 381
apparently healthy subjects from three communities was re-
ported.
13
The other two reports were on two different regions
of two provinces of the Department of La Paz (area
133,985 km
2
with 2,406,185 inhabitants in 1990). One of
them, Coroico, a village located at an altitude of only 1,828
meters in the Yungas region (Nor Yungas Province), had a
prevalence rate of 1.3% in 385 children 29 years of age;
14
the other in an Indian (Quechua ethnicity) hamlet called
Amarete, at an altitude of 3,700 meters and located in the
northern Altiplano region in Saavedra Province 200 km from
the city of La Paz, had a prevalence rate of 8% in 100 chil-
dren 415 years of age.
15
The presence of B. coli in Indians of Aymara ethnicity
inhabiting Los Andes, Omasuyos, Ingavi, and Murillo Prov-
inces of the northern Bolivian Altiplano has been unknown
until recently,
16
although prevalences (2.6% and 3.9% in
Corapata and Caleria, respectively) have been recently re-
ported in studies of Fasciola hepatica infection.
17
The aim of this study was to investigate human balanti-
diasis in a region of the northern Bolivian Northern where
other human parasitoses, such as fascioliasis
1620
and cryp-
tosporidiosis
21
are considered endemic infections.
SUBJECTS, MATERIALS, AND METHODS
Human study population. This study was conducted in
the Department of La Paz in a region of the northern Boli-
vian Altiplano at an altitude of 3,8004,200 meters where
there are four political provinces (Ingavi, Los Andes, Mu-
rillo, and Omasuyos), as shown in Figure 1. The area and
human population (data from the Bolivian Ministry of
Health) of these provinces (area of the country 1,098,581
km
2
; total population 6,344,396 inhabitants) are as fol-
lows: Los Andes: 1,658 km
2
and 61,627 inhabitants; Oma-
suyos: 2,065 km
2
and 73,415 inhabitants; Ingavi: 5,410 km
2
and 77,896 inhabitants; Murillo: 4,705 km
2
and approxi-
mately 1,200,000 inhabitants, including the two most im-
portant cities, La Paz and El Alto, with 710,940 and 392,774
inhabitants, respectively.
16
The Aymara communities surveyed are fundamently rural
with the main economic activities being livestock breeding
(mainly cattle, sheep, and pigs) and agriculture. Fishing is
important in the communities near Lake Titicaca, and in
some communities, such as Achacachi, commercial activities
are more important. Most inhabitants of these zones are poor
and have lived in conditions of poor health. The houses are
rudimentary (roofs made of straw or calamine, walls of ado-
be or sun dried bricks), and the communities lack such basic
services as potable water systems, sewage disposal, and
trash removal. Humans and animals share the same water
sources contaminated with fecal stools. Food, including local
vegetables, is washed with contaminated water, increasing
the risk of acquiring parasitic, bacterial, or viral diseases.
Under these poor living conditions, the family members (av-
erage of ve members per family) live together in crowded
conditions on a small piece of land in close association with
small (chicken, dogs, rabbits, guinea pigs) and large (nor-
mally 12 cattle, sheep, and pigs) animals. Indiscriminate
defecation is commonly practiced.
16
Feces as well as other
materials are commonly eaten by pigs.
Human data collection. Coprologic studies were made
over a ve-year period from 1992 to 1996 in 22 communi-
923 BALANTIDIASIS IN AYMARA CHILDREN IN BOLIVIA
FIGURE 1. Map showing the location of the 22 communities sur-
veyed in the four provinces of the northern Bolivian Altiplano.
