PREVALENCE OF Schistosoma mansoni AND Giardia lamblia
INFECTIONS AND THEIR ASSOCIATION WITH
ANTHROPOMETRIC MEASUREMENTS IN SCHOOL CHILDREN IN
ADWA TOWN, ETHIOPIA
M.Sc. Thesis
ELSABET AMARE
AUGUST, 2012
HARAMAYA UNIVERSITY
PREVALENCE OF Schistosoma mansoni AND Giardia lamblia
INFECTIONS AND THEIR ASSOCIATION WITH
ANTHROPOMETRIC MEASURIMENTS IN SCHOOL CHILDREN IN
ADWA TOWN, ETHIOPIA
A Thesis Submitted to the Department of Biology, College of Natural and Computational
Sciences, School of Graduate Studies
HARAMAYA UNIVERSITY
In Partial Fulfillment of the Requirements for the Degree of MASTER OF SCIENCE in
Microbiology
By
Elsabet Amare
August, 2012
Haramaya University
ii
APPROVAL SHEET
SCHOOL OF GRADUATE STUDIES
HARAMAYA UNIVERSITY
As thesis research advisors, we herby certify that we have read and evaluated this thesis
prepared, under our guidance, by Elsabet Amare, entitled “Prevalence of Schistosoma
mansoni and Giardia lamblia Infections and their Association with Anthropometric
measurements in School Children in Adwa Town, Ethiopia”. We recommend that it can
be submitted as fulfilling all the thesis requirements.
Sissay Menkir (PhD)
Name of Major Advisor
Tsehaye Asmelash (PhD)
Name of Co. Advisor
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As member of the board of the examiners of the open defenses of the examination, we
certify that we have read and evaluated this thesis properly which was prepared by
Elsabet Amare. We recommended that the thesis can be accepted as fulfilling the
Thesis requirement for the degree of Master of Science in Biology (Microbiology).
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iii
BIOGRAPHICAL SKETCH
The author was born from her father Ato Amare G/Egziabher and her mother W/ro Kibra
Desta in Axum, Central Zone of Tigray, in 1962 E.C. She attended her primary education in
Axum Abrha-We-Atsebeha Primary School and her secondary education in Axum
Comprehensive Secondary School. She did her certificate in Asmara Teacher Training
Institute (Asmara TTI) in 1980 E.C; her diploma in Biology at Abiy-Adi College in 1992 E.C;
her degree of Bachelor of Education in Biology (BEd) in Mekelle University in 1998 E.C. In
her long journey, the author was teaching Biology in different schools starting from
elementary schools to secondary schools until joining Haramaya University for her graduate
study program in Microbiology in September, 2002 E.C.
Life starts from a single cell, and then growth and development proceed; so does my
educational level.
Thanks to the Omnipotent God, his mother (Mariam Dingl) and his entire lover who
strengthened me throughout my career.
iv
DEDICATION
I dedicated this paper to my beloved father, Ato Amare G/Egziabher whom I
wish his soul to rest in peace (heaven/jennet).
v
ACKNOWLEDGMENT
Above all, I want to express my endless thank to the Omnipotent God, his mother (Mariam
Dingl) and his entire lover who strengthened me throughout my career.
I would like to express my deepest gratitude to my advisor, Dr. Sissay Menkir, for his
consistent invaluable advice, close supervision at each and every step of the progress, critical
evaluation and immediate feedback with valuable comments from problem identification up
to the completion of this work as well as for his immediate response for any problems faced
me.
I also want to express my appreciation to Dr. Tsehaye Asmelash for his helpful comments that
supported in my work.
My sincere appreciation is also extended to Dr. Tadesse Dejenie who provided me materials
needed for S. mansoni determination and for his constructive suggestion and openness.
I wish to extend my grateful appreciation to the Ethiopian Ministry of Education (MOE), for
financially supporting to carry out this study, without which this study could not have been
achieved.
I would like to express my heart-felt gratitude to my Brother, Mekonen Tadesse, and my sister
Awetash Meresa for their unreserved moral and material support. I also want to express my
appreciation for their patience. Both of them were with me and helped through the ups and
downs I had during this study.
I also want to express my deep appreciation to Adwa Hospital administrative staff for
chemicals and materials supply needed for this study and letting me use all laboratory
facilities. I give special thanks to the whole members of the staff for their sincere
collaboration in general, and Ato Gebremicael Weldegebriel and Ato Ataklti in particular for
their valuable assistance and moral support.
vi
My great gratitude also goes to all school children who volunteered to participate in the study;
and their teachers those helped me in coordinating them.
My special thanks go to the health professionals serving in Adwa Health Center for their
technical assistance during data collection and laboratory sample examinations.
I would like to express my earnest gratitude to my lovely friend Freweyni Belay and her
husband Ato Melaku , and Mitselal Teklu with her husband Ato Negasie for their material and
moral support.
I also want to extend my admiration to Ato Nega Siyum, W/R Tsigereda, Leul, W/Gebrriel
Haile Abnet, Abrham, G/Hawaria, Ataklti, G/Hana and T/weyni for their all rounded
assistance and moral support.
My genuine appreciation also goes to my family, my sisters, brothers and friends for their
cooperation and moral support.
Last, but not least, I would like to forward my great thanks to those whose names are not
mentioned but contributed to the fulfillment of this study.
vii
LIST OF ABBREVIATIONS AND ACRONYMS
AFEDB
Adwa finance and Economic Development Bureau
BMI
Body Mass Index
CDC
Center for Disease Control
CI
Confidence intervals
CSO
Central Statistic Office
EDHS
Ethiopian Demographic and Health Survey
EHNRI
Ethiopian Health and Nutrition Research Institute
EPG
Egg per Gram of faeces
HAZ
Height for age Z-score
NCCLS
National Committee on Clinical Laboratory standard
NCHS
National center for health statistics
NTD
Neglected Tropical Disease
OR
Odds ratio
SD
Standard deviation
SPSS
Statistical Package for Social Sciences
SRS
Simpler Random Sampling
WAZ
Weight- for- Age Z-score
WHZ
Weight- for- Height Z-score
WHO
World Health Organization
viii
TABLE OF CONTENTS
BIOGRAPHICAL SKETCH
iv
DEDICATION
v
ACKNOWLEDGMENT
vi
LIST OF ABBREVIATIONS AND ACRONYMS
viii
TABLE OF CONTENTS
ix
LIST OF TABLES
xi
LIST OF FIGURES
xii
ABSTRACT
xiii
1. INTRODUCTION
1
2. LITERATURE REVIEW
5
2.1. General characteristics of schistosomes and Giardia lamblia
2.1.1. Schistosomes
2.1.2. Giardia lamblia
2.1.3. Life cycle of schistosomes and Giardia lamblia
2.2. Epidemiology and transmission of schistosomes and Giardia infections
2.2.1. Epidemiology of schistosomiasis and giardiasis
2.2.2. Transmission of schistosome and Giardia lamblia infections
2.3. Factors affecting the epidemiology of schistosomes and Giardia infections
2.3.1. Poverty and Sanitation
2.3.2. Climatic factors and development of water resources
2.3.3. Age dependency
2.3.4. Behavioral and socio-economic factors
2.4. Morbidity and public health effects due to schistosomes and Giardia lamblia
infections
2.5. Diagnosis of schistosomes and Giardia lamblia infections
2.6. Prevention and control of schistosome and Giardia lamblia infections
2.6.1. Prevention
2.6.2. Treatment
2.6.3. Health education
5
5
5
6
9
9
12
13
13
13
14
14
3. MATERIALS AND METHODS
20
3.1. Study area
3.2. Study design
20
21
ix
15
16
18
18
18
19
TABLE OF CONTENTS(Cont…)
3.3. Study population
3. 4.Exclusion criteria
3.5. Sample size determination and sampling procedure
3.6. Methods of data collection
3.6.1. Questionnaire survey
3.6.2. Stool sample collection and examination
3.6.3. Anthropometric measurements
3.7. Data analysis
3.8. Data quality control (QC)
3.9. Ethical considerations
21
21
21
22
22
22
23
24
24
25
4. RESULTS AND DISCUSSION
26
4.1 Prevalence of Schistosoma mansoni and Giardia lamblia infections in school children
26
4.1.1. Prevalence of S. mansoni infection in school children
26
4.1.2. Prevalence of Giardia lamblia infection in school children
29
4.2. Intensity of S. mansoni infection in school children
32
4.3. Socio-demographic characteristics of the study children
34
4.4. Anthropometric measurements
36
4.4.1. Prevalence of stunting, underweight and wasting status among the study subject
aged 6-9 Years
36
4.4.2. Prevalence of underweight and/or thinness in the age group of 10-18 years by
gender
38
4.5. Association of intestinal schistosomiasis and giardiasis with anthropometric
measurement and socio-demographic characteristics of school children
39
4.6. Associated risk factors with S. mansoni and G. lamblia infections in school children
42
5. SUMMARY, CONCLUSION AND RECOMMENDATIONS
46
5.1. Summary
5.2. Conclusion
5.3. Recommendations
46
47
48
6. REFERENCES
49
7. APPENDICES
61
7.1 Appendix: I
7.2 Appendix: II
7.3 Appendix: III
7.4 Appendix: IV
62
63
64
65
x
LIST OF TABLES
Table
page
1. Prevalence of S.mansoni by age and sex of examined children in Adwa schools during
February-April, 2012
28
2. Prevalence of G. lamblia infection by age and sex among school children in Adwa town,
northern Ethiopia from February-April, 2012
31
3. Mean ± SEM egg per gram of facese of S.mansoni identified in examined school children
in Adwa town during February-April, 2012
33
4. Socio-demographic characteristics of the study participants in Adwa elementary schools,
northern Ethiopia from February-April, 2012
35
5. Prevalence of stunting, underweight and wasting status by sex among the study children
aged 6-9 years in Adwa elementary schools during February-April, 2012
37
6. Prevalence of underweight and/or thinness in the age group of 10-18 years by gender
39
7. Relationship between scistosomiasis and giardiasis with nutritional indicators among the
participant children aged 6-9 years
41
8. Major risk factors related with S.mansoni and G.lamblia infections in school children,
Adwa town from February-April, 2012
45
xi
LIST OF FIGURES
Figure
page
1. Life Cycle of schistosomes……………………………...…………………………7
2. Life cycle of Giardia lamblia……………………………………………………. 8
3. Map of Adwa town, Tigray region ………………………………………….….. 20
xii
PREVALENCE OF Schistosoma mansoni AND Giardia lamblia
INFECTIONS AND THEIR ASSOCIATION WITH
ANTHROPOMETRIC MEASURIMENTS IN SCHOOL CHILDREN IN
ADWA TOWN, ETHIOPIA
ABSTRACT
A cross-sectional survey was conducted from February-April, 2012 to determine the prevalence,
intensity and associated risk factors of the S. mansoni and G. lamblia infections and their association
with anthropometric measurements of school children, in Adwa town, northern Ethiopia. Single stool
specimens were collected from 369 subjects aged 6-18 years and examined using Kato-Katz and direct
wet mount methods. Structured questionnaire was also used to obtain the socio-demographic
information and associated risk factors for the parasite infection. Height, weight and body mass index
(BMI) were measured to determine nutritional status of children as stunted, wasted or underweight.
The National Center for Health Statistics (NCHS) median reference was used as cut-off point to
determine malnourishment. Data was analyzed using the SPSS version 16. Out of the 369 children
examined, 194 (52.6%) and 87 (23.6%) were found positive for S. mansoni and G. lamblia,
respectively. Schistosomiasis is significantly associated in male and in age group of 10-14 years of
students (p<0.05). However, no significant differences was observed for giardiasis among gender and
age groups (p>0.05). The mean egg count of S. mansoni was 141.53 eggs per gram of feaces. The
prevalence of wasting, underweight and stunting for 6-9 years old was 12.8%, 32.0% and 25.6%,
respectively, and 38.8% underweight/thinness for aged 10-18 years. There was no statistically
significant association observed between the two parasitic infections and malnutrition (P>0.05).
Significant relation was found between S. mansoni infection and age groups, sex, bathing in stream,
washing cloth in stream, swimming habit in stream, and contact of water during crossing the stream
(P<0.05). Similarly source of water for drinking showed statistically significant association with G.
lamblia (p<0.05). The present study indicated that schistosomiasis, giardiasis and malnutrition were
highly prevalent in the study area. Even though, no association was observed between the parasitic
infections and malnutrition, mass drug treatment, health education on personal and environmental
hygiene practice and awareness about balanced diet was recommended to keep the prevalence of
infections low and to improve nutritional status of school children in the study area.
Key words: Anthropometry, G. lamblia, Intensity, Malnutrition, Prevalence, Risk factors, School
children, S. mansoni.
xiii
1. INTRODUCTION
Intestinal parasites are the causative agents of common infections responsible for significant
public health problems in the world. It is estimated that more than two billion people are live
with unremitting illness as a result of these parasites globally (WHO, 2005). Intestinal
helminth and protozoan infections are among the most common infections worldwide (Barnes
et al., 2009).
The prevalence of parasitic infections with ascariasis, hookworms, giardiasis, schistosomiasis,
cestodes, amebiasis and strongyloidiasis is 20% (1.3 billion), 20% (1.3 billion), 3.3% (200
million), 2.5% (150 million), 1.08% (65 million), 1.0% (60 million), and 0.6% (35 million)
people, respectively globally (Michael, 1997). The high prevalence of the above parasites are
attributed largely to low socio-economic status, poor personal sanitation, absence of safe
water supplies for drinking and other purposes, unsafe waste removal system, especially the
use of facilities to dispose faeces, presence of favorable climatic condition, inadequate
medical care and lack of knowledge and awareness about worms (Tedla, 1986; WHO, 2004;
Montresor et a1, 1998). The variation in prevalence depends on factors such as the
geographical area, the urban or rural setting of the society, the age group composition and the
socio-economical conditions of the study subject (Flanagan, 1992). Prevalence and intensity
are also related and, generally, populations with high prevalence of infection tend to have
high intensity of parasites (Hoffman et al, 1979).
Intestinal parasitic infections can adversely impact host nutritional status in several different
ways. They can depress appetite and nutrient absorption (Hadju et al., 1996), compete for
micronutrients (Stoltzfus et al., 1997) cause nutrient malabsorbtion (Solomons, 1982) or
blood loss resulting in the loss of iron or other essential nutrients (Stoltzfus et al., 1998).
Some infections can have a negative effect on metabolic or nutrient excretion rates
(Stephenson et al., 2000b). The impact of intestinal infections on child nutrition, growth and
development depend on the parasite species and burden (Chan et al., 1994; Oberhelman et al.,
1998) and host immune response (Eckmann and Gillin, 2001). The consequence of infection
1
in children may interfere with growth and development and may limit their school
achievement. The health effects include anemia, growth retardation, lower work capacity and
increased susceptibility to other infections (Koroma et al., 1996).
Schistosomiasis is chronic water-borne parasitic disease caused by blood flukes of the genus
Schistosoma. It ranks second to malaria in terms of posing a great public health and socio
economic threat in affected communities and individuals. Still now, it is a major helminth
infection in many developing countries of the tropics. The disease is endemic in 76 tropical
developing countries (Chitsulo et al., 2000). People become infected when coming in contact
with water containing the infective larval stage called cercariae (Wu and Halim, 2000). There
are five species of schistosomes that cause disease in humans, namely S. mansoni, S.
intercalatum, S. haematobium, S. japonicum and S. mekongi (Gurarie and Seto, 2009).
Recent studies suggest that 779 million people are at risk of schistosomiasis and 207 million
people are infected worldwide (Steinmann et al. 2006). In Africa it is endemic in 46 countries
(Boelee and Madsen, 2006) and majority (80-85%) of schistosomiasis cases are found in subSaharan Africa (Bergquist, 2002). In Ethiopia, both S. mansoni and S. haematobium pose
considerable public health and socioeconomic problem (Erko et al., 1997; Kloss et al., 1988).
It is estimated that 29.89 million people are at risk and of those 4 million are to be infected in
the country (Chitsulo et al., 2000).
The parasite has distinct separate sexes and complex life cycle involving alternation of
generations with the sexual reproduction of adult schistosomes in the definitive vertebrate
host and an asexual multiplication stage in a snail host (Webbe, 1981).
Giardia lamblia is the most common protozoan intestinal parasite isolated worldwide as
causative agents of diarrhoea. Epidemiological studies suggest that the parasite is responsible
for about 5% of acute diarrhoea and 20% of chronic diarrhoeal illness in the world
(Thompson et al., 1993). It is estimated that up to 200 million people have symptoms of
giardiasis with some 500,000 new cases per year worldwide, especially among children
2
(WHO, 1998). The prevalence of giardiasis varies from 2-5% in the developed and 20-30% in
the developing countries (Farting, 1994).
Giardia is transmitted by the feacal-oral route. Infection occurs when infective cysts of G.
lamblia are ingested through contaminated water or food (Meyer and Jarrol, 1980). Symptom
of the disease includes acute watery diarrhoea with abdominal pain, foul-smelling stools
associated with flatulence, abdominal distention and nausea (Ortega and Adam, 1997). The
parasite has a simple direct life cycle consisting of an infective cyst and a vegetative
trophozoite (Ortega and Adam, 1997).
Prevention of intestinal infections can be possible by maintaining good personal hygiene,
proper disposal of fecal material, good water treatment and food sanitation (Backer, 2000).
In Ethiopia, giardiasis is common cause of intestinal infection (Haile et al., 1994). Both
intestinal and urinary schistosomiasis are also endemic and cause considerable health and
economic impact (Kloos et al., 1988). New transmission foci are being discovered in different
parts of the country. The spread of the disease to new localities seem to be extensive
population mobility due to settlement and job opportunities; and water resource development
(Erko et al., 1996). Several epidemiological studies on S. mansoni infections were conducted
in Adwa, (Lemma et al., 1975; Birrie et al., 1994; Lemlem., 2008).
However, there has been no current epidemiological information on schistosomiasis and/or
giardiasis in relation them with anthropometric measurement of school children in the area.
Therefore, it is very crucial to know the recent epidemiological data on the magnitude of S.
mansoni and Giardia lamblia infections and their association with nutritional indicators of the
children. The information obtained from the study can be enabling for the motivation and
implementation of parasite control program. In addition to this, it is believed to serve as a
baseline data for the future study.
3
The general objective of this study was to investigate the prevalence and intensity of
Schistosoma mansoni and Giardia lamblia infections and their relation with anthropometric
measurement and socio-demographic factors of school children in Adwa town.
Specific objectives

To determine the prevalence and intensity of S. mansoni infection among the school children
in the study area.

To determine the prevalence of Giardia lamblia infection among school children in the study
area.

To relate intestinal schistosomiasis and giardiasis with anthropometric measurement and
socio-demographic factors of school children.

To identify major risk factors associated with S. mansoni and G. lamblia infections.
4
2. LITERATURE REVIEW
2.1. General characteristics of schistosomes and Giardia lamblia
2.1.1. Schistosomes
Schistosomes are trematodes or flukes. They are short, bilaterally symmetrical worms. Unlike
many other trematodes, schistosomes exhibit sexual dimorphism and have distinct separate
sexes. Moreover, their thread like appearance is not typical for flukes which are usually flat
and leaf like.” Schisto-soma” means split body, referring to a deep groove running along the
male’s body. The more slender female is held permanently in a groove in the front of the
male. Male and female adult worms remain joined together for life. S. mansoni, the most
common cause of schistosomiasis worldwide, is 10-20 mm long. They live in small vein of
the human intestine (intestinal schistosomiasis); and in blood vessels of the bladder (urinary
schistosomiasis). Because of this they are called blood flukes (Nester et al., 2001).
2.1.2. Giardia lamblia
Giardia lamblia (also known as Giardia duodenalis or G. intestinalis) is a unicellular,
flagellated intestinal protozoan parasite of humans isolated worldwide. It has two
morphological forms, cyst and trophozoite.
The cysts of Giardia lamblia are elliptically shaped, non-motile, range in size 8-14 μm by 710 μm, and contains two to four nuclei (Heresi and Cleary, 1997). They are encased by a
smooth and colorless, thick and refractile wall. The cysts are hardy, and very resistant to
environmental factors and standard concentrations of chlorine used in water treatment. They
can persist in feces for weeks or in cold water for months. The cysts are the infective form of
the parasite and each cyst gives rise two trophozoites (Ortega and Adam, 1997).
5
Trophozoites are motile and non-infectious because they cannot survive long outside the host
body. They are pear shaped with a broad anterior end and a narrow posterior end. They range
in size 12-15 microns by 6-8 microns. The organism has a pointed elongated median body
with two symmetric nuclei and four pairs of flagella. It resembles a human face on stained
preparations (Heresy and Cleary, 1997). The trophozoite is the reproducing forms that
attaches to the intestinal wall via its ventral disc and causes the symptoms of giardiasis.
Trophozoites are rarely infective because they are not resistant to gastric acid and die rapidly
outside the body (Ortega and Adam, 1997).
2.1.3. Life cycle of schistosomes and Giardia lamblia
The basic life-cycle of schistosomiasis is complex involving an alternation of generations
with the sexual reproduction of adult schistosomes in the definitive vertebrate host and an
asexual multiplication stage in a snail host (Webbe, 1981). The life cycle begins when pairing
adult worms within the blood vessels of the host mate and the female start to lay eggs.
Through the intestinal walls, the eggs get inside the gut and are passed out in the feces
(intestinal schistosomes) or through urine (S. haematobium). Once they reach water, the eggs
hatch and free-swimming miracidium larvae released. The purpose of miracidium larvae is to
find and penetrate an appropriate snail in which to develop. After a period of multiplicative
asexual reproduction, numerous large tailed free-swimming larvae called cercariae leave the
snail and swim in water where they actively seek an appropriate vertebrate host. When the
definitive host and the cercaria converge in water medium, cercaria can penetrate the intact
skin of the host and infect it. This process sometimes causes itching, but most people do not
notice it. The cercariae shed their bifurcated tails and transform their tegument into a form
adaptive to a mammalian environment and this is called schistosomula. Once in the blood,
they find their way into the blood circulation to heart, lungs, and eventually to the liver where
they grow and form male-female pairs, and then migrate to final destination: the mesenteric
veins in the wall of the intestines or bladder, thus repeating the cycle (Brooker, 2007).
6
Fig. 1. The life cycle of the three common human schistosomes
Source: CDC. http: /dpd. Cdc. gov/ dpdx
Giardia lamblia is a flagellated, binucleated microaerophilic Protozoa that inhabits the upper
part of the small intestine of its host and reproduces by binary fission. This parasite has a
simple direct life cycle consisting of an infective cyst and a vegetative trophozoite.
.
Giardiasis is then contracted via ingestion of cysts in contaminated water or foods. The cysts
pass through the stomach and enter the small intestine. The protective wall allows the cyst to
survive the acidic conditions of the stomach until the cyst reaches the small intestine, where
the conditions are alkaline. The alkaline environment triggers excystation. During excystation,
the cyst wall ruptures and trophozoites are released. The trophozoites multiply asexually by
binary fission in the small intestine, either as free floating bodies or attached to intestinal
epithelium via their ventral disc and causes the symptoms of giardiasis (Ortega andAdam,
1997). As trophozoites migrate toward the large intestine, they retreat into the cyst form in a
7
process called encystation. Cyst wall formation is completed and appears to be initiated by the
presence of bile salts in the lower small intestine. The cysts then leave the body in excrements
will quickly become infectious and will begin a new cycle of infection if ingested by a
susceptible host in contaminated food or water.
Fig.2. Life cycle of Giardia lamblia
Source; (CDC. http://www.dpd.cdc.gov/dpdx)
When trophozoites are excreted in feces, they cannot survive long in the environment and are
therefore non infectious; so, cyst formation is essential for the survival of Giardia outside the
host and for the transmission of the parasite among susceptible hosts (Adam, 1991). Although
8
infection after the ingestion of only one Giardia cyst is theoretically possible, the minimum
number of cysts shown to infect a human under experimental conditions is ten. Generally the
cyst stage of Giardia lamblia causes the infection while the trophozoite causes the symptoms
of giardiasis (Meyer and Jarrol, 1980).
2.2. Epidemiology and transmission of schistosomes and Giardia infections
2.2.1. Epidemiology of schistosomiasis and giardiasis
Schistosomiasis is achronic water-borne parasitic disease caused by blood flukes of the genus
Schistosoma. It ranks second to malaria in terms of posing a great public health and socio
economic threat in affected communities and individuals. Still now, it is a major helminth
infection in many developing countries of the tropics. The disease is endemic in 76 tropical
developing countries (Chitsulo et al., 2000). Infection occurs when People coming in contact
with water containing the infective larval stage called cercariae (Wu and Halim, 2000).
There are five species that cause schistosomiasis in humans, namely S. mansoni, the most
pathogenic located in tropical Africa, South West Asia, South America and Caribbean
Islands; S. haematobium found in Tropical Africa and South West Asia; S. japonicum,
previously found in Japan and now mainly in China and Philippines; S. intercalatum West
Africa; and S. mekongi around the Mekong river in Asia, mostly Laos and Cambodia (Jordan
1993). Among these, S. mansoni, S. japonicum and S. haematobium cause significant public
health problems (McManus and Loukas, 2008). S. mansoni, S. japonicum and S. intercalatum
cause intestinal schistosomiasis whereas S. haematobium is responsible for urinary
schistosomiasis. These worms deposit eggs in blood vessels surrounding the gut (intestinal
schistosomes) or bladder (S. haematobium) of the infected hosts. The five species also differ
in size and shape of their eggs.
Recent studies estimates that 779 million people are at risk of schistosomiasis and 207 million
people are infected worldwide (Steinmann et al., 2006). Among those infected, 120 million
are symptomatic and 20 million have severe clinical disease. Mortality was estimated at more
9
than 250, 000 deaths per year, making it the most deadly neglected tropical disease (NTD)
(van der Werf et al., 2003).
In Africa it is endemic in 46 countries (Boelee and Madsen, 2006) and majority (80-85%) of
schistosomiasis is found in sub-saharan Africa (Bergquist, 2002). S. haematobium, S.
intercalatum and S. mansoni are endemic. However, the two main causative species are S.
haematobium and S. mansoni. In Africa, approximately 393 million people are at risk of
infection for S. mansoni, of which 54 million are infected and for S. haematobium 436 million
are at risk, of which112 million are infected (van der Werf et al., 2003).
In Ethiopia, both S. mansoni and S. haematobium pose considerable public health and socioeconomic problem (Erko et al., 1997; Kloss et al, 1988). It is estimated that 29.89 million
people are at risk and of those 4 million are to be infected in the country (Chitsulo et al.,
2000). The distribution of schistosomiasis is highly focal and discontinuous (Erko et al.,
1997; Kloss et al., 1988). S. mansoni has been reported in wide places with an altitude range
between 650 and 2400 above sea level (Erko et al., 1997); most transmission sites of S.
mansoni infections are in agricultural communities along streams between 1300 and 2000 m
above sea level. It is transmitted by two freshwater biomphalarid species (B. pfeifferi and B.
sudanica). S. haematobium is restricted to some low and arid areas of Ethiopia, such as the
Awash valley and transmitted by two bulinid species (B. abyssinicus and B. africanus) (Erko
et al., 1997). New transmission foci are being discovered in different parts of the country. The
spread of the disease to new localities seem to be extensive population mobility due to
settlement and job opportunities; and water resource development (Erko, 1996).
Numerous local epidemiological studies have been conducted in different parts of Ethiopia.
The various epidemiological reports have also shown the occurrence of intestinal
schistosomiasis in various magnitudes. These included 45% in northeast (Gashaw, 2010), 7%
in northwest (Mengstu, 2010), 1% in eastern Ethiopia (Dawit, 2006). The disease is
particularly prevalent in the northern and northwestern administrative regions of the country
(Haile et al., 1994). A study was done on S. mansoni in Tigray in 1992 in six schools
accessible by roads. The overall prevalence ranged from 1% in Maychew to 61.8% in Adwa.
10
Among those whose stools were examined in Adwa town; prevalence (68%) was highest in
the 10 to 14 years age group followed by (64%) prevalence in the 15 to 19 years of age
respectively (Birrie et al., 1994). Another study also indicated in Adwa, the prevalence of
58.9% (Lemlem, 2008).
Giardia lamblia
Antonie van Leeuwenhoek was the first person to discover G. lamblia in 1600 but, he was not
provided illustration about the parasite. Further studies were made in 1859 by Vilem Lambl,
(Cox, 2002; Smith and Paget, 2007) and, he did not link the diarrheal disease with the Giardia
parasite, rather he assumed that the organism as part of the normal, harmless flora of the
intestines.
In 1915, Charles Wardell Stiles gave the parasite its current name, Giardia lamblia and also
suspected a link between Giardia and diarrhea for the first time. The pathogenicity of Giardia
was studied during the First World War, when a large number of soldiers developed diarrhea.
Giardia cysts were isolated from their feces and found to cause diarrheal symptoms in
laboratory animals . In 1926, Justin Achoo found that Giardia causes malabsorption in some
children but not in others. The causal link between Giardia and the disease was finally
established in 1954 by Dr. Robert Rendroff of the United States (Cox, 2002).
Today, Giardia lamblia has a worldewide distribution and is the most common protozoan
isolated from human stools. It is ranked among the top 10 parasites of man (Wolfe 1992;
Farthing, 1997). In addition to human, it also infect mammals, rodents, reptiles and birds
(Filice, 1952; Baker, 2007). Epidemiological studies suggest that the parasite is responsible
for about 5% of acute diarrhoea and 20% of chronic diarrhoeal illness in the world
(Thompson et al., 1993). The incidence of diarrhoea associated with Giardia is generally
higher in developing countries in Africa, Asia, South and Central America where access to
clean water and basic sanitation is lacking. The prevalence of the disease varies from 2-5% in
the developed and 20-30% in the developing countries (Farting, 1994). It is estimated that up
11
to 200 million people have symptoms of giardiasis with some 500,000 new cases per year
Worldwide, especially among children (WHO, 1998).
Although symptomatic infection causes a broad spectrum of clinical manifestations, Giardia
results in asymptomatic carrier state in a majority of cases. The asymptomatic infections are
most common in children and people with prior exposure to a source of infection (Ortega and
Adam, 1997). Both symptomatic and asymptomatic cases excrete infectious cysts with their
feces (Nester et al., 2001).
Giardiasis is greatly associated with poor sanitary conditions, insufficient water treatment and
day-care centers (Meyer and Jarrol, 1980; Wadood et al., 2005). Ethiopia has one of the
lowest qualities of drinking water supply and latrine coverage in the world. As a report from
2000 study shows Ethiopia had only 12% latrine coverage while Kenya had 87% (Kumie et
al., 2005). The disease is common causes of intestinal protozoal infection throughout the
country; and the prevalence range 3%-23% (Haile et al., 1994). According to Birrie and Erko
(1995) based on a countrywide survey of giardiasis, the overall prevalence among school
children and residents were 8.9% and 3.1%, respectively and that of the non- school children
were 4.4%. Endeshaw et al., (2004) reported a prevalence of 20.8% among diarrheal patients
referred to EHNRI. Dawit (2006) also reported a prevalence of 38% among children from
eastern Ethiopia (Dire-Dawa), Mengstu (2010) indicated a prevalence of 14% (south Gonder).
These reports have also shown that prevalence of the disease varies from place to place.
2.2.2. Transmission of schistosome and Giardia lamblia infections
The transmition of schistosome is associated with contamination of freshwater with human
feces containing schistosome eggs, in the presence of snail intermediate host species and
human contact activities (Okpala et al., 2004). People become infected when coming in
contact with water containing the infective larval stage called cercariae (Gurarie and Seto,
2009).
12
Giardia is transmitted by fecal-oral route. It is dependent upon the ingestion of cysts excreted
in the feces of infected persons or animals. The principal mode of transmission to humans
appears to be person-to person. Although indirect transmission from contaminated water and
food, originating from humans and animals has been described (Thompson, 1994).
2.3. Factors affecting the epidemiology of schistosomes and Giardia infections
2.3.1. Poverty and Sanitation
Both schistosomiasis and giardiasis are caused by intestinal parasites. They are considered as
diseases of the less developed society characterized by poverty, lacking basic services,
information and instruction. Particularly, the scarcity of latrines enhances transmission
probabilities through indiscriminate defecation habits. Under poor hygienic condition, faeces
and urine often enter water body occurring near human habitations and this enhances
transmission (Wadood et al., 2005).
2.3.2. Climatic factors and development of water resources
Rainfall and temperature are important determinants of the distribution of schistosomiasis.
Seasonal changes in those factors cause marked fluctuations in snail population densities and
transmission rates. Moderate rainfall could enhance transmission of schistosomiasis by
increasing the amount of surface water which can be suitable environment for breeding of
snail host. On the other hand dry season or too much raining gives negative result. Moderate
temperature enhances transmission rates. However, temperature below and above the
optimum level is not useful for the survival of larva and the snail. For instance, below 15 oc
larval development is inhibited while above 35oc, snail and parasite death occur (Anderson
and May, 1979).
As study indicates, the development of water resources and irrigation systems may create
more suitable conditions for the transmission of water borne parasites and breeding snails,
thereby causing an increase in the incidence rate of infection. Increased incidence and spread
of schistosomiasis has been observed following new irrigation scheme developments and dam
13
construction (Markell and Voge, 1971). In Ethiopia the establishment of the endemicity of S.
mansoni infection in areas previously non-endemic following introduction of water based and
water related activities has been reported from Methara, Wonji, and Finchaa Sugar plantation
areas (Kloos, 1993; Birrie et al., 1997).
Surface water may be contaminated by rain and wind that carrying Giardia cysts from fields
containing faeces of infected humans, livestock, or wild animals to nearby rivers and streams.
As a result it increases the spread of infection (Baker, 2007).
2.3.3. Age dependency
As compared with any other age group, school-aged children and preschool children tend to
harbor the greatest numbers of intestinal infections and as a result experience growth stunting
and diminished physical fitness as well as impaired memory and cognition (Crompton and
Nesheim, 2002). According to Scott et al., (2003) exposure to infection drop with rise in age.
In most schistosomiasis endemic areas, prevalence and intensity of infection are higher in
children than adults (Davis, 2003). It is predominant in school- age children between 10 and
15 years old [Barbosa 2006].
The difference in the peak age-related prevalence of disease is not only for schistosomiasis,
but also for other intestinal infections. It is probably due to the gradual development of
immunity and differences in the extent of exposure (Barbosa, 2006).
2.3.4. Behavioral and socio-economic factors
Behavioral activities and socio-economic status plays a great role on the transmission and
spread of intestinal parasites. In the case of schistosome parasite in endemic areas, exposure
to the polluted water by bathing, swimming, washing utensils and clothes, walking bare-foot
during irrigation in agricultural activities will be increase the spread. Moreover, the risk of
infection becomes greater when, water contact is during the middle of the day or early
14
afternoon, which is just the time that cercariae are released from the snail intermediate host
(Azim et al., 2008).
2.4. Morbidity and public health effects due to schistosomes and Giardia lamblia
infections
The neglected diseases often receive less attention. That is partly because not everyone
infected becomes ill. However the disability caused by their morbidity remains a serious
public health problem.
Schistosomiasis infection is often asymptomatic and that is why incidence is not known. In
acute infection, show symptoms like fever, cough, abdominal, joint and muscle pain, and
these symptoms subside. The disease is characterized by general enlarged liver, spleen and
lymph nodes; and blood, mucus and pus in stool (Ruberanziza et al., 2007). A generalized
illness occurs, probably due to circulating schistosomal antigens reacting with antibody.
Although some people die from the reaction (Nester et al., 2001). Host immune response to
eggs of schistosome parasites causes development of organ fibrosis and portal hypertension
(Engels et al., 2002). The lesions can lead to blockage of blood flow. Only about half of the
eggs are excreted and the rest are carried away by the blood stream and are finally trapped in
portal system of the liver. This cause hepato-splenomegaly. In a later stage these lesions may
result in periportal fibrosis of the liver (George & Mohb, 2000). Chronic malnutrition and
swelling of the abdomen result from liver damage (Nester et al., 2001).
Schistosome infection during childhood causes substantial growth retardation and anemia
(Olds et al., 1996) and also have cognitive impairment and memory deficits (Nokes et al.,
1999; Savioli et al., 2004) that have been shown to impair their school performance (Nokes et
al., 1999). The disease is linked with anemia perhaps due to blood and nutrient loss in either
the stool or urine (Hoffman et al., 1979).
As in any parasitic infections, host parasite interaction is the initial step in the pathogenesis of
giardiasis. When the disease occurs, it can result acute watery diarrhea, abdominal pain,
15
nausea, vomiting, fatigue, foul-smelling stools associated with flatulence and abdominal
distention (Ortega and Adam, 1997). Infection occurs by ingestion of cysts. Two trophozoites
are emerging from each cyst. The trophozoites are the reproducing and motile forms of
Giardia either attaches to the intestinal wall via their ventral disc (Ortega and Adam, 1997),
or moves freely in the intestinal mucus. Some may migrate up the bile duct to the gallbladder
and cause crampy pain. In severe cases, the trophozoites can become so numerous along the
intestine not only absorbs but also may entirely cover epithelial surface (Nester et al., 2001).
These inhibit the absorption of fats, carbohydrates, vitamin and folic acid (Ortega and Adam,
1997) and impair activity of mucosal enzymes. The result is malabsorption, deficiency of
disaccharidase and lactose intolorance (Partovi et al., 2007).
2.5. Diagnosis of schistosomes and Giardia lamblia infections
Different diagnostic methods that have been developed for determinations of intestinal
infection include clinical symptoms, microscopy, immunodiagnosis, ultrasonography,
parasitological diagnosis, Kