Acta Tropica 120S (2011) S12–S18

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Soil-transmitted helminth and other intestinal parasitic infections among school

children in indigenous people communities in Davao del Norte, Philippines
Vicente Y. Belizario Jr. a , Francis Isidore G. Totañes a,∗ , Winifreda U. de Leon a ,
Yvonne F. Lumampao b , Raezelle Nadine T. Ciro a
a
National Institutes of Health, University of the Philippines Manila, 623 Pedro Gil St., Taft Avenue, Ermita, Manila 1000, Philippines
b
National Center for Disease Prevention and Control, Department of Health, San Lazaro Compound, Sta. Cruz, Manila, Philippines

a r t i c l e i n f o a b s t r a c t

Article history: A significant portion of the population in the Philippines consists of indigenous people (IP) groups, approx-
Received 4 June 2010 imately 9% or 8.1 million. Data on the health status of these groups are very limited including the status
Received in revised form 15 February 2011 of soil-transmitted helminth (STH) infections. Provision of such data will be of great importance in the
Accepted 19 February 2011
formulation of policy on control and prevention of these diseases in this group. This study was conducted
Available online 9 March 2011
in selected villages/barangays in the municipalities of Carmen, Kapalong, San Isidro and Sto. Tomas in the
Province of Davao del Norte in Southern Mindanao, Philippines. Parasitologic assessment was performed
Keywords:
using Kato-Katz to qualify and quantify STH infections, while nutritional status assessment was based on
Helminthiasis
Indigenous people
hemoglobin determination and on nutritional status indicators, i.e., weight-for-age (WFA), height-for-
Intestinal helminth infections age (HFA), and body mass index (BMI) for age derived from anthropometric measurements. A total of 572
Neglected tropical disease school children participated in the survey, 264 (46.2%) of whom belonged to a specific IP group. Results
Soil-transmitted helminth infections showed that 34.1% of the school children had at least one STH infection while 5.9% had heavy intensity
infections. Cumulative prevalence in IP school children was significantly higher than in non-IP children
with rates at 39.0% and 29.9%, respectively (P = 0.021). Overall prevalence of school children with below
normal WFA was 29.9%, while prevalence of those with below normal HFA and BMI for age was 42.8%
and 14.9%, respectively. Of those examined, 8.3% had below normal hemoglobin levels. There was no sig-
nificant difference observed between the nutritional status parameters of IP and non-IP school children.
The parasitologic parameters reported in this study signify the need to pay more attention to IP children
who are at higher risk of morbidity due to helminth infections. Access of IP communities to quality health
services, which include mass drug administration (MDA) and health education on a regular basis, must
be ensured. Further studies to determine factors that contribute to the higher prevalence of STH among
IP groups are recommended.
© 2011 Elsevier B.V. Open access under CC BY-NC-ND license.

1. Introduction
Soil-transmitted helminth (STH) infections, or infection with
Ascaris lumbricoides, Trichuris trichiura and hookworm, rank first
among all communicable and non-communicable diseases in the
school-age population of developing countries worldwide (World
Bank, 1993). In the Philippines, intestinal helminthiasis remains
a major public health concern. In a study involving elementary
school children in selected sites in Luzon, Visayas and Mindanao,
the cumulative prevalence, which is the positivity for at least one
type of STH infection, was 67% (Belizario et al., 2005). A nationwide
study also revealed that 66% of preschool children were infected
with STH (de Leon and Lumampao, 2005), while a much recent
∗ Corresponding author.
E-mail address: doydoytotanes@yahoo.com (F.I.G. Totañes).
study that served as a baseline for the Integrated Helminth Control
Program (IHCP) of Department of Health (DOH) noted an overall
cumulative prevalence of 54.0% and prevalence of heavy intensity
infections of 23.1% (Belizario et al., 2009).
Children ages two to four years old as well as elementary school
children, ages 5–14 years old, are at highest risk for STH infec-
tions due to poor personal hygiene, frequent outdoor exposures and
high risk behavior (WHO, 1998). These children are most prone to
significant morbidity especially those with chronic untreated infec-
tions. A. lumbricoides infection has been known to cause permanent
growth deficits apart from acute complications such as intestinal
obstruction, biliary disease, appendicitis and peritonitis (de Silva
et al., 1997). T. trichiura infection affects the child’s cognition and
the general well-being (Nokes et al., 1992) and has also been associ-
ated with diarrhea and rectal prolapse (Callender et al., 1993; Bundy
and Cooper, 1989). Hookworm infection causes chronic intestinal
blood loss that may eventually result in iron-deficiency anemia and

0001-706X © 2011 Elsevier B.V. Open access under CC BY-NC-ND license.

doi:10.1016/j.actatropica.2011.02.010
 V.Y. Belizario Jr. et al. / Acta Tropica 120S (2011) S12–S18
hypoalbuminemia (Hotez et al., 2004; Stoltzfus et al., 1997). Nutri-
tional deficits due to STH infections in early age may result in severe
and long-term consequences (WHO, 2003). STH infections are also
recognized as a cause of school absenteeism and poor academic
performance. The World Health Organization (WHO) recommends
preventive chemotherapy as a means to control STH infections. This
strategy is implemented through mass drug administration (MDA)
in endemic communities (WHO, 2006).
In addition to STH infections, other intestinal parasitic infec-
tions are also endemic in the Philippines. A study by Belizario et al.
(2007a) showed a prevalence of 31.8% for schistosomiasis among
students in Agusan del Sur. Among those examined, a little more
than half (54.4%) had moderate to heavy intensities of infection. In
another study in Surigao del Norte, Echinostoma sp. was reported
in 11.4% of examined residents (Belizario et al., 2007b). An excep-
tionally high heterophyid infection rate of 36% was also reported
in Compostela Valley (Belizario et al., 2004).
A significant portion of the population in the Philippines consists
of indigenous people (IP) groups, approximately 9% or 8.1 million
of the total population. Among the indigenous-population are the
Ata Manobos, Bagobos, Dibabawons, Mandayas and Mansakas who
inhabit the Davao region (NCIP, 2007). These ethnic groups, con-
sidered as one of the disadvantaged sectors, may be considered to
be more susceptible to diseases such as STH infections, dengue,
filariasis, malaria, diarrhea, malnutrition and other skin infections,
compared to the general population (WHO, 2009). Data on the
health status of these people, which includes the status of STH
infections, are very limited. Therefore, provision of such data will
be of great importance in the formulation of policy on control and
prevention of these diseases in this group.
This project aimed to determine and compare the prevalence
and intensity of STH infections in IP and non-IP school children in
selected communities in Davao del Norte where the IHCP of the
DOH has been implemented for almost three years. In addition,
the project aimed to describe and compare the nutritional status
of these two groups through anthropometric measurements and
hemoglobin level determination.
2. Methodology
2.1. Study site and population
Davao del Norte is located in the Davao Region in Mindanao,
Southern Philippines (Fig. 1). It is bounded by the province of
Agusan del Sur on the north, Davao Gulf and Davao City on the
south, Compostela Valley on the east, and Bukidnon and Davao
del Sur on the west. Davao del Norte is subdivided into 8 munic-
ipalities and 3 cities with a total population of 847,731 (NSCB,
2007). Seven major IP groups occupy Davao region. Of these, the
Manobo and Bagobo groups are the most numerous (NCIP, 2007).
The Manobos occupy most of Davao del Norte, while the Bagobos
are found in the northern part of Davao del Sur. Their major means
of livelihood is agriculture which is supplemented by hunting and
food gathering. They perform roles similar to non-indigenous Fil-
ipino families where men are generally given a higher regard
in terms of decision-making and leadership, while their women
occupy a subordinate position in the society (Mensh, 2009; Uchem,
2001).
The study was conducted in schools in selected barangays in
the municipalities of Carmen, Kapalong, San Isidro and Sto. Tomas.
These barangays were selected based on the presence of IP popula-
tion in the area, accessibility, peace and order situation, no history
of MDA for STH infections within the last three months and will-
ingness of the local government units (LGUs) and tribal chieftains
to participate. School class lists were utilized to obtain informa-
S13
Fig. 1. Map of the Philippines showing the province of Davao del Norte and the four
study sites.
tion like name, age, sex and grade level of students. The IP children
were initially identified with the help of school authorities and
class advisers. This information was verified by the children when
they were asked to specify the specific IP group to which they
belong.
2.2. Study design
A cross sectional study design was utilized to determine
the prevalence and intensity of STH and other intestinal par-
asitic infections in the school children surveyed. A total of 11