TABLE 1
Prevalence of Balantidium coli infection inthe communities sur-
veyed
Communties
surveyed No.*
Year of
survey
No. infected/
No. tested %
Omasuyos Province
Achacachi
Huatajata
Cuyahuani
1
2
3
1996
1996
1996
2/92
2/193
0/110
2.2
1.0
0
Los Andes Province
Aygachi
Belen Yayes
Caleria
Chijipata Alto
Corapata
4
5
6
7
8
1994
1949
1993
1996
1993
0/107
0/42
2/51
0/22
2/78
0
0
3.9
0
2.6
Cohana
Iquiaca
Kharapata
Oketiti
Pantini
Quiripujo
9
10
11
12
13
14
1994
1995
1996
1995
1995
1993
5/161
7/131
0/97
0/20
0/33
0/43
3.1
5.3
0
0
0
0
Ingavi Province
Causaya
Chambi Grandi
Huacullani
15
16
17
1995
1995
1992
1/59
0/25
0/123
1.7
0
0
Huacullani
Huacullani
Ticuyo
Yanarico
17
17
18
19
1993
1996
1995
1995
0/254
3/136
1/32
1/82
0
2.2
3.1
1.2
Murillo Province
Achocalla
Kajchiri
Tuni
Total
20
21
22
1996
1994
1994
1992/1996
0/188
0/20
0/25
26/2,124
0
0
0
1.2
* Numbers correspond to the identifying number on the map of Figure 1.
Number of B. coli-infected students/number tested.
Percentage with respect to the number tested.
ties. These surveys were done in June (1992), February (all
communities in 1993 and some communities in 1996), and
September (all communities in 1994 and 1995, and some
communities in 1996) and involved 2,124 Aymara children
(1,146 boys and 978 girls) 519 years of age from the
schools in these communities (Table 1). Surveys were car-
ried out so that the sample size in each school was repre-
sentative of both the student enrollment in the school (at
least 50%) and the number of children present on the day
of the survey (at least 75%). The surveys were made on
randomly selected persons on a given day among all partic-
ipating students.
A clean, 30-ml plastic, wide-mouth, numbered container
with a snap-on lid was given to every child. The students
were then asked to try to ll the container with their own
feces and to return it immediately. One stool sample per
student was collected from all participating school children
and personal data (name, sex, and age) were noted on deliv-
ery of the container. Other data related to gastrointestinal
and intermittent symptoms were not considered because the
answers of children appeared to be contradictory in the few
cases in which an answer was obtained. Thus, the ignorance
of the Aymaras concerning biological risk must be taken into
account. Among the Aymaras, the so-called usu constitutes
not only a concept of illness or health, or of life or death,
but represents a mythic, symbolic horizon from which a se-
ries of behaviors and interpretations of this process arise.
The parasitoses and other internal diseases without a specic
location are usually considered as a punishment or a retali-
ation of the demiurgos, that is, a Pachamaman jasuti pacha-
wa (punishment by the Pachamama). A fatalistic guilt feel-
ing appears when faced with the possibility of death, with
its existence not being questioned because of its divine and
immutable character.
16
Fecal specimens were transported to the Parasitology Lab-
oratory of the Instituto Nacional de Laboratorios de Salud
(La Paz, Bolivia) within 5 hr of collection. In this laboratory,
the consistency (formed, soft, loose, or watery) of each stool
sample was evaluated and noted. From each stool sample a
Kato-Katz slide
22
was made, and if possible (sufcient ma-
terial present) two aliquots were preserved in merthiolate-
iodine-formalin (MIF) xative and 10% formalin solution (1:
3).
23
Parasitologic studies were carried out no longer than
one month later at the Departamento de Parasitolog a (Va-
lencia, Spain). Samples xed in MIF were processed by the
direct MIF and MIF concentration techniques,
24,25
and those
xed in 10% formalin were processed by a formol-ether con-
centration technique.
26
Four slides per specimen were fully
examined by one professional and nally by one of the au-
thors (J-GE). Microscopic slides and materials from the hu-
man parasite collection of the Parasitology Department of
the University of Valencia were used for quality control
when needed.
Nutritional and health status. The nutritional and health
status of the inhabitants of the zone surveyed agreed with
observations previously reported.
16
This zone is markedly
impoverished, with inhabitants in extreme indigence and
with morbility and mortality rates related to a deterioration
of living conditions. More than 30% of the children of this
zone show malnutrition and appear to be below the mini-
mum recommended level of weight and height.
