1
INTRODUCTION
Soil-transmitted helminths include roundworm (Ascaris
lumbricoides), whipworm (Trichuris trichiura), and hookworm
(Ancylostoma duodenale/Necator americanus). These intestinal
parasites are responsible for many human health problems, causing
malnutrition in children [17], [18]. Hookworm also causes anemia,
micronutrient deficiency, and many other complications [16], [61].
In 2017, the World Health Organization reported that more
than 1.5 billion people (25% of the world's population) are infected
with soil-transmitted helminths, mostly in tropical countries in
Africa, America, China, and Western Asia [119].
Dak Lak is one of the Central Highlands provinces where people’s
habits of living, eating and farming are outdated. Therefore, the
prevalence of worm infection in the province is very high, especially in
primary school children, which affects not only the physical development
but the intellectual development of children, especially ethnic minority
children, including Ede children. So, we conducted the study:
Situation and some related factors to soil-transmitted helminth
infection among Ede primary school children in Krong Pac district,
Dak Lak province and effectiveness of intervention (2015-2016)”. The
objectives of the study are:
1- To evaluate the situation and related factors to soil-transmitted
helminth infection among Ede primary school chilren in 4 communes of
Krong Pac district, Dak Lak province in 2015.
2- To identify the species composition of hookworm by morphology
and molecular biology.
3- To evaluate the effectiveness of interventional treatment with
albendazole in combination with education and communication
(2015-2016).



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Chapter 1: LITERATURE REVIEW
1.1. An overview of studies on soil-transmitted helminthiasis
Roundworm, whipworm, and hookworm have plagued humans since
before the era of our earliest recorded history. The diseases they cause are
reported in ancient medical literature.
In Vietnam, the documents on helminthiases as well as remedies to
cure them were mentioned in the 14th century. In the late nineteenth century
and early twentieth century, scientists conducted the first surveys on
helminthiases, i.e. Séguin (1905), Mouzels (1907), Mathis and Léger (1911),
etc. Since 1954, especially after the unification of the country, there have
been thousands of studies conducted on many aspects of helminthiasis,
including soil-transmitted helminth infection such as studies on
epidemiology, pathology, immunology, diagnosis, treatment and prevention.
1.2. Biological characteristics of soil-transmitted helminths (STH)
1.2.1. Life-cycle
Life-cycle of soil-transmitted helminths is simply the process when an
individual is infected with eggs or larvae, then eggs or larvae develop into
adult worms, which produce eggs. The eggs are passed in the faeces.

Human

Environment

1.3. The situation of STH infection
1.3.1. The situation of STH infection in the world
1.3.1.1. STH infection in the community
WHO reports that Ascaridosis (roundworm infection) is the most
common disease and widespread in many countries over the world. An

area; in the Central: 27-47% in the delta, 4.2 - 10.6% in the mountains, 12.7%
in the coast; in the South: 0.5-1.5% in the delta, 1.7% in the Central Highlands.
Similarly, the prevalence of hookworm infection is: in the North: 30-60% in
the delta, 64% in the midland, 61-85% in the mountains, 67% in the coast; in
the Central: 52% in the delta, 61% in the mountains, 68% in the coast; in the
South: 52% in the delta, and 47% in the Central Highlands.
1.3.2.2. The situation of STH infections in primary school children
In Vietnam, many studies on STH infections among primary
school children have been conducted with very different prevalences in
different regions.


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According to the study on the situation of intestinal helminthiasis
among primary school children in some provinces of Vietnam by Nguyen
Thu Huong et al. (2012), the prevalance of worm infection was still
16.3% (ranging from 1.8 to 34.8%) after 10 years of deworming.
1.3.2.3. The situation of STH infections in Dak Lak
STH infection is common in low-income communities, including
Dak Lak. The prevalence of STH infection in Dak Lak in 1996 was
88.97%; in 2002 71.87%; in 2007 46.32%; and 2010 75.1%.
1.4. Impacts of STH infections
Soil-transmitted helminthiases affect people of all ages silently and
in a long-term. They take nutrients, reduce the human body's ability to
do work, and cause memory loss. In children, STH infection results in
malnutrition, anemia, and mental retardation.
1.5. Related factors to STH infections
Roundworm, whipworm, and hookworm are human intestinal
parasites. They are only infectious when eggs develop into larvae.
Therefore, factors affecting the survival and development of their eggs

- For intervention:
Two schools with a similar prevalence were chosen for
intervention. Ly Thuong Kiet is the control school and Ly Tu Trong is the
intervention school.
A total of 100 students with the highest intensity of hookworm
infection were selected for stool sampling (about 10g) for larval culture.
2.2. Study duration
From January 2015 to December 2016.
2.3. Study methods
2.3.1. Study design:
- A descriptive cross sectional method (for objectives 1 and 2).
- A controlled community intervention (for objective 3).
2.3.2. Sample size and sampling