barangays with notable IP populations were chosen from the four
municipalities, at least two from each municipality. According to
WHO guidelines (1998), 200–250 individuals for each ecologically
homogeneous area are adequate in order to evaluate helminth
prevalence and intensity. In order to address the possible drop-
out of participants, approximately 100 grade 1 to grade 6 IP
and non-IP elementary school children were targeted for each
municipality for parasitologic and nutritional status assessments.
Purposive sampling was used for the selection of the schools, where
approximately 40–50 participants per school were targeted. The
recruitment of participants was done through convenience sam-
pling.
2.3. Parasitologic assessment
The parasitologic assessment was conducted in November 2009
before the conduct of MDA for filariasis. Stool cups were distributed
to both IP and non-IP children in the selected schools who were ori-
ented on appropriate collection instructions. One stool sample was
collected from each student at least one day after the orientation.
These samples were sent to the field laboratory for processing and
analysis as described in the WHO Bench Aids for the Diagnosis of
Intestinal Parasites (WHO, 1994).
Parasitologic assessment using Kato-Katz (using approximately
41.7 mg of stool) was performed to qualitatively and quantitatively
describe the presence of STH infections. One Kato-Katz slide (with
one aliquot of sample) was prepared from each stool sample. Micro-
scopic reading of the slides was done the same day after processing,
from a few minutes to about 2 h after preparation. This posed as
a limitation in the detection of hookworm eggs, which may be
affected by the clearing effect of glycerine. Raw egg counts were
S14 V.Y. Belizario Jr. et al. / Acta Tropica 120S (2011) S12–S18
multiplied by 24, a constant value, to derive the number of eggs
per gram (epg) of stool. For the purposes of this study, moder-
ate and heavy intensity infections (WHO, 1998) were considered
heavy intensity infections. Kato thick for qualitative parasitologic
assessment was performed when the amount of stool submitted
was not adequate. Trained microscopists from the University of
the Philippines Manila-National Institutes of Health (UPM-NIH),
DOH-Provincial Health Team Office (PHTO) and the Davao del
Norte Provincial Health Office (PHO) processed and examined
the stool specimens. Capacity building for improved microscopic
examination of stool specimens was also conducted for local
microscopists.
The accuracy and reliability of parasitologic assessment were
maintained through quality assurance measures. These mea-
sures involved proper collection of stool specimens, utilization
of fresh reagents, execution of appropriate laboratory tech-
niques, meticulous examination of processed specimens, and
accurate reporting of findings. Slides positive for Echinostoma
sp., Enterobius vermicularis, heterophyid and schistosome eggs
were referred to an expert microscopist for cross-checking
and validation. Initially, at least 10% of all slides were re-
examined blindly by a reference microscopist to ensure accuracy
of microscopic readings. Due to results of quality control (QC)
of initial microscopic readings showing low sensitivity, all neg-
ative slides were reread as part of maintaining quality control.
The results of the slide validation were considered in cases of
discrepancies between the initial and the quality control read-
ings.
2.4. Nutritional status assessment
Anthropometric data were taken from children who submitted
stool samples and who were present during the time of weight and
height measurement. Height measurement was performed with
the aid of a measuring tape attached to a 6 × 1 × 3 wooden plank
and a 12-in. plastic ruler in place of a microtoise. The wooden plank
was secured by taping the upper- and lowermost ends onto a flat
wall. The children were requested to remove their footwear, and
any headgear, hair clips, and hair bands that may obstruct with the
height measurement. A ruler was placed on top of their heads, per-
pendicular to the measuring tape, and the reading was taken from
the top of the ruler at eye level. Height was then read and recorded
to the nearest 0.1 cm.
A calibrated spring-scale or simple bathroom scale was used
to measure weight. This was placed on a firm level surface. Each
child was asked to stand at the center of the scale platform with-
out touching anything, barefoot, in minimal/light clothing and with
