Nghiên cứu thực trạng, một số yếu tố liên quan đến nhiễm giun truyền qua đất ở học sinh tiểu học người Ê đê tại huyện Krông Pắc, tỉnh Đắk Lắk và hiệu quả can thiệp (2015-2016)

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habits of living, eating and farming are outdated.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).

2
NOVELTY AND SCIENTIFIC SIGNIFICANCE OF THE THESIS
1. Novelty
- The study presents a picture of soil-transmitted helminth infection
in Ede primary school children in Krong Pac district, Dak Lak province.
Results showed that they were mainly infected with hookworms.
- The study employed the method of culture and species
identification of hookworm by morphology and molecular biology and
the hookworm was identified as Necator americanus. The results were
published in a recognized international journal.
1. Scientific significance
The thesis results revealed the prevalence, intensity of soiltransmitted helminth infection and some related factors including: no use
of latrines at home, at school; open defecation; no washing hands with
soap after defecation; going barefoot to the field and at home; unhygienic
latrines; and poor knowledge of parents about helminths and their effects.
The average Hb and Hct of the infected students were lower than that of
the uninfected ones. The thesis also determined the role of
communication and education in the prevention of soil-transmitted
helminthiasis in primary school children.

THESIS STRUCTURE
The thesis consists of 126 pages (excluding references and
appendices) divided into the following sections: Introduction (2 pages),
literature review (33 pages), study subjects and methods (25 pages),
results (30 pages), discussions (32 pages), conclusions (2 pages), and
recommendations (1 page). There are 120 references including 85
Vietnamese references and 35 English references, 31 tables, 16 figures,
and 8 appendices.

3
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

estimated 25% of the world’s population are infected with STH infections
worldwide. Infections are widely distributed in tropical and subtropical
areas. In 1995, WHO reported 1.5 billion people infected with hookworm
and 65,000 people died from hookworm each year.
1.3.1.2. STH infection in school children
STH infection such as roundworm, whipworm, and hookworm is
very common in school-age children with the highest prevalence and
intensity in tropical and subtropical areas. A high prevalence of STH


4
infection among school-age children has been reported in many countries
such as Panama, China, USA, Mexico, and Colombia. They realise that
the prevalence (70 - 95%) is the highest in children aged 5 to 9 years old,
then decreases by age and reaches the lowest level of 10 - 50% in adults.
WHO, 2017 revealed that over 600 million school-age children
live in areas where these parasites are intensively transmitted, and are in
need of treatment and preventive interventions.
1.3.2. STH infection in Vietnam
1.3.2.1. STH infection in the community
According to inadequate data collected from provinces all over the
country, there are an estimated 60 million roundworm infections, 40
million whipworm infections and 20 million hookworm infections.
The prevalence of roundworm infection in the North is the highest: 8095% in the Northern Delta, 80-90% in the midlands, 50-70% in the
mountainous areas, and 70% in the coastal areas. In the Central of Vietnam,
the prevalence is lower: 70.5% in the delta, 38.4% in the mountainous area,
and 12.5% in the coastal area. In the South, the prevalence is 45-60% in the
delta, below 10% in the Cuu Long delta, and 10-25% in the Highlands.
Whipworm is distributed as follows: In the north: 58-89% in the delta, 38-41%
in the midland, 29- 52% in the mountainous area, and 28-75% in the coastal

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.


5
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

as well as external factors (temperature, humidity, oxygen, light , pH of
soil...) have an important influence.
1.6. Diagnosis and treatment of STH infections
Ascariasis (the disease caused by roundworm) and Trichuriasis
(the disease caused by whipworm) have no specific clinical signs.
Anemia is a manifestation of hookworm disease in the late stage,
especially severe infection can cause a change to specific skin color
(yellow gold ), edema and signs of heart, liver, or kidney failure.
The diagnosis of STH infection is mainly based on faecal
examination for eggs, which is a simple and accurate method.
- Currently, roundworm and hookworm are treated with
Albendazole, Mebendazole and Pyrantel-pamoat. And Albendazol and
Mebendazol are used for treatment of whipworm.
- Deworming for primary schools from 2000 but up to now, the
helminthic infection is so high.


