Acta Tropica 83 (2002) 223
/231

www.parasitology-online.com

Ascaris lumbricoides among children in rural communities in

the Northern Area, Pakistan: prevalence, intensity, and
associated socio-cultural and behavioral risk factors
Hiroshi Nishiura a,*, Hirohisa Imai a, Hiroyuki Nakao a, Hiromasa Tsukino a,
Mohammad Ali Changazi b, Gulzar Ali Hussain b, Yoshiki Kuroda a,
Takahiko Katoh a
a
Department of Public Health, School of Medicine, Miyazaki Medical College, 5200 Kihara, Kiyotake, Miyazaki Prefecture 889-1692,
Japan
b
Social Welfare Association of Baltistan, Casualty Department, Skardu District Headquarters Hospital, Skardu, Baltistan District,
Northern Area 16100, Pakistan

Received 20 October 2001; received in revised form 3 April 2002; accepted 15 April 2002

Abstract

The prevalence and intensity of Ascaris lumbricoides in 492 children from five rural villages in the Northern Area of
Pakistan was examined. The overall prevalence of A. lumbricoides was 91% (95%CI 88.6
/93.6) with geometric mean
(GM) egg count intensities of 3985 eggs per g (epg). The most intense A. lumbricoides infections were found in children
aged 5
/8 years. We also investigated selected socio-cultural and behavioral variables for A. lumbricoides infections that
might be relevant for the design of appropriate prevention and control programs. Univariate analysis associated A.
lumbricoides intensity with age (P /0.004), location of household (P B/0.01), defecation practices (P/0.02), soil eating
habit (P B/0.01), hand washing after defecation (P B/0.01), and living with children under 5 years old (P/0.02).
Multivariate analysis identified the childrens age 5
/8 (P B/0.01), location of household in Surngo, Askole, and
Stakchun where the pilot health care model activities were not done (P B/0.01), and living with children under 5 years
old (P/0.03) as variables statistically associated with the intensity of A. lumbricoides . The results indicated that there
were certain clear risk factors in A. lumbricoides transmission, and that its intensity was influenced by age-related
behavioral and environmental factors that contribute to exposure. # 2002 Elsevier Science B.V. All rights reserved.

Keywords: Ascaris lumbricoides ; Intensity; Socio-cultural study; Risk factors; Children; Pakistan

1. Introduction

* Corresponding author. Tel.: /81-985-85-0874; fax: /81- Intestinal parasites remain a major health pro-
985-85-6258 blem in many developing countries. Global num-
E-mail address: hiroshi.nishiura@mc2.seikyou.ne.jp (H. bers of ascariasis due to Ascaris lumbricoides have
Nishiura).

0001-706X/02/$ - see front matter # 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 0 0 1 - 7 0 6 X ( 0 2 ) 0 0 1 1 6 - X
224 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231
been estimated at about 1.5 billion cases (Cromp-
ton, 2001). The global burden of this disease is an
estimated 10.5 million disability-adjusted life-years
(DALYs) lost (World Bank, 1993). Helminth
infections are often described as providing differ-
ent clinical pictures to those of other infectious
diseases as they tend to be chronic, with slow onset
(Hall and Chan, 1994). In clinical practice, a heavy
infection of A. lumbricoides is an important cause
of intestinal obstruction (Cooper et al., 1992), and
it is widely considered that most infections sig-
nificantly impair childhood nutrition, especially in
areas where poor growth is common (Stephenson
et al., 2000). Recent investigations have indicated
that this heavy infection can also affect mental
processing or cognitive functions (Hadidjaja et al.,
1998; Oberhelman et al., 1998).
Interventions to solve helminthiases problems in
humans rely mostly on chemotherapy aimed at
destroying the parasite in the short-term and on
improving hygiene and sanitation in the long-term
(OLorcain and Holland, 2000). Targeted treat-
ment, especially aimed at children in primary
schools, has been a major recent focus in some
areas. The World Health Organization advocates a
strategy of health-promoting in schools worldwide
(WHO, 1997). The relevance of this for Northern
Pakistan is the synergistic impact appropriate
nutritional and educational interventions can
have.
Many studies regarding intestinal parasites have
focused on establishing prevalence and intensity of
these infections in different populations, but fewer
studies have examined the socio-cultural factors
affecting transmission. Factors enhancing expo-
sure to A. lumbricoides eggs that have been
implicated in previous studies include the lack of
latrines (Smith et al., 2001), defecation practices
(Haswell-Elkins et al., 1989), geophagia (Geissler
et al., 1998), the level of sanitation in households
(Hidayah et al., 1997), lower socio-economic
status (Henry, 1988) and so on. Hidayah et al.
(1997) argues that effective strategies in the pre-
vention and control of soil-transmitted helminthia-
sis are dependent on identifying modifiable risk
factors that increase the susceptibility of the
community. However, few studies provide contri-
butable discussion for health workers in rural
areas. Although the Government of Pakistan has
recently completed a national health examination
survey, the National Health Survey of Pakistan
(Pappas et al., 2001), the Northern Area was not
included, and there is therefore little data regard-
ing the health status of the Pakistani population in
this area. The Himalayan Green Club, a Japanese
non-governmental organization, beginning in
1993, has introduced measures against helminth
infections in this area as an integrated primary
health care program in cooperation with the
Ministry of Health and Social Welfare, Pakistan
(MHSW), and the Social Welfare Association of
Baltistan (SWAB), a Pakistani non-governmental
organization. This study was done in collaboration
with these organizations with the purpose of
investigating the prevalence and intensity, and
analyzing the socio-cultural risk factors for A.
lumbricoides infections that might be relevant for
the design of appropriate intervention in this area.
2. Subjects, materials, and methods
2.1. Subjects
Parasitological studies and socio-cultural sur-
veys for ascariasis were carried out in five selected
villages, endemic for A. lumbricoides infection, in
the Baltistan District in the Northern Area along
with the left bank of the Braldu River, about 120
km away from the District Headquarters of
Skardu, which lies in the mountain area of
Pakistan. There are no pipe borne water supplies
and the people therefore depend on spring water
from melted snow. The village houses are mud-
walled and roofed with wood and leaves. Men are
subsistence farmers while women combine farming
with domestic work and petty trading. Both sexes
had limited access to major cities. The five villages,
Askole, Srungo, Stakchun, Teste, and Korphe,
each populated with between 300 and 600 persons,
are comprised of mostly Balti speaking people of
whom about 80% cannot read or write. These
villages, highly endemically infected by A. lumbri-
coides , were enrolled in an integrated primary
health care program that included treatment for
geohelminthiasis. The proportion of the popula-
 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231
tion under 15 years old was between 46 and 53%
including children who didnt attend a primary
school. Among the five primary schools, a total of
650 pupils (308 male and 342 female) were
randomly selected from the list of students for
this study. Ages ranged from 5 to 12 years, with
396 (60.9%) aged 9
/12.
Since August 1999 Teste and Korphe have been
set up as pilot health care model villages, where
some trained health workers were always present.
Inhabitants in these two villages had several kinds
of treatments in the primary health care program
including anthelmintics; the treatment method
detailed by Kightlinger et al. (1995) as a reference,
children were examined and dewormed twice at a
12-month interval, using mebendazole, 500 mg, at
the first deworming; and pyrantel pamoate, 11 mg/
kg, at the second deworming. They were also given
many opportunities to learn about common dis-
eases and their own health. However, there was no
apparent difference in lifestyle, opportunities of
primary education or living environment among
the five villages. Although residents in the other
three villages had opportunities from occasional
health education campaigns in primary school,
there were no health workers in their villages.
2.2. Methods
2.2.1. Data collection
In the first phase of this study, group interviews
in Balti, the local language, were used to obtain
descriptive information on peoples perceptions,
knowledge and beliefs in relation to the clinical
symptoms or control of A. lumbricoides infections.
Interviews were conducted from June to August
2000, and each guided by the research team, was
held at the primary schools in each of the five
villages with pupils (n/223), their parents (n /76)
and teachers (n /8). Participants were selected
based on a convenient sampling, and each inter-
view lasted between 60 and 90 min. Eight to 12