16
The great-
est nutritional problem seems to be chronic malnutrition,
924 ESTEBAN AND OTHERS
TABLE 2
Prevalence of balantidiasis among students by sex and age
Age group
(years)
Males
No. infected/
No. tested*
(%) %
Females
No. infected/
No. tested*
(%) %
Total
No. infected/
No. tested*
(%) %
58
912
9/418
(2.2)
4/535
(0.7)
50.0
22.2
2/368
(0.5)
5/480
(1.0)
25.0
62.5
11/786
(1.4)
9/1,015
(0.9)
42.3
34.6
1316
1719
5/183
(2.7)
0/10
(0)
27.8
0
1/128
(0.8)
0/2
(0)
12.5
0
6/311
(1.9)
0/12
(0)
23.1
0
Total 18/1,146
(1.6)
69.2 8/978
(0.8)
30.8 26/2,124
(1.2)
100
* Number of B. coli-infected students/number tested.
Percentage with respect to the number tested.
Percentage with respect to the total number of males, females, or total school children presenting B. coli infection ().
characterized by a delay in growth, as the consequence of a
protein and energy decit affecting the longitudinal growth
of the long bones. The socioeconomic conditions have mark-
edly deteriorated in recent years, causing an increase of
acute undernourished children in this area to such an extent
that only 2.3% of the children showed development and
growth within normal values. According to the data from the
Pan American Health Organization in Bolivia, the health in-
dicators for the Bolivian Altiplano in 1994
27,28
were the fol-
lowing: 86% poor, 35% with chronic malnutrition, 5% with
adequate excreta disposal facilities available, and 10% with
safe drinking water available in the home or with reasonable
access.
Institutional ethical review procedure. The surveys
were carried out after informed consent was obtained from
the local authorities of the community (among Aymaras,
community authorities are responsible for transmitting pa-
rental consent after previous meetings), as well as from the
Director and teachers of each school. The project was ap-
proved by the Secretar a Nacional de Salud del Ministerio
de Desarrollo Humano (La Paz, Bolivia) and was performed
in collaboration with the INLASA Institute in La Paz, the
ofcial disease reference center for Bolivia. Ethical aspects
of the study were reviewed and approved by the European
Commission as the project funding institution.
Pig samples and data collection. For comparison pur-
poses, 50 stool samples of pigs were obtained from several
of the zones surveyed. In the human communities studied,
almost all the families kept pigs (average 19 pigs per
family).
16
Fresh feces were collected off the ground as ani-
mals were observed defecating. Stool samples were put in a
plastic bag and transported to the Parasitology Laboratory
of the Instituto Nacional de Laboratorios de Salud (La Paz,
Bolivia) within 5 hr. In this laboratory, a small but sufcient
amount of feces was homogenized in 10% formalin. The
mixture was then strained through a funnel containing sterile
gauze into an assay tube, which was then allowed to stand
for 2 hr to allow sedimentation. Finally, several drops of the
sediment were examined with a microscope.
Statistical analysis. Statistical analyses were done using
the chi-square test or Fishers exact test when appropriate
for comparison. A P value 0.05 was considered signi-
cant.
RESULTS
Only 11 of the 22 communities surveyed showed B. coli
infection. The prevalence ranged from 1.0% to 5.3%, with
an overall prevalence in the area studied of 1.2% (Table 1).
Among the 26 positive stool samples, 21 were formed and
containing only cysts and ve were soft and contained tro-
phozoites (3), cysts (1), and both (1). The trophozoites were
5088 (70 10 [mean SD]) m by 4068 (56 8) m
and the cysts were 3560 (51 6) m by 3058 (49 6)
m. Loose and/or watery stool specimens were detected in
5% of the total of 2,124 samples analyzed.
The distribution of prevalences of infection according to
age and sex is shown in Table 2. Prevalences did not differ
signicantly among the various age groups; the highest prev-
alence was found in the 58-year-old age group. Although
no signicant differences were observed between boys and
girls, there appeared to be a trend for increased number of
infections in males.
Thirteen or 14 protozoan and seven helminth species were
detected in all school children studied. These included En-
tamoeba histolytica/E. dispar complex, E. coli, E. hartman-
ni, Endolimax nana, Iodamoeba buetschlii, Chilomastix mes-
nili, Retortamonas intestinalis, Giardia intestinalis, Entero-
monas hominis, Dientamoeba fragilis, Cryptosporidium sp.,
Balantidium coli, Blastocystis hominis, Fasciola hepatica,
Hymenolepis nana, Taenia spp., Trichuris trichiura, Enter-
obius vermicularis, Ascaris lumbricoides, and undetermined
ancylostomids. More than 90% of the total children studied
showed infection with at least one of these parasite species.
Multiple parasite infections were detected, i.e., one girl
showed 11 different parasites (eight protozoan and three hel-
minth species).
Among the 26 samples positive for B. coli infection, the
number of other parasite species found varied from one to
ve or six. The multiparasitism cases were one case of B.
coli concomitantly with the E. histolytica/E. dispar complex,
G. intestinalis, Blastocystis hominis, H. nana, and T. trichi-
925 BALANTIDIASIS IN AYMARA CHILDREN IN BOLIVIA
ura, and another case of B. coli with E. histolytica/E. dispar
complex, E. coli, Cryptosporidium sp., Taenia spp., and T.
trichiura.
Coprologic analyses of the 50 porcine stool samples
showed B. coli infection in 54% of the pigs.
DISCUSSION
This study is believed to be the largest parasitologic sur-
vey carried out to determine infection rates in B. coli. The
prevalences observed may be some of the highest reported
among apparently healthy school children up to the present
time.
While B. coli is considered to be a commensal organism
(rare occurrences of acute infection are reported) in pig pop-
ulations, different types of infection have been described in
humans. Chronic and acute infections can occur sporadically
and in epidemics.
1,8,12,29
In these cases, different symptoms
are present and the stools may be watery or dysenteric
(bloody). Fulminating acute balantidiasis has been reported
to have a case fatality rate of 30%.
1
Patients may die of
intestinal perforation or fulminating dysentery with hemor-
rhage and shock.
3033
Involvement of the lymphatics of the
colonic wall is common and this may extend to the mesen-
teric lymph nodes.
29,34
The appendix
3539
and terminal ileum
40
may be affected. Balantidial vaginitis has been reported,
41
as
have two instances of liver abscess
42,43
and four of lung and/
or pleural involvement.
37,4446
Nevertheless, in populations in
which the parasite is endemic, B. coli is usually found in
asymptomatic persons.
6,7,13
The prevalences obtained, the apparent absence of symp-
toms or signs of illness due to this parasite in the school
children surveyed at the moment of stool sampling (ill chil-
dren did not go to school), and the consistency of stool sam-
ples suggest that the infected students are apparently asymp-
tomatic carriers.
In relation to the source of B. coli infection in humans,
most of the patients with balantidiasis reported in the liter-
ature had a history of contact with pigs,
1,2,11,47,48
and the in-
fection was acquired as a result of contamination of water
supplies by pig feces. Results obtained by other investigators
suggest the existence of different B. coli strains. A few
strains of porcine B. coli can be transmitted among different
experimental animals.
1
Attempts to infect human volunteers
with either human or animal strains of this ciliate have
failed.
49
Antigenic differences between human and porcine
strains have been found.
50
Strains from humans have been
transmitted to monkeys, pigs, cats, and rodents, but experi-
mental infection of humans with strains from pigs and hu-
mans has not been successful, and it appears that humans
are relatively refractory to this parasite, whatever the source
or strain.
48
Diarrhea in piglets and monkeys experimentally
infected with B. coli isolated from human feces have been
demostrated.
12
Features such as infections occurring in people who had
no contact with pigs, in institutions, or in people who work
closely with swine even in poor sanitary conditions suggest
that person-to-person transmission may be important.
1
More-
over, the possibility exists that other animals, notably do-
mestic rodents, may act as reservoirs and play an important
role in the transmission dynamics of human balantidi-
asis.
1,51,52
It appears from our observations that there might be a
relationship between human infections and B. coli in swine
in the northern Bolivian Altiplano. The parasite was found
in pig feces around the homes of several families in some
of the communities surveyed (i.e., Caleria and Huacullani)
in which human infection was found. Moreover, we know
that pigs are commonly fed raw garbage and they are al-
lowed to roam freely in search of food; in the Altiplanic area
surveyed there is a lack of potable water systems and water
may have been contaminated with pig excreta.
The detection of positive human cases in different prov-
inces in different years and no signicant differences based
on the sex and age of the groups studied indicates the ex-
istence of an environment highly contaminated with fecal
material. Thus, infection with B. coli must be considered an
endemic anthropozoonosis in the area studied.
In relation to the pathogenicity of B. coli, several host
factors have been suggested to explain whether an infected
person becomes ill: malnutrition (low protein, high carbo-
hydrate diet), intestinal bacterial ora, concomitant helmin-
thic infection, achlorhydria, alcoholism, and other chronic,
debilitating diseases.
1
Nevertheless, some of these host fac-
tors do not explain the apparently healthy state of the school
children studied. For example, in the Altiplano, the native
Bolivian prepubertal girls and boys with a low socioeco-
nomic status showed overall relatively low energy and nu-
trient intake (fundamentally protein and fat); thus, the lower
energy intake and the higher energy expenditure of these
children is related to their smaller body size.
53
The results suggest the possibility of a high degree of
natural or acquired resistance to this parasite. A similar sit-
uation was observed in the outbreak in Truk, where the peo-
ple were quite resistant to porcine B. coli even when living
in close association with pigs and under poor sanitary con-
ditions.
5
Nevertheless, the possibility that asymptomatic bal-
antidiasis becomes invasive when the immune state of the
body is depressed must be considered.
Acknowledgments: Collaboration by Dr. J. A. Oviedo (Valencia,
Spain) and W. Strauss and M. Magarinos (La Paz, Bolivia) is ac-
knowledged. We thank Dr. C. Feliu (Barcelona, Spain) for supplying
some of the literature. Thanks are also given to the following Bo-
livian institutions in La Paz for use of their facilities and collabo-
ration: Direccion Nacional de Epidemiolog a of the Ministerio de
Prevision Social y Salud Publica (now the Secretar a Nacional de
Salud of the new Ministerio de Desarrollo Humano); Comite Re-
gional de Zoonosis and Centro Piloto of the Unidad Sanitaria La
Paz; and the Ofce of the Pan American Health Organization. This
research was performed during a three-month stay of Professor Law-
rence R. Ash (Department of Epidemiology, School of Public
Health, University of California, Los Angeles, CA) in the Parasitol-
ogy Department of the University of Valencia during a special con-
tract with this university.
Financial support: This work was supported by funding from the
Life Sciences and Technologies for the Developing Countries Pro-
gram of the Commission of the European Communities (DG XII:
Science, Research and Development) (Contract no. TS3-CT94-
0294), Brussels, European Union, by the Program of Scientic Co-
operation with Latin America, Instituto de Cooperacion Iberoamer-
icana, Agencia Espanola de Cooperacion Internacional (ICI-AECI),
and by Project no. UE96-0001 of the Direccion General de Inves-
tigacion Cientif ca y Tecnica (DGICYT), Spanish Ministry of Ed-
926 ESTEBAN AND OTHERS
ucation and Science, Madrid. Carlos Aguirre thanks the Mutis Schol-
arship Program of the Instituto de Cooperacion Iberoamericana of
the Agencia Espanola de Cooperacion Internacional (ICI-AECI),
Madrid for a fellowship.
Authors addresses: Jose-Guillermo Esteban, Carlos Aguirre, and
Santiago Mas-Coma, Departamento de Parasitolog a, Facultad de
Farmacia, Universidad de Valencia, Av. Vicente Andres Estelles s/
n, 46100 Burjassot, Valencia, Spain. Rene Angles, Unidad de Par-
asitolog a, Instituto Nacional de Laboratorios de Salud Nestor Mo-
rales Villazon, Pasaje Rafael Subieta No. 1889, Miraores, La Paz,
Bolivia. Lawrence R. Ash, Division of Epidemiology, School of
Public Health, University of California, 10833 Le Conte Avenue,
Los Angeles, CA 90024-1772.
Reprint requests: Jose-Guillermo Esteban, Departamento de Parasi-
tolog a, Facultad de Farmacia, Universidad de Valencia, Av. Vicente
Andres Estelles s/n, 46100 Burjassot, Valencia, Spain.
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