6
Chapter 2:
STUDY SUBJECTS AND METHODS
2.1. Subjects and location of the study
- For evaluation of STH infections and anemia:
+ Ede primary school children (aged 6-12 years old) in Krong Pac
district, Dak Lak province:
Ly Thuong Kiet primary school, Krong Buk commune: 300 Ede
students.
Ngo Gia Tu primary school, Tan Tien commune: 309 Ede students.
Ly Tu Trong primary school, Ea Uy commune: 316 Ede students.
No Trang Long primary school, Ea Yong commune: 354 Ede
students.

- 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


7
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:

We use the formula:
n=

( Ζ1−α / 2 + Ζ1−β ) 2 [ P1 (1 − P1 ) + P2 (1 − P2 )]

( P1 − P2 ) 2

- Where:
+ P1: The expected prevalence of worm infections through the
first stage of the study which was 75% (0.75).
+ P2 The expected prevalence after intervention which was 45%
= 0.45 (decreased 30% in comparison with before intervention).
+ α: The significance level which was defined as 0.05 => Z1-α/2 = 1.96
+ β: It is 0.10 => Z1-β = 1.28


8
Putting this into the formula we have a theoretical sample size n
= 73.06. We took 75 pupils in each intervention school. Therefore we had
150 pupils for intervention in total.
2.4. Techniques used for information collection
2.4.1 KAP survey
2.4.2. Kato-Katz technique
2.4.3. Harada Mori Culture
2.4.4. Molecular biology (PCR with ITS1)
2.4.5. Blood test for hemoglobin (Hb) and hematocrit (Hct)
Hb and Hct were measured using HemoCue
2.4.6. Data processing methods
- The data collected in the study were processed using biostatistical
method and SPSS 11.5 software.

- 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.


9
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

55.1
142
44.9
316
NGT (3)
157
52.2
144
47.8
301
NTL (4)
152
52.2
139
47.8
291
Total
635
52.7
571
47.4
1206
p1,2,3,4
> 0.05
> 0.05
> 0.05
Notes: LTK: Ly Thuong Kiet primary school; LTT: Ly Tu Trong primary
school; NGT: Ngo Gia Tu primary school; NTL: No Trang Long
primary school.
Comments: The total number of pupils in 4 study schools was 1206,

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

NGT (3)
301
2
0.7
1
0.3
52
17.3
NTL (4)
291
5
1.7
1
0.3
31
10.7
Total
1206
24
2.0
4
0.3
275
22.8
P
p(1,2) – (3,4) < 0.05
Comments: Stool examination by Kato-Katz technique for 1206
students showed that the overall prevalence of soil-transmitted helminth
infection was 25.0% (12.7 - 35.8%).

10
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

3,7 ± 4,4

1

0,2

103

85,4 ± 6,8

NGT (3)

2

0,2± 0,1

1

0,1

52

22,5 ± 4,9

NTL (4)

5

3,0 ± 2,6

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 <999 eggs per gram of feces).
3.1.2. Anemia in the pupils infected with STHs
Table 3.4. The mean values for hemoglobin and hematocrit

Infected
School

No. of
Mean
Mean
samples value for value for
Hb (g/dL) Hct (%)

Uninfected
Mean
value for
Hb (g/dL)

Mean
value for
Hct (%)

P

LTK (1)
LTT (2)

298
316

11.3 ± 1.3 33.1 ± 3.7 12.5 ± 1.1 36.5 ± 3.4 < 0.05

NGT (3)

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 <0.05.
3.1.3. Some factors related to the knowlege, attitudes, and practices of
the pupils toward STH infection
Table 3.5. Relationship between STH infection and latrine use


11
Place of
use

At home

At school

Use

Infected
Uninfected
Total
pupils
pupils
No
122
294
416
Yes
179
611
790
Total
301
905
1206
OR = 1.42; CI95%: (1.07-1.87); p = 0.011
No
138
342
480
Yes
163
563
726

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

Yes
11
31
42
No
290
874
1164
In the field
Total
301
905
1206
OR = 1.07, CI95% (0.50 -2.25), p = 0.851
Comments: Open defecation in the home garden was associated with
soil-transmitted helminth infection.

Table 3.7. Relationship between STH infection and hand washing
practice
Hand washing practice
Infected Uninfected Total
pupils
pupils
No use of soap
187
556
743


12

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

Going barefoot

Infected
pupils
166

Uninfected
pupils
419

Total

Going barefoot
585
Not going
621
135
486
At the
barefoot
field
Total
301
905
1206
OR= 1,43; CI95%: 1,09 - 1,87); p = 0,008
At the
Going barefoot
35
85

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 =

0.0009).
Table 3.9. Relationship between STH infection and status of
household latrines
Status of household
Infected
Uninfected
Total
latrines
pupils
pupils


13
Having no latrines

67

152

219

Having latrines

234

753

987

Total

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 <0.05.
Table 3.10. Relationship between STH infection and the hygiene of
household latrines
Hygiene of
Infected
Uninfected
Total
latrines
pupils
pupils
Unhygiene
234
548
782
Hygiene
67
357
424
Total
301

905
1206
OR= 2.28, CI95% (1.81 – 3.57), p < 0.001
Comments: There was an association between the use of unhygienic latrines
and STH infection (29.9% vs. 15.9%) with OR= 2.28, CI95% (1.81-3.57), p
< 0.01.
3.2. 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.
3.3. Evaluation of the intervention effectiveness with albendazole
combined with education and communication
3.3.1. The prevalence of STH infection after intervention
Table 3.11. The prevalence of STH infection before and after 3 and 6
months of intervention


14
Time

Before
intervention
(0)
After 3 months
of intervention
(3)
After 6 months
of intervention
(6)

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

infecti
ons

Prevalenc
e (%)

97

32.55

307

31

10.10

286

52

18.18

290

62

21.38

265

76

28.68

EI-A3-0= 71.76%; p3-0
EI-B3-0= 44.15%;
<0.01
p3-0 <0.01
EI-A6-0= 40.21%; p6EI-B6-0= 11.88;
p6-0 >0.05
0<0.01
IE3-0 = 27.61% ; p3-0 < 0.01
IE6-0 = 28.33%; p6-0 < 0.01

Comments: 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 <0.01.

3.3.2. Intensity of STH infection after intervention
Table 3.12. Intensity of infection before and after 3 and 6 months of
intervention at Ly Tu Trong and Ly Thuong Kiet school
Intervention school
Control school
(Ly Tu Trong)
(Ly Thuong Kiet)
Time
Round
Whip Hookw Round Whip Hookw
worm
worm

orm
worm worm
orm


15
Before
intervention (0)

1,2±2,4

0,2±0,1 75,2±5,7 3,7±4,4 0,2±0,1 85,4± 6,8

After 3 months
0
0,1±0,1 7,8±3,0 0,2±0,1 0,1±0,1 23,9±3,2
of intervention
(3)
After 6 months
0,2
0,1±0,1 28,9±3,7 3,1±0,2 0,1±0,1 56,6±4,5
of intervention
(6)
P
p3-0 < 0.05 p>0.05
p3-0 <
p3-0 <
p>0.05
p3-0 <
0.05

0.05
0.05
p6-0 < 0.05
p6-0 <
p6-0 <
p6-0 <
0.05
0.05
0.05
Comments: Because most of the cases were hookworm infections, we
looked at the intensity of hookworm infection before intervention at the
two similar schools (75.2 EPG and 85.4 EPG with p> 0.05); reinfection
(new infection) after 3 months in interventive school was 7.5% and in
control school was 15.7%; reinfection after 6 months in preventive
school was 18.6% and in control school was 26.0%.
Table 3.13. Latrine use practices among students before and after
intervention
Intervention
Control school Effectiveness
school
of
Content
(Ly Thuong Kiet)
intervention
(Ly Tu Trong)
(%)
Before
After
Before
After

(n=303) (n=303) (n=298) (n=290)
Latrine Number
128
238
207
233
use at
%
(42.2)
(78.6)
(69.5)
(80.3)
70.8
home
p < 0.01
EI %
86.3
15.5
Latrine Number
77
211
254
233
use at
%
(25.4)
(69.6)
(85.2)
(80.3)
168.2

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


16
Before
After
Before After
(%)
(n=303) (n=303) (n=298) (n=290)
Number% 242
72
91
90

Defecatio
(79.9)
(23.8)
(30.5) (31.0)
68.6
n in the
p < 0.01
EI %
70,2
1,6
garden
Number
22
2
109
92
Defecatio
%
(7.3)
(0.7)
(36.6) (31.7)
77.0
n in the
p < 0.01
EI %
90.4
13.4
field
/forest
Comments: After intervention, the percentage of open defecation (in the

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)

intervention
(%)
Before After
(n=298) (n=290)
73
150
(24.5) (51.7)
180,0
p < 0.01
111.0
146
120
(49.0) (41.4)
15.5

72.2
p < 0.05

Comments: After intervention, the percentage of pupils drinking
unboiled water and eating raw vegetables decreased significantly.
Table 3.16. The practice of going barefoot among pupils before and
after intervention
Content

Intervention
school
(Ly Tu Trong)

Control school Effectiveness
(Ly Thuong Kiet)

of
intervention


17
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

%
(9.9)
(1.7)
(11.7)
(7.2)
p < 0.05
to the
EI %
82.8
38.5
field
Going Number
195
74
139
156
24.5
barefoot
%
(64.4) (24.4) (46.6) (53.8)
p < 0.05
at home EI %
40,0
15,5
Comments: The table shows that the percentage of students going
barefoot to the field, to the school and at home dropped significantly for
the intervention school compared to the control school.
Chapter 4: DISCUSSIONS
4.1. Situation and some related factors to soil-transmitted helminth
infection among Ede primary school children in 4 study schools

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


18
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 <0.05).
Hookworm infections in LTK và LTT were much more than in NGT và
NTL (29.9% and 32.6% vs. 16.9% and 10.7%, p <0.05). Both the two
schools selected for intervention, i.e. Ly Tu Trong and Ly Thuong Kiet
schools had high STH infection rates and the difference between these
two schools was not statistically significant at p> 0.05.
Also conducted in Dak Lak, the study by Nguyen Chau Thanh

(2009) showed that the prevalence of STH infection among primary
school pupils in two communes of Buon Don district, Dak Lak province
was 37.07%, in which roundworm infection was 1.22%, whipworm
0.78%, and hookworm 35.05%. Phan Van Trong et al. (2017) found that
the prevalence of STH infections among primary school pupils in
Cu'Mgar, Dak Lak was as low as 15.67%, and hookworm was the most
dominant (roundworm: 2.67%, whipworm: 1.67%, hookworm: 13.00%).
Yapi et al. (2016) revealed hookworm, whipworm, and roundworm
infections in primary school pupils in Côte d'Ivoire in 2012 were 17.2%,
1.2%, and 1.9% respectively.
- Infection intensity among the students
The intensity of STH infections at 4 study school was mild (36.00
- 218.0 eggs per gram of feces < 999 eggs per gram of feces).
Two intervention schools had the higher hookworm infection
intensity than two control schools (p (1+2) – (3+4) < 0,05). However, the
infection intensity between two intervention schools as well as between
two control schools was of no statistically significant difference (p 1-2
>0.05; p3-4 >0.05).
Similarly, the study by Than Trong Quang also revealed that the
intensity of STH infection in two communes of Hoa Xuan and Ea Tieu in
Dak Lak was mild.
4.1.2. The situation of anemia among the primary school students
infected with STHs
- Mean values for Hemoglobin and Hematocrit among the students


19
Of the 4 surveyed schools for anemia based on the average Hb and
Hct level, three schools showed an association between anemia and STH
infections with p <0.05.

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

school. Up to 33.2% of the students did not use home latrines but 37.6%
of the students defecated in the garden and in the field.
- Relationship between STH infection and hand washing practice


20
Those students who did not wash their hands with soap after
defecation were at 2.88 times higher risk of intection than those did (OR
= 2.88; CI95%: 2.12 – 3.91; p = 0.0001).
We did not find any statistically significant difference in the risk of
STH infections between the group using and the group not using soap to
wash hands before eating (OR = 1.07; CI95%: 0.77 - 1,49; p = 0.674).
- Relationship between STH infections and going barefoot
Those students going barefoot to the field and around the house
were at higher risk of infection than those not (To the field: OR = 1.43;
CI95%: 1.09 - 1.87); p = 0.008, and around the house: OR = 1.58;
CI95%: 1.20 - 2.10; p = 0.0009).
However, no correlation between the group going barefoot to
school and the group not going barefoot to school was found (OR = 1.27;
CI95%: 0.82 - 1.96; p = 0.261 ).
Both the study by Le Huu Cau et al. (2017) and the study by Phan
Van Trong et al. (2017) also showed the lower percentage of students
going barefoot than in our study (26.74% and 24.57% vs. 48.50% 58.62). However, the study at 2 primary schools of Lao Cai by Vo Thi
Thanh Hien (2010) revealed the high rate of going barefoot: around the
house 62.6%, to the field 41,4%, to the school 13.3%.
- Relationship between STH infection and status of household latrines
The pupils in the families without latrines were more infected with
STHs than the pupils in the families with latrines; the association was
statistically significant at p < 0.05.
- Relationship between STH infection and the hygiene of household

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 <0.01. The interventional
effectiveness index in the intervention school and control shcool was

71.76% and 44.15% respectively after 3 months, and 40.21% and 11.88%
respectively after 6 months; the intervention effectiveness was 28.33%.
Thus, the intervention effectiveness at the intervention school was
significantly higher than that of the control school with p < 0.01 after 3
months and 6 months.
4.3.2. Intensity of STH infection after intervention
- Intensity of STH infection before and after 3 and 6 months of
intervention at Ly Tu Trong and Ly Thuong Kiet school
Infections were mild.
Because most of the cases were hookworm infections, we looked
at the intensity of hookworm infection before intervention at the two
similar schools (75.2 EPG and 85.4 EPG with p> 0.05); reinfection (new
infection) after 3 months in interventive school was 7.5% and in control
school was 15.7%; reinfection after 6 months in preventive school was
18.6% and in control school was 26.0%
According to Speich et al. (2016), the reinfection rate after 18
weeks among primary school students in Tanzania was 34.6% for
roundworm, 37.2% for whipworm, and 25.0% for hookworm.
- Latrine use practices among the students before and after intervention


22
At the intervention school, home latrine use increased from 42.2% to
78.6%, the efficiency index was 86.3%. Thus, the intervention effectiveness
was 70.8%; the difference was of statistical significance at p < 0.01.
School latrine use for the intervention school rose from 25.4% to 69.6%
with an efficiency index of 174.0%. Thus, the intervention effectiveness was
168.2%; the difference was statistically significant at p < 0.01.
- Open defecation practices among the students before and after
intervention

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


23
The percentage of pupils going barefoot to the field, to the school
and at home dropped significantly for the intervention school compared

to the control school. The efficiency index for each indicator at the
intervention school was higher than that in the control school, i.e. 18.7%,
44.3%, and 24.5% respectively. The difference was statistically
significant at p < 0.05.
CONCLUSIONS
1- Situation and some related factors to soil-transmitted helminth
infections among Ede primary school children in 4 study schools
1.1. Situation of STH infections among the students
The prevalence of STH infections among Ede primary school
children in Krong Pac district, Dak Lak province in 2015 was 25.0%, in
which hookworm infection accounted for the highest percentage of
22.7%, followed by roundworm (2.0%) and whipworm (0.3%). Infection
was not different between males and females. Most of the cases were
mild. Average Hb and Hct in the infected group were lower than that in
the non-infected group.
1.2. Some related factors to STH infections:
Some related factors to STH infections in Ede primary school
children included: no use of latrines at home, at school; open defecation
in the home garden; no washing hands with soap after defecation; going
barefoot to the field and at home; and no households latrines or
unhygienic latrines.
2- Species composition of hookworms
By morphology and molecular biology, the hookworm was
identified as Necator americanus, belonging to the Ancylostomatidae
family.
3- Effectiveness of interventional treatment with albendazole in
combination with education and communication
Communication education on the prevention of STH infections in
combination with periodical deworming helped reduce the prevalence and
intensity of STH infections and improve the knowledge and practices of

the pupils:


24
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

should focus on educating people not to go barefoot, not to defecate
outside in the environment and to protect their skin from direct contact
to soils.
2. The prevalence of STH infection decreased after 3 months and
increased after 6 months of intervention. New infections were high after
6 months. Therefore, periodical deworming should be conducted every 6
months as recommended by the national deworming program.


25
MINISTRY OF EDUCATION AND TRAINING
HEALTH

MINISTRY OF

NATIONAL INSTITUTE OF MALARIOLOGYPARASITOLOGY AND ENTOMOLOGY
------------------------

BUI KHAC HUNG

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)
Major: Medical Parasitology
Code: 62 72 01 16

THESIS SUMMARY

HANOI - 2018