people participated in each interview. Summary
notes were recorded by note takers from the
research team who acted as observers. The in-
formation collected from each of the interview was
coded and analyzed. Recurring ideas were identi-
fied and patterns of belief analyzed.
225
Subsequently, the research team formulated a
pilot questionnaire. Based on information ob-
tained from the interviews, soap availability,
housing construction, and illiteracy of parents,
which were perceived and indicated as a possible
risk factor in each interview group, were incorpo-
rated to the questionnaire. The pilot questionnaire
was administered to 15 individuals, three each
from separate households in different five
villages. The pre-tested questionnaire was com-
pleted 1 year after the time of the group interview,
and covered 13 closed questions; demographics,
parental awareness, soap availability, housing
construction, illiteracy of parents, and ex-
perience of common childhood behavior such as
defecation practices, hand washing, and eating of
soil. All participating pupils were given an identity
(ID) number and surveyed in their own
primary school in the local language. Teachers
and research assistants guided the questionnaires
which were recorded without names (only ID
numbers).
2.2.2. Collection and analysis of fecal specimens
Following the questionnaire, single stool speci-
mens from all the selected children were collected
and labeled with ID number. Kato-Katz technique
(Martin and Beaver, 1968) was used to measure
infestation by A. lumbricoides (eggs per g of feces;
epg). As for the estimation of the intensity,
individuals were categorized as having light, mod-
erate or heavy infections based on the criteria set
by the WHO Expert Committee (WHO, 1987).
For A. lumbricoides infection the presence of 0
/
4999 epg was regarded as a light infection, between
5000
/50 000 epg as a moderate infection and /
50 000 epg as a heavy infection. Although other
helminthic infections including Trichuris trichiura
and hookworm were found by the stool examina-
tion, neither prevalence nor individual egg
counts were recorded. The same anthelmintic
treatment described above was implemented for
children in the five villages including Askole,
Stakchun, and Surngo from 1995. The study was
conducted 4 months after the last treatment in
each village.
226 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231
2.3. Statistical analysis
All data were entered using Microsoft Excel
2000 (Microsoft Corporation, Redmond, WA) by
two different persons and checked. The statistical
data were analyzed using SPSS (SPSS, Chicago,
IL) software. Egg counts (epg/1) were trans-
formed to common logs for statistical application,
and reported as geometric mean (GM; calculated
as antilog [{a log(x/1)}/n]/1; x/egg counts,
n /the number of subjects). In this study, intensity
refers to the mean epg in the population sampled.
Comparisons between groups were performed
using chi-square or Fishers exact tests to assess
the univariate association of the risk factors with
the heavy infections of A. lumbricoides in each
household. The level of statistical significance was
set at P /0.05. A multiple regression model was
employed to determine risk factors significantly
associated with intensity of A. lumbricoides , and to
eliminate confounding variables. As there were
many potential predictor variables concerning
intensity of A. lumbricoides , we selected only
variables that were significantly associated with
A. lumbricoides in univariate analysis. Further, in
multiple regression, we selected the set of variables
to be included in the model by the stepwise
method. The estimates of regression coefficients
and the corresponding standard errors were calcu-
lated using the variables significantly associated
with the intensity.
2.4. Ethical consideration
Approval for this study was obtained from the
Ethics Committee at the Miyazaki Medical Col-
lege and the Pakistan Medical Research Council as
well as from local committees in Northern Area.
Considerable thought had been given to the
methodology that was used when determining
Teste and Korphe as the pilot health care model
village (PHCV), and asking participants to take
part. PHCV was firstly determined by the discus-
sions and votes with the village heads, representa-
tive from MHSW, and all of householders in each
enrolled villages in order PHCV to be good
example of community health intervention. Prior
to the beginning of the study, the parents or
guardians of children (with or without A. lumbri-
coides ) were held in primary schools in the five
communities. Research team explained that the
enrollment in this study is voluntary, and gave
participants the explicit right to withdraw at any
time. The parents or guardians were informed of
how the information would be used and assured of
the confidentiality of the responses. The purpose
of this study was explained in the local language
Balti, and informed verbal consent was obtained
from parents or guardians. No names (only ID
numbers) were assigned to each questionnaire.
3. Results
3.1. Study population
Approximately 75.7% (n /492; 234 male and
258 female) of the randomly sampled eligible
children in the five communities participated in
this study. The main reasons for non-participation
among 158 pupils (24.3%) were the decision by
parent or guardian not to take part or the family
moved away. There was no significant difference
in attendance between the villages. The mean age
of respondents to the questionnaire was 8.8 years
(Standard Deviation (S.D.) /2.19, median age /9
years). All participants were pupils in primary
schools.
3.2. Prevalence and Intensity
The overall prevalence of A. lumbricoides in the
five villages was 91.1% (95% Confidence Interval;
CI, 88.6
/93.6). Table 1 shows the differences in
prevalence and intensity of A. lumbricoides infec-
tions by age group and village. GM egg count
intensities were 3985 epg. Prevalence in children
aged 5
/8 years was as same as that of 9
/12 years.
Overall, infection of A. lumbricoides was mostly
moderate or light (8% heavy infection, 82.9%
moderate or light infection), except in the village
of Surngo where there were 21 cases (16.4%) of
heavy infections. Children aged 5
/8 had heavier
infections while children aged 9
/12 more fre-
quently had moderate or light infections. Boys
tended to have more intensive infections than girls.
 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231 227

Table 1
Intensity of A. lumbricoides by age

Community/age in years (N ) Heavy Moderate Light Total infected

N (%) N (%) N (%) N (%)

Surngo (N/128)
5
/8 (55) 14 (25) 27 (49) 12 (22) 53 (96)
9
/12 (73) 7 (10) 32 (44) 31 (42) 70 (96)
Total infected (%) 21 (16) 59 (46) 43 (42) 123 (96)
Teste (N/83)
5
/8 (36) 1 (3) 10 (28) 17 (47) 28 (78)
9
/12 (47) 0 (0) 13 (28) 26 (55) 39 (83)
Total infected (%) 1 (1) 23 (28) 43 (52) 67 (81)
Korphe (N/119)
5
/8 (50) 4 (8) 22 (44) 18 (36) 44 (88)
9
/12 (69) 0 (0) 28 (41) 32 (46) 60 (87)
Total infected (%) 4 (3) 50 (42) 50 (42) 104 (87)
Askole (N/91)
5
/8 (36) 8 (22) 15 (42) 12 (33) 35 (97)
9
/12 (55) 1 (2) 30 (55) 21 (38) 52 (95)
Total infected (%) 9 (10) 45 (49) 33 (36) 87 (96)
Stakchun (N /71)
5
/8 (26) 5 (19) 16 (62) 5 (19) 26 (100)
9
/12 (45) 0 (0) 26 (58) 15 (33) 41 (91)
Total infected (%) 5 (7) 42 (59) 20 (28) 67 (94)
All villages (N/492)
5
/8 (203) 32 (16) 90 (44) 64 (32) 186 (92)
9
/12 (289) 8 (3) 129 (45) 125 (43) 262 (91)
Total 91.1
95% CI 88.6
/93.6

N : number.

Surngo was the village with the highest pre-
valence of A. lumbricoides ; 96.1% (95%CI; 92.7
/
99.5) of those surveyed (male 96.7%, female 95.5%
respectively), and had much higher intensity of
infection in both age groups. On the other hand,
Teste had the lowest prevalence of A. lumbricoides
infection (80.7%, 95%CI; 72.2
/89.2) and there was
only one case of heavy infection. Among the
children surveyed in this village, 83.3% of males
and 78.0% of females were infected with A.
lumbricoides . Korphe followed, having the second
lowest prevalence (87.4%, 95%CI; 81.4
/93.4) of
the five villages. The prevalence of A. lumbricoides
in Askole and Stakchun was 95.6% (95%CI; 91.4
/
99.8) and 94.4% (95%CI; 89.0
/99.7), respectively.
In both villages, most of the heavy infections
occurred in 5
/8 year olds. In Stakchun, all of
the 5
/8 years old participants were infected with
A. lumbricoides .
3.3. Univariate analysis of socio-cultural and
behavioral factors associated with infections of A.
lumbricoides
Table 2 summarizes the A. lumbricoides GM
epgs grouped by socio-cultural proxy exposure
factor, and compares non-infected (n/43) and
heavily infected children (n /40) in each grouping.
Overall, the boys had a higher GM epg than girls;
however, there was no significant sex-related
difference in intensity. As for childrens age,
children 5
/8 years old had significantly higher
worm intensities than did 9
/12 year olds (P /
0.004) (Table 2).
228 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231

Table 2
Univariate analysis: socio
/cultural and behavioral factors in relation to A. lumbricoides intensity, and comparisons of the non-infected
and most heavily infected children

N Geometric mean EPG No. non-infected No. heavily infected x2, Fisher P

All children in sample 492 3985 43 40

Sex
Boys 234 4690 19 23
Girls 258 3437 24 17 NS
Age
5
/8 203 5737 17 32
9
/12 289 3074 26 8 0.004
Location of household
Askole, Surngo, and Stakchun 290 7551 12 35
Teste, Korphe 232 1910 31 5 B/0.01
Place of child defecation
Latrine 411 3565 35 22
Promiscuous 81 7011 8 18 0.02
Washing hands after defecation
Yes 277 2567 33 11
No 215 7022 10 29 B/0.01
Soap available
Yes 223 3563 20 17
No 269 4372 23 23 NS
Eating soil
Yes 103 7497 3 19
No 389 3371 40 21 B/0.01
Living with children under 5 years
Yes 230 5479 10 20
No 262 3013 33 20 0.02
Literacy, father
Yes 48 1079 10 6
No 444 4589 33 34 NS
Literacy, mother
Yes 99 1585 17 10
No 393 5026 26 30 NS
Awareness of worm transmission
Yes 232 4960 14 21
No 260 3278 29 19 NS
Floor construction
Dirt 272 4304 21 21
Sticks or concrete 220 3623 22 19 NS

A higher percentage of households located in
Askole, Surngo and Stakchun (non-pilot villages),
had more members heavily infected with A.
lumbricoides (12.1%) than households in the pilot
health care model villages, Teste and Korphe
(2.4%). There was a significant difference of
intensity between the pilot model villages and
non-pilot (P B/0.01) (Table 2). Also, there were
significant differences in prevalence between Teste
and other villages (P /0.02).
There was an association between the presence
of children under 5 years old and intensity in
 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231
household members (P/0.02). Households with
children under 5 years old had a higher intensity
and more infection of A. lumbricoides compared to
households without. About 12% of participants
living with children under 5 years old were heavily
infected.
About 22% of children who did defecate pro-
miscuously were heavily infected. In this respect,
children defecating in a site other than a latrine
were associated with heavy infections of A. lum-
bricoides (P /0.02) (Table 2). Households that did
not own a latrine and households where children
did not always use the latrine for defecation had a
higher percentage of members with infections.
Hand washing behavior was examined as a
possible variable associated with infection. Ap-
proximately 44% of children responded they did
not wash their hands after defecation. Geometric
mean epg in children not washing hands after
defecation was nearly three times that of children
washing hands. In this way, the children who did
not wash their hands after defecation had signifi-
cantly higher intensity than children who washed
(P B/0.01) (Table 2). As for common childhood
behavior of eating soil, about 20% of children had
had an experience of eating soil within the past 3
months. More than 70% of children who re-
sponded that they had eaten were under 8 years
old. The intensity among children having experi-
ence of eating soil was significantly higher than in
those who did not (P B/0.01).
Other variables, soap available, illiteracy of
both father and mother, awareness of worm
transmission, and floor construction were not
significantly associated with worm intensities.
3.4. Multivariate analysis of variables associated
with infections of A. lumbricoides
A multiple regression model (Table 3) shows an
overall weak model for predicting A. lumbricoides
intensity. This analysis identified the following
variables as those statistically associated with
intensity of A. lumbricoides : children aged 5
/8
(P B/0.01), location of household in Surngo,
Askole, and Stakchun where the pilot healthcare
model activities were not instituted (P B/0.01), and
living with children under 5 years old (P /0.03).
229
Place of child defecation, eating soil, and hand
washing behavior after defecation were not useful
predictors of worm intensity.
4. Discussion
4.1. Identifying risk factors
A. lumbricoides is highly prevalent in the com-
munities studied in Pakistan and the levels of
infection are indicative of major problems in basic
hygiene and sanitation. Our study showed that
there were certain clear risk factors in A. lumbri-
coides transmission, and that its intensity is
influenced by age-related behavioral and environ-
mental factors that contribute to exposure. Often,
this kind of disease control program is unsuccess-
ful or unsustainable in developing countries be-
cause the strategies pursued are inappropriate for
the community or incompatible with traditional
perceptions of etiology (Ahorlu et al., 1999). In the
short term, mass chemotherapy at a community
level using anthelmintics on a regular basis is the
most cost-effective mode of intervention. How-
ever, for longer term benefits, the ways of limiting
transmission through improvements in water sup-
ply, personal sanitation, and hygiene is necessary
(Mascie-Taylor et al., 1999). Therefore, we con-
sidered it was essential to examine the longer-term
socio-cultural and behavioral factors associated
with A. lumbricoides infection to decrease the
susceptibility in each community.
4.2. Association of socio-cultural factors
Although adults usually defecated in the woods
surrounding the village, children were allowed to
defecate in the village. Our study showed that
children who defecated promiscuously had a
higher prevalence and a greater intensity of A.
lumbricoides . Although our finding, defining pro-
miscuous defecation as a possible risk factor,
supports similar results (Haswell-Elkins et al.,
1989; Olsen et al., 2001), it should be noted that
if the community at large is fecally contaminated,
toilet and latrine use are not necessarily protective
for individuals (Feachem et al., 1983). However,
230 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231

Table 3
Multiple regression analysis for Ascaris lumbricoides worm intensity and socio-cultural factor related exposure*

Independent variables Parameter coefficient S.E. t P

Intercept constant 4.148 0.306 13.54 B/0.01

/Age /0.125 0.029 /4.28 B/0.01
/Location of household 0.665 0.108 6.18 B/0.01
(Teste, Korphe or not)
/Living with children under 5 0.225 0.105 2.15 0.03
/Eating soil 0.147 0.136 1.08 0.28
/Hands washing 0.089 0.119 0.75 0.46
/Place of defecation 0.089 0.153 /0.58 0.56
(latrine or promiscuous)
*
r2 /0.143 (F value/13.48, P B/0.0005). Dependent variable: log(egg counts/1).

defecation practices are described as focal points 4.3. Applying results

for disease transmission (Chandiwana et al., 1989).
Muller et al. (1989) found that fecal pollution of
the household environment was due more to
promiscuous defecation than to poor construction
or maintenance of latrines, indicating that it is
necessary to complement sanitation with health
education.
Even though Kightlinger et al. (1998) found no
practical link between childrens hygiene and their
intestinal worms, our study, however, showed that
common childhood behavior such as eating soil
and not washing hands after defecation increased
opportunities to be infected. This result supported
the findings by Geissler et al. (1998) stating
geophagy as a risk factor for geohelminth infec-
tions.
In Teste and Korphe, combined intervention,
mass chemotherapy and health education, was
conducted regularly by health workers. In our
study, while the impact of pilot health care model
projects might be difficult to measure, there was a
significant difference in the intensity of A. lum-
bricoides between the villages with combined
intervention and those without. Eve et al. (1998)
showed that differences in prevalence between
districts surveyed might have been due to the level
of each areas hygienic practices. It can be
hypothesized that varying levels of sanitation in
the community influenced the intensity.
An effective primary health care program to
bring about changes in behavior and hygienic level
needs to be based on a clear understanding of
socio-cultural and behavioral risk factors. Multi-
variate analysis, performed in order to control for
possible confounding effects of other study vari-
ables, identified the three significant variables:
childrens age of 5
/8, a primary health care
program like in pilot health care model village,
and living with children under 5, which should be
taken into consideration in prevention and control
strategies in the transmission of ascariasis in the
communities studied. The long term approach
towards the prevention and control in the com-
munities studied should be directed towards im-
plementing primary health care programs like in
Teste and Korphe along with intensifying health
education of mothers with respect to the safe
disposal of small childrens excreta.
Acknowledgements
We are grateful to the village leaders, health
workers and all the respondents from the five
study villages for their participation and colla-
boration. We would like to thank the members of
the Himalayan Green Club for their cooperation;
Ms Kyoko Endo, Ms Yumiko Osaka, Ms Maki
 H. Nishiura et al. / Acta Tropica 83 (2002) 223
/231
Tamura, Dr Tsune Kuroishi, and Dr Fumio
Matsudaira. We sincerely thank the members of
the Social Welfare Association of Blatistan for
their help in data collection; Mr Nasir Ali Khan
and Mr Zamin Ali Khan.
References
Ahorlu, C.K., Dunyo, S.K., Koram, K.A., Nkrumah, F.K.,
Aagaard-Hansen, J., Simonsen, P.E., 1999. Lymphatic
filariasis related perceptions and practices on the coast of
Ghana: implications for prevention and control. Acta Trop.
73, 251
/261.
Chandiwana, S.K., Bradley, M., Chombo, F., 1989. Hook-
worm and roundworm infections in farm-worker commu-
nities in the large-scale agricultural sector in Zimbabwe. J.
Trop. Med. Hyg. 92, 338
/344.
Cooper, E.S., Whyte-Alleng, C.A.M., Finzi-Smith, J.S., Mac-
Donald, T.T., 1992. Intestinal nematode infections in
children: the pathophysiologic price paid. Parasitology
104, S91
/S93.
Crompton, D.W., 2001. Ascaris and ascariasis. Adv. Parasitol.
48, 285
/375.
Eve, E., Ferraz, E., Thatcher, V.E., 1998. Parasitic infections in
villagers from three districts of the Brazilian Amazon. Ann.
Trop. Med. Parasitol. 92, 79
/87.
Feachem, R.G., Guy, M.W., Harrison, S., Iwugo, K.O.,
Marshal, T., Mbere, N., Muller, R., Wright, A.M., 1983.
Excreta disposal facilities and intestinal parasitism in urban
Africa: preliminary studies in Botswana, Ghana and Zam-
bia. Trans. R. Soc. Trop. Med. Hyg. 77, 515
/521.
Geissler, P.W., Mwaniki, D., Thiongo, F., Friis, H., 1998.
Geophagy as a risk factor for geohelminth infections: a
longitudinal study of Kenyan primary schoolchildren.
Trans. R. Soc. Trop. Med. Hyg. 92, 7
/11.
Hadidjaja, P., Bonang, E., Suyardi, M.A., Abidin, S.A., Ismid,
I.S., Margano, S.S., 1998. The effect of intervention on
nutritional status and cognitive function of primary school
children infected with Ascaris lumbricoides . Am. J. Trop.
Med. Hyg. 59, 791
/795.
Hall, A., Chan, M., 1994. Intestinal worms: strategies to control
disease. Afr. Health 17, 23
/26.
Haswell-Elkins, M., Elkins, D.B., Anderson, R.M., 1989. The
influence of individual, social group and household factors
on the distribution of Ascaris lumbricoides within a com-
munity and implications for control strategies. Parasitology
98, 125
/134.
Henry, F.J., 1988. Reinfection with Ascaris lumbricoides after
chemotherapy: a comparative study in three villages with
varying sanitation. Trans. R. Soc. Trop. Med. Hyg. 82,
460
/464.
Hidayah, N.T., Teoh, S.T., Hillman, E., 1997. Socio-environ-
mental predictors of soil-transmitted helminthiasis in a rural
231
community in Malaysia. Southeast Asian J. Trop. Med.
Public Health 28, 811
/815.
Kightlinger, L.K., Seed, J.R., Kightlinger, M.B., 1995. The
epidemiology of Ascaris lumbricoides , Trichuris trichiura ,
and hookworm in children in the Ranomafana rainforest,
Madagascar. J. Parasitol. 81, 159
/169.
Kightlinger, L.K., Seed, J.R., Kightlinger, M.B., 1998. Ascaris
lumbricoides intensity in relation to environmental, socio-
economic, and behavioral determinants of exposure to
infection in children from Southeast Madagascar. J. Para-
sitol. 84, 480
/484.
Martin, L.K., Beaver, P.C., 1968. Evaluation of Kato thick-
smear technique for quantitative diagnosis of helminth
infections. Am. J. Trop. Med. Hyg. 17, 382
/391.
Mascie-Taylor, C.G., Alam, M., Montanari, R.M., Karim, R.,
Ahmed, T., Karim, E., Akhtar, S., 1999. A study of the cost
effectiveness of selective health interventions for the control
of intestinal parasites in rural Bangladesh. J. Parasitol. 85,
6
/11.
Muller, M., Sanchez, R.M., Suswillo, R.R., 1989. Evaluation of
a sanitation programme using eggs of Ascaris lumbricoides
in household yard soils as indicators. J. Trop. Med. Hyg. 92,
10
/16.
Oberhelman, R.A., Guerrero, E.S., Fernandez, M.L., Silio, M.,
Mercado, D., Comiskey, N., Ihenacho, G., Mera, R., 1998.
Correlations between intestinal parasitosis, physical growth,
and psychomotor development among infants and children
from rural Nicaragua. Am. J. Trop. Med. Hyg. 58, 470
/
475.
OLorcain, P., Holland, C.V., 2000. The public health signifi-
cance of Ascaris lumbricoides . Parasitology 121, S51
/S71.
Olsen, A., Samuelsen, H., Onyango-Ouma, W., 2001. A study
of risk factors for intestinal helminth infections using
epidemiological and anthropological approaches. J. Biosoc.
Sci. 33, 569
/584.
Pappas, G., Akhtar, T., Gergen, P.J., Hadden, W.C., Khan,
A.Q., 2001. Health status of Pakistani population: a health
profile and comparison with the United States. Am. J.
Public Health 91, 93
/98.
Smith, H.M., DeKaminsky, R.G., Niwas, S., Soto, R.J., Jolly,
P.E., 2001. Prevalence and intensity of infections of Ascaris
lumbricoides and Trichuris trichiura and associated socio-
demographic variables in four rural Honduran commu-
nities. Mem. Inst. Oswaldo. Cruz. 96, 303
/314.
Stephenson, L.S., Latham, M.C., Ottesen, E.A., 2000. Malnu-
trition and parasitic helminth infections. Parasitology 121,
S23
/S38.
WHO, 1987. Prevention and control of intestinal parasitic
infections. WHO. Tech. Rep. Ser. 749, World Health
Organization, Geneva.
WHO, 1997. Strengthening interventions to reduce helminth
infections as an entry point for the development of health
promoting schools. World Health Organization, Geneva.
World Bank, 1993. World Development Report: Investing in
Health. Oxford University Press, Oxford.