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2.3.2.1. Sample size for studying worm infection and anemia:
We use this formula for calculating the sample size:

where n is the required sample size
p = Expected prevalence
z1-α/2 = confidence coefficient; at a confidence level of 95%, z1-α/2 is 1.96
d = Absolute error, we decided d = 5% (0.05)
Based on the study by Than Trong Quang in 2009 that the
prevalence of intestinal helminthiasis among children in Dak Lak
province was 75.1%, we decided p = 75% (= 0.75). Our theoretical
calculation produced n = 288.
Since the number of Ede pupils in 4 schools was 300, 309, 316 and
354 pupils respectively, we enrolled them all.
2.3.2.2. Sample size for intervention:

- Bioinformatics tools were applied for molecular biology data.
2.5. Research ethics
The students were informed in advance and explained the purpose,
requirement and benefit of the study. They were voluntarily invovled in
the study. They could withdraw their particiaption from the study without
any form of reprimands. Those students who refused to cooperate would
be excluded from the study.


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Chapter 3:
STUDY RESULTS
3.1. Situation and some related factors to soiltransmitted helminth (STH) infection among Ede
primary school children in 4 study schools
3.1.1 STH infection among the pupils
Table 3.1. Sex distribution
Males
Females
Total
School Number Percentage Number Percentage number
%
%
LTK (1)
152
51.0
146
49.0
298
LTT (2)
174

distributed evenly among the schools. The difference in gender was not
statistically significant.
Table 3.2. Prevalence of STH infection in the pupils
Number Roundworm Whipworm
Hookworm
School
of
(+)
%
(+)
%
(+)
%
samples
LTK (1)
298
7
2.4
1
0.3
89
29.9
LTT (2)
316
10
3.2
1
0.3
103
32.6


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Table 3.3. Intensity of infection
Roundworm
Whipworm
Hookworm
Posit
Posi
Positi
ive
EPG
tive
EPG
EPG
ve (+)
(+)
(+)
7
1,2 ± 2,4
1
0,2
89
75,2 ± 5,7

School
LTK (1)
LTT (2)

10


1

0,2

31

13,0 ± 3,1

Total

24

2,0 ± 1,5

4

0,1

275
49,7 ± 8,5
p(1,2) – (3,4) < 0.05
p
< 0.05
> 0.05
p1-2 > 0.05;
p3-4 > 0.05
Comments: The infection intensity for all 4 schools was mild (85.4 eggs
per gram of feces
301

11.3 ± 1.1 33.5 ± 3.4 12.2 ± 1.1 35.7 ± 2.6 < 0.05

NTL (4)

291

Total

1206

11.6 ± 1.2 34.2 ± 3.5 12.4 ± 1.0 36.5 ± 3.0 < 0.05
11.5 ± 1.1 33.6 ± 3.4 12.2 ± 1.1 35.8 ± 3.1 < 0.05

11.6 ± 1.0 33.8 ± 3.0 11.7 ± 1.1 34.5 ± 3.1 >0.05

Comments: Of the 4 surveyed schools, three schools showed an
association between anemia and worm infection with p
Total
301
905
1206
OR = 1.39; CI95% (1.06 -1.83); p =0.013

Comments: Results showed that there was a statistically significant
association between latrine use and soil-transmitted helminth infection.
Table 3.6. Relationship between STH infection and open defecation
Open defecation
Infected
Uninfected
Total
pupils
pupils
Yes
159
371
530
No
142
534
676
In the
Total
301
905
1206
garden
OR = 1.61 CI95%: 1.23 – 2.11; p = 0.0003

Use of soap
51
164
215
Total
238
720
958
OR = 1.07; CI95%: 0.77 – 1.49; p = 0.674
No use of soap
188
389
577
After
Use of soap
59
353
412
defecation
Total
247
742
989
OR = 2.88; CI95%: 2.12 – 3.91; p = 0.0001
Comments: Those pupils who did not wash their hands with soap after
defecation were at 2.88 times higher risk of worm infection.
Before
eating

Table 3.8. Relationship between STH infection and going barefoot

120
school
Not going
1086
266
820
barefoot
Total
301
905
1206
OR= 1.27; CI95%: 0.82 – 1.96; p = 0.261
At home
Going barefoot
201
506
707
Not going
499
100
399
barefoot
Total
305
905
1206
OR= 1.58; CI95%: 1.20 – 2.10; p = 0.0009
Comments: Those pupils going barefoot to the field and at home were at a
higher risk of worm infection than those not (to the field: OR= 1.43; CI95%:
1.09 – 1.87); p = 0.008 and at home: OR= 1.58; CI95%: 1.20 – 2.10; p =


301

905

1206

OR = 1.42; CI95%: 1.01-1.98; p = 0.033
Comments: The table shows that those pupils in the families without
latrines had a higher rate of worm infection than those in the families
having latrines; the association was statistically significant at p
Efficiency
index (EI)
Intervention
Effectiveness
(IE)

Intervention school
(A)
(Ly Tu Trong)
No. No. of Preval
of
infecti
ence
sam
ons
(%)
ples
316
113
35.76

Control school (B)
(Ly Thuong Kiet)
No.
of
sam
ples
298

No. of

76

28.68

EI-A3-0= 71.76%; p3-0
EI-B3-0= 44.15%;

0.05
0.05
p6-0 < 0.05
p6-0

school EI %
p < 0.01
174.0
5.8
Comments: At the intervention school, home latrine use increased
from 42.2% to 78.6%, the efficiency index was 86.3%; school latrine use
rose from 25.4% to 69.6% with an efficiency index of 174.0%.
Table 3.14. Open defecation practices among students before and
after intervention
Intervention
Control school Effectiveness
Content
school
(Ly Thuong
of
(Ly Tu Trong)
Kiet)
intervention


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Before
After
Before After
(%)
(n=303) (n=303) (n=298) (n=290)
Number% 242
72
91
90

garden, field and forest) fell sharply.
Table 3.15. The practice of drinking unboiled water and eating raw
vegatables before and after intervention
Intervention
school
(Ly Tu Trong)
Before After
(n=303) (n=303)
Drinking Number 219
90
unboiled
%
(72.3) (29.7)
water
EI %
39.6
Content

Eating Number 144
65
raw
%
(47.5) (21.5)
vegetables EI %
54.7

Control school Effectiveness
(Ly Thuong
of
Kiet)

of
intervention


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Before After Before After
(%)
(n=303) (n=303) (n=298) (n=290)
Going Number
158
37
120
92
18,7
barefoot
%
(52.2) (12.2) (40.3) (31.7)
p < 0.05
to
EI %
40.0
21.3
school
Going Number
30
5
35
21
44,3
barefoot

4.1.1 Situation of STH infections among the pupils
- Sex distribution of the students
The total number of pupils in 4 study schools is 1206, distributed
quite evenly among the schools. Although males were more than females,
the difference was not statistically significant at p > 0.05.
The study by Phan Van Trong et al. (2017) also showed no
difference in STH infection between male and female students in primary
schools of Cu'Mgar, Dak Lak at p> 0.05 (14.55% vs. 17.04%).
In addition, the study by Vu Thi Lam Binh et al. (2015) showed no
difference in worm infection between male and female primary school
students, too.
- Prevalences of STH infections among the students
Stool examination by Kato-Katz technique for 1206 pupils in 4
primary schools showed that the overall prevalence of infection was
25.0% (ranging from 12.7 to 35.8%), in which hookworm infection was
22.7%, followed by roundworm (2.0%) and whipworm (0.3%) (Table


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3.2). Most of the cases in all the four schools were hookworm infections
with the highest prevalence in Ly Tu Trong (35.8%) and the lowest
prevalence in No Trang Long (12.7%).
There was a difference in the prevalence of STH infection among
schools (LTK: 32.6%, LTT: 35.8%, NGT: 17.9%, NTL: 12.7%, p
Compared to some studies on the association between anemia with
STH infections, the study by Nguyen Van De (1995) on 478 patients with
hookworm infection revealed that red blood cells decreased 74.6%,
hematocrit (Hct) 3.4%, serum iron 12.3%, Hb 51.9% - 91% and mean Hb
8.8-9.7g/dl. A study by Cao Ba Loi (2011) found that the prevalence of
anemia among workers in Phu Tho tea plantation was 44.4% and there was
an association between anemia and worm infection among primary school
children in Lang Son province .
Similarly, Ta Thi Tinh (2011) also showed a link between intestinal
helminthiasis and anemia in one commune of Thanh Hoa province.
4.1.3. Some factors related to the knowlege, attitudes, and practices
of the students toward STH infection
- Relationship between STH infection and latrine use
The study results showed that there was a statistically significant
association between the use of latrines and STH infections. No use of
latrines (both at home and at school) increased the risk of infection, i.e. at
home the risk was 1.42 times higher (OR = 1.42, CI95%: (1.07-1.87); p =
0.011), and at school the risk was 1.39 times higher (OR = 1.39, CI95%
(1.06-1.83), p = 0.013).
The study by Phan Van Trong et al. (2017) showed the percentage of
pupils not using latrines (16.67%) was lower than that of our study.
- Relationship between STH infection and open defecation
Open defecation in the home garden was associated with STH
infections, i.e. increasing the risk of infection to 1.61 times (OR = 1.61;
CI95%: 1.23 - 2.11; p = 0.0003).
However, we did not find this association in the group defecating
in the field and the group not (OR = 1.07; CI95%: 0.50 -2.25; p = 0.851).
The study results by Vo Thi Thanh Hien (2010) showed that the
number of primary school students not using the school toilet accounted
for 8.1%, but there were 17.8% students defecating outside aroung the

latrines
There was an association between the use of unhygienic household
latrines with STH infections (29.9% vs. 15.9%) with OR= 2.28, CI95%
(1.81-3.57), p < 0.01.
4.2. Identification of hookworm species composition by morphology
and molecular biology
By morphology and molecular biology, the hookworm was
identified as Necator americanus, belonging to the Ancylostomatidae
family.
According to Do Duc Tuy (1960), Ancylostoma duodenale
infection was 36.06%, Necator americanus infection was 54.9%, and
mixed infection of these two species was 9.04%. According to Pham Van


21
Than (1968), A.duodenale was 34.39% and N.americanus was 65.61%.
Dao Trong Hoang (1970) revealed that the species composition of
A.duodenale and N.americanus was 30% and 70% respectively. Another
finding by Hoang Thi Kim (1987) showed 5% of A.duodenale and 95%
of N. americanus. And Nguyen Van De (1995) found out that
A.duodenale accounted for 3.1%, and N.americanus shared 96.9 %.
Thus, the prevalence of N.americanus increases over time.
4.3. Effectiveness of interventional treatment with albendazole in
combination with education and communication
3.3.1. The prevalence of STH infections after intervention
- The prevalence of STHs before and after 3 and 6 months of intervention
After 3 and 6 months, the prevalence of STH infection dropped more
at the intervention school in comparison with the control school; the
difference is statistically significant with p
After intervention, the percentage of open defecation (in the
garden, field and forest) fell sharply.
The rate of intervened students defecating in the home garden
decreased from 79.9% to 23.8%, reaching the efficiency index of 70.2%.
This decrease was not found among the control group with an efficiency
index of 68.6%. The difference was statistically significant with p < 0.01.
The rate of intervened students defecating in the field or forest fell
from 7.3% to 0.7% with the efficiency index of 90.4% which is 13.4%
higher than that in the control group. The difference was statistically
significant with p < 0.01.
- The practice of drinking unboiled water and eating raw vegatables
among the students before and after intervention
After intervention, the percentage of students drinking unboiled
water and eating raw vegetables decreased significantly.
The percentage of students drinking unboiled water at the
intervention school decreased from 72.3% to 29.7% with the
efficiency index of 39.6%. Whereas, this rate at the control school
increased, reaching the efficiency index of 180.0%. The difference
was statistically significant at p < 0.01.
The percentage of pupils consuming raw vegetables at the
intervention school dropped from 47.5% to 21.5%, resulting in the
efficiency index of 54.7% which is 15.5% higher than that at the
control school. The difference was statistically significant at p < 0.01.
- The practice of going barefoot among the students before and after
intervention


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The percentage of pupils going barefoot to the field, to the school
and at home dropped significantly for the intervention school compared

the pupils:


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After intervention, the prevalence of STH infections at the
intervention school fell sharply, reaching the efficiency index of 71.8%
after 3 months and 40.2% after 6 months. While these indexes at the
control school were 44.2% and 11.9%, respectively. The intervention
effectiveness after 3 and 6 months was 27.6% and 28.3%, respectively.
The intensity of infection decreased markedly after 3 months of
intervention but tended to increase again after 6 months. New infections
of roundworm and hookworm in the control school were more than in
the intervention school. The knowledge and practice of prevention
among the pupils was improved, i.e. the percentage of students using
household and school latrines at the intervention school was much higher
than that at the control school with the intervention effectiveness of
70.8% and 168.2 %. The rate of open defecation (in the home garden, in
the field, and in the forest) decreased with the intervention effectiveness
of 68.6% and 77.0%. The habit of drinking unboiled water and eating
raw vegetables was also less common among the pupils with the
intervention effectiveness of 180.0% and 72.2%; the difference was
statistically significant. The knowledge about STHs among the
intervened pupils increased from 75.9% to 99.7% with the efficiency
index of 31.4%, however the intervention effectiveness only reached
1.5%. Also, the pupils got familiar with the habit of washing hands
before eating and after defecation, and cutting nails regularly; the
difference was statistically significant.
RECOMMENDATIONS
1. Due to the high prevalence of Necator americanus infection among
the students, skin protection is essential. Communication and education

HANOI - 2018