empty pockets. The weight was measured and recorded to the near-
est 0.1 kg.
Nutritional status indicators, i.e., weight-for-age (WFA), height-
for-age (HFA) and BMI for age were derived from weight and height
measurements. WFA was computed for children ages 10 years and
below while HFA and BMI for age were computed for school chil-
dren ages 5–19 years. The students were classified as below normal,
normal or above normal according to the standards based on the
WHO Growth Reference (2007).
A portable hemoglobin analyzer (HemoCue® Hb 201+ , Angholm,
Sweden) was used to determine hemoglobin levels in children.
Blood was collected by fingerprick using a lancing device with
disposable lancets, and blood was allowed to fill a microcu-
vette. The blood-filled microcuvette was placed in the cuvette
holder of the analyzer. After approximately 15–60 s, the mea-
surement from the analyzer screen was recorded opposite the
identification number of the student participant on the nutritional
assessment form. The cut-off value used to identify below normal
level was 11.0 g/dL as specified by the machine handbook (Lewis
et al., 2001) and standard cut-off levels for hemoglobin (Henry,
1984).
2.5. Data analysis
Chi-square test or Fisher’s exact test, whichever is appropriate,
were employed to examine association or differences of propor-
tions based on parasitologic and nutritional status of IP and non-IP
school children. The level of significance was set at 0.05. Statistical
analyses were performed using STATA 11.
2.6. Ethical considerations
The proposal was approved by the UPM-NIH Institutional
Review Board. A consultation meeting was held prior to project
implementation where procedures and requirements for obtaining
consent and approval from the community and other key persons
were discussed. Under the supervision of the provincial National
Commission on Indigenous Peoples (NCIP), the municipal tribal
chieftains of the selected municipalities were informed and ori-
ented on the proposed project, and verbal approval from the said
leaders was obtained. Community resolutions from each of the
selected municipalities were obtained from the respective munic-
ipal tribal leaders.
Study participant codes were used to replace identifiers, i.e.,
name, age, grade level and school. A master list of names and cor-
responding codes was created and kept for reference. All results of
parasitologic assessment were written opposite the codes and were
held confidential. Only authorized personnel from the research
team were allowed to access the results.
All school children received albendazole for STH as part of the
yearly MDA for filariasis elimination in November. Those infected
with other intestinal helminths (Schistosoma, heterophyids) and
those with anemia were referred to the DOH-PHT for appropriate
treatment.
3. Results
3.1. Parasitologic assessment
A total of 572 school children participated in the survey, 264
(46.2%) of whom belonged to specific indigenous groups. The IP
children who participated in the study were composed of Ata
Manobos (67.4%), Dibabawons (17.4%), Mansakas (5.7%), Bagobos
(4.2%), Mandayas (3.4%), Aetas (1.5%) and Maranaos (0.4%). The
sex distribution between the IP and non-IP group was homoge-
neous (P = 0.86). Mean age of the study participants was 9.91 years
(SD = 2.2). Age matching was not done, which is a limitation of
this study. Children in the non-IP group were younger by approx-
imately five months compared with the IP group (P = 0.031). The
main characteristics of IP and non-IP school children are presented
in Table 1.
Results of the parasitologic assessment revealed that 195 of
the 572 IP and non-IP school children had at least one STH infec-
tion, giving a cumulative prevalence of 34.1%. The most prevalent
STH infection was A. lumbricoides infection (20.1%), followed by
hookworm infection (11.9%) and T. trichiura infection (11.7%). A
comparison between IP and non-IP school children showed a signif-
icantly higher cumulative STH prevalence in the IP group (P = 0.02).
Analysis also showed that the IP school children had a significantly
higher prevalence of A. lumbricoides compared with non-IP chil-
dren (P < 0.001), while the prevalence of T. trichiura and hookworm
between the two groups were not significantly different (P = 0.81,
P = 0.23, respectively) (Table 2).
Of the 572 stool samples examined, 510 were assessed using
the Kato-Katz method. The overall prevalence of heavy intensity
 V.Y. Belizario Jr. et al. / Acta Tropica 120S (2011) S12–S18 S15

Table 1
Age and sex of IP and non-IP school children who participated in the study (November 2009).

Overall IP Non-IP P-value

No. of school children 572 264 (46.2) 308 (53.8)

Sex, no. (%)
Male 249 116 (43.9) 133 (43.2)
Female 323 148 (56.1) 175 (56.8) 0.855a
Age in years, mean (SD) 9.91 (2.2) 10.08 (2.0) 9.70 (2.3) 0.031b
a
Chi-square test.
b
t-test.

Table 2
Comparison of the prevalence of STH and specific STH infections in IP and non-IP children in selected municipalities in Davao del Norte (November 2009).

Parameters Overall IP Non-IP P-valuea

No. (%) No. (%) No. (%)

Examined (KT + KK) 572 264 308

Positive for STH 195 (34.1) 103 (39.0) 92 (29.9) 0.021
Positive for A. lumbricoides 115 (20.1) 70 (26.5) 45 (14.6) <0.001
Positive for T. trichiura 67 (11.7) 30 (11.4) 37 (12.0) 0.810
Positive for hookworm 68 (11.9) 36 (13.6) 32 (10.4) 0.232

KT = Kato thick; KK = Kato-Katz.

a
Chi-square test.

STH infections was 5.9%. There was no significant difference noted
in the prevalence of heavy intensity STH infections between the
two groups (P = 0.1). Light and moderate to heavy infections with
A. lumbricoides were significantly higher in IP children than in non-
IP children (P = 0.07). The differences in the distribution of infection
among the intensity classes of T. trichiura and hookworm infections
between IP and non-IP children were not statistically significant.
The prevalence of heavy intensity STH infections and the distribu-
tion according to the intensity of a specific STH infection are shown
in Table 3.
The most common co-infection was seen between A. lum-
bricoides and hookworm with an overall prevalence of 5.8%.
In addition, co-infection between these two species among IP
children was observed to be significantly higher than in non-
IP children (P = 0.038). There was no significant difference in
the prevalence of other co-infections between IP and non-IP
children (Table 4). Other findings included infections with het-
erophyids (5.6%), Schistosoma japonicum (1.2%), E. vermicularis
(1.0%), and Echinostoma sp. (0.2%) in a small minority of chil-
dren.
3.2. Nutritional status assessment
Anthropometric data were gathered from 556 of the 572 chil-
dren who submitted their stool samples (with 358 children who
were 5–10 years old). Of the 358 children, 107 (29.9%) had below
normal WFA. Among the 556 participants, the proportion of chil-
dren with below normal HFA and BMI for age was 42.8% and 14.9%,
respectively. Nutritional status data showed higher prevalence of
below normal WFA and HFA and lower prevalence of below normal
BMI for age among IP children as compared with non-IP children.
However, the noted differences were not found to be statistically
significant (P > 0.05) (Table 5).
Of the 555 children with measured hemoglobin concentrations,
below normal levels were observed in 8.3% of the participants.
Prevalence of below normal hemoglobin levels was observed to be
higher in IP school children (9.6%) than in non-IP children (7.1%),
the difference of which was not statistically significant (P = 0.3)
(Table 5). The overall mean hemoglobin level of IP and non-IP
children was 12.57 ± 1.19 g/dL which is above the cut-off value of
11.0 g/dL.

Table 3
Prevalence of heavy intensity STH infections, distribution according to intensity of each specific STH infection, and geometric mean egg counts per STH species in IP and
non-IP children in selected municipalities in Davao del Norte (November 2009).

Total IP Non-IP P-value

No. (%) No. (%) No. (%)

Examined (KK) 510 232 278

Heavy intensity STH infections 30 (5.9) 18 (7.8) 12 (4.3) 0.100a
Positive for A. lumbricoides (KK) 101 (19.8) 60 (25.9) 41 (14.8) 0.002a
None 409 (80.2) 172 (74.1) 237 (85.2)
Light 72 (14.1) 42 (18.1) 30 (10.8)
Moderate–heavy 29 (5.7) 18 (7.8) 11 (4.0) 0.007a
A. lumbricoides GMEC (epg) 2.77 5.12 1.51
Positive for T. trichiura (KK) 58 (11.4) 26 (11.2) 32 (11.5) 0.914a
None 452 (88.6) 206 (88.8) 246 (88.5)
Light 57 (11.2) 25 (10.8) 32 (11.5)
Moderate–heavy 1 (0.2) 1 (0.4) 0 (0.0) 0.666b
T. trichiura GMEC (epg) 0.70 0.68 0.71
Positive for hookworm (KK) 63 (12.4) 34 (14.7) 29 (10.4) 0.149a
None 447 (87.7) 198 (85.3) 249 (89.6)
Light 62 (12.2) 34 (14.7) 28 (10.1)
Moderate–heavy 1 (0.2) 0 (0.0) 1 (0.4) 0.135b
Hookworm GMEC (epg) 0.79 0.97 0.66

KK = Kato-Katz.
a
Chi-square test.
b
Fisher’s exact test.
S16 V.Y. Belizario Jr. et al. / Acta Tropica 120S (2011) S12–S18

Table 4
Co-infection rates between and among STH and S. japonicum in IP and non-IP children in selected municipalities in Davao del Norte (November 2009).

Total IP Non-IP P-value

No. (%) No. (%) No. (%)

Examined (KT + KK) 572 264 308

A. lumbricoides + T. trichiura co-infections 19 (3.3) 11 (4.2) 8 (2.6) 0.300a
T. trichiura + hookworm co-infections 13 (2.3) 7 (2.7) 6 (1.9) 0.574a
A. lumbricoides + hookworm co-infections 33 (5.8) 21 (8.0) 12 (3.9) 0.038a
A. lumbricoides + T. trichiura + hookworm co-infections 10 (1.7) 6 (2.3) 4 (1.3) 0.376a
Any 1 STH + S. japonicum co-infections 2 (0.3) 0 (0.0) 2 (0.6) 0.190a

KT = Kato thick; KK = Kato-Katz.

a
Chi-square test.

4. Discussion plished through program monitoring and evaluation, taking into

Results of the parasitologic survey showed an overall cumula-
tive STH prevalence of 34.1%, almost 40% lower than the cumulative
prevalence reported in the baseline survey of school children for
the IHCP initiated about three years ago (Belizario et al., 2009).
Similarly, prevalence of heavy intensity infections was 5.9%, almost
75% lower compared with that in the initial survey (Belizario et al.,
2009). The lower prevalence rates and much lower intensities of
infection may be a result of ongoing helminth control initiatives.
These include deworming in schools under the DepEd conducted
every January and July and MDA for the National Lymphatic Filar-
iasis Elimination Program (NFEP) conducted every November in
endemic areas.
Cumulative STH prevalence observed in this study was signif-
icantly higher in IP children than in non-IP children. This finding
is consistent with results of studies from other countries wherein
indigenous people were more commonly infected with parasitic
infections compared with non-indigenous groups (Scolari et al.,
2000; Hotez, 2008). Evidences show that ethnicity, particularly
in conjunction with poverty, contributes strongly to disparities
in health between population groups (WHO, 2007). The United
Nations Permanent Forum on Indigenous Issues (2005) declared
that children born into indigenous families often live in remote
areas where governments do not invest in basic social services. The
major consequence of this issue is that indigenous youth and chil-
dren have limited or no access to services such as health care and
quality education. These IP communities may have limited access
to sanitary toilets and clean water, a condition which contributes
to increased risk of transmission of STH and reinfection (de Souza
et al., 2007). It is also important to look into the factors that may
predispose IP children to helminth infection. This can be accom-
consideration access of the IP communities to health services like
MDA, access to and utilization of sanitary toilets, access to health
education, as well as knowledge, attitudes and practices, pertaining
to personal hygiene.
A. lumbricoides prevalence among IP school children were signif-
icantly higher compared with non-IP children, while the prevalence
of T. trichiura and hookworm between the two groups were not
significantly different. The finding which pertains to the difference
in A. lumbricoides prevalence is consistent with a previous study
where A. lumbricoides prevalence was found to be higher in indige-
nous children than in urban children. Similarly, the previous study
reported no significant difference between T. trichiura prevalence
rates among indigenous and urban school children (Scolari et al.,
2000).
Other intestinal helminths were observed in this study. They
were identified as Echinostoma sp., E. vermicularis, heterophyids
and S. japonicum. It may be important to look at knowledge and
practices in the community that contribute to the transmission of
these helminths (Belizario et al., 2004). Praziquantel is the recom-
mended treatment for schistosomiasis and food borne helminths
such as Echinostoma sp., and heterophyid infections, while alben-
dazole or mebendazole is recommended for E. vermicularis (Drugs
for Parasitic Infections, 2002). Control of these parasitic infections
treated with praziquantel may be integrated as part of the Schis-
tosomiasis Control Program. This drug-based approach may be
applied in putting together the different control programs by tak-
ing into consideration the different helminths that are treated by
the same anthelminthic drug (WHO, 2006).
Double infection with A. lumbricoides and hookworm was
observed to be significantly higher among IP school children com-
pared with non-IP school children in this study. Polyparasitism

Table 5
Comparison of the nutritional status indicators between IP and non-IP school children in selected municipalities in Davao del Norte (November 2009).

Parameters Total IP Non-IP P-value

No. (%) No. (%) No. (%)

No. of school children aged 5–10 yrs old 359 (100.0) 176 (49.0) 183 (51.0)
WFA
Below normal 107 (29.9) 53 (30.3) 54 (29.5)
Normal 248 (69.3) 122 (69.7) 126 (68.9)
Above normal 3 (0.8) 0 3 (1.6) 0.360b
No. of school children aged 5–19 yrs old 556 (100.0) 260 (46.7) 296 (53.2)
HFA
Below normal 238 (42.8) 117 (45.0) 121 (40.9)
Normal 316 (56.8) 142 (54.6) 174 (58.8)
Above normal 2 (0.36) 1 (0.38) 1 (0.34) 0.673b
BMI for age
Below normal 83 (14.9) 38 (14.6) 45 (15.2)
Normal 469 (84.4) 221 (85.0) 248 (83.8)
Above normal 4 (0.7) 1 (0.4) 3 (1.0) 0.751b
No. of school children aged 5–19 yrs old with determined Hb 555 (100.0) 260 (46.9) 295 (53.2)
Below normal 46 (8.3) 25 (9.6) 21 (7.1)
Normal 509 (91.7) 235 (90.4) 274 (92.9) 0.287a
a
Chi-square test.
b
Fisher’s exact test.
 V.Y. Belizario Jr. et al. / Acta Tropica 120S (2011) S12–S18
has a considerable impact on children’s health (Beasley et al.,
2002). Co-infections in these areas signify combined and increased
morbidity, and are therefore considered as a public health con-
cern (Utzinger et al., 2003). Efforts to increase MDA coverage as
well as strategies to improve environmental sanitation and access
to safe water, to increase awareness and to promote personal
hygiene and health practices should be considered. Infections with
other helminths such as heterophyids and S. japonicum were also
observed in this study, which suggest the need to consider delivery
of drug combinations (albendazole/mebendazole plus praziquan-
tel) in co-endemic areas. Safety of drug combinations, looking at
adverse reactions, drug delivery systems, and community accept-
ability can be explored. Cost-analysis and cost-effectiveness studies
may help assess feasibility of combined helminth control strate-
gies. In the same way, many of these parasitic infections are a
result of poor environmental sanitation. Improvements in sanita-
tion by increasing access to sanitary toilets and safe water, and
efforts towards influencing health behaviors and proper personal
hygiene can address most, if not all, of these helminths altogether.
A major concern in diagnosis is the limitation in the detection
of helminth infections by microscopists in peripheral health care
settings. In this study, the sensitivity of field microscopists for the
detection of STH infections was low at 64.3%. This low sensitivity
exemplifies the continuing challenges in the laboratory diagno-
sis of helminth infections that have been cited in earlier literature
from the Philippines (Belizario et al., 2007c; Belizario et al., 2008).
Studies show varying sensitivities of a single Kato-Katz smear for
the detection of STH infections and Schistosoma, from as high as
90% (Tarafder et al., 2010) to as low as 8% (Booth et al., 2003) in
areas with low intensity infections. Furthermore, the sensitivity of
Kato-Katz is affected by day-to-day variation in egg output of the
parasites and the relatively rapid degeneration of hookworm eggs
with time (Knopp et al., 2008). In the case of disease surveillance
for program monitoring, poor sensitivity may provide a less accu-
rate picture of the current magnitude of disease in a given area or
community. This may be misinterpreted as having achieved satis-
factory disease control. Therefore, there is a strong need for capacity
building on laboratory diagnosis in different health facilities which
include local health units and hospitals. A quality assurance scheme
to ensure accurate diagnosis of helminth infections will play an
important role in the prevention of morbidity and complications
as well as in the monitoring of disease control programs.
In this study, it has been demonstrated that 29.9% of all those
examined (IP and non-IP children) were underweight, and 42.8%
were stunted. These rates were higher compared with those
reported in the 7th National Nutrition Survey of the Food and
Nutrition Research Institute (FNRI) where 25.6% and 33.1% of chil-
dren were underweight and stunted, respectively (FNRI, 2009). It is
worth noting that the higher prevalence of STH infections, preva-
lence of heavy intensity infections and prevalence of co-infections
in IP children were observed alongside higher proportions of IP chil-
dren with below normal WFA and HFA as compared with non-IP
children. Malnutrition is one of the complications of STH infections
that eventually lead to growth stunting (Moore et al., 2001). More-
over, multiple helminth infections may have combined impact on
nutrition, especially during childhood (Pullan and Brooker, 2008).
However, other factors that affect the nutritional status should also
be considered. Dietary practices and availability of food with essen-
tial nutrients influence nutritional status (Mosley and Chen, 1984;
Birch, 1972). Non-ownership of land and livestock has also been
identified as risk factors contributing to malnutrition (Owor et al.,
2000). Further studies on factors that influence nutritional status
of IP and non-IP children such as eating habits may be explored.
Hemoglobin determination was used as another indicator to
define nutritional status of children. Results of hemoglobin deter-
mination are highly correlated with hookworm infections where
S17
anemia is the most common complication. In this study, there
was no significant difference between the prevalence of ane-
mia in both IP and non-IP school children. Prevalence of anemia
among the study participants (8.3%) was lower compared with
another local study that reported a prevalence of anemia (21%,
hemoglobin < 11.0 g/dL) in elementary school children (Solon et al.,
2003).
Cumulative prevalence among IP children was observed to be
significantly higher compared with that among non-IP children.
In addition, A. lumbricoides prevalence, prevalence of moderate to
heavy intensity ascariasis, as well as prevalence of A. lumbricoides-
hookworm co-infections were also found to be significantly higher
among IP children. These findings signify the need for more atten-
tion to IP children who are at higher risk of morbidity due to
helminth infections. Access of IP communities to quality health ser-
vices and access to sanitary toilets and clean water must be ensured.
The LGUs, in collaboration with the DepEd, can help guarantee that
these services reach the IP children and are sustained. Prevalence
rates of anemia and below normal anthropometric parameters
between the two groups were not significantly different. Fur-
ther studies to determine factors that contribute to the higher
prevalence of STH and prevalence of anemia among IP groups
are recommended. Program monitoring and evaluation including
household survey on environmental sanitation, personal hygiene
and dietary practices, MDA acceptability and coverage may be con-
ducted in order to identify contributory factors. Data from these
studies may be used to create an approach that would cater to the
needs of IP communities.
Acknowledgments
The project team would like to extend its gratitude to the offi-
cials and staff of the Department of Health Central Office; the
DOH-Center for Health Development XI and the Provincial Health
Team Office; the Department of Education Division Office of Davao
del Norte; the National Commission on Indigenous Peoples Region
XI; the local government units of the province of Davao del Norte
and the municipalities of Carmen, Kapalong, San Isidro and Sto.
Tomas; and the municipal tribal leaders of the selected municipali-
ties. The team also acknowledges the contributions of Ms. Kara Mae
Matias for the assistance during project implementation and of Ms.
Kathy Salazar for the provision of support on statistical analysis.
Special thanks to the World Health Organization for providing the
research grant and technical support for the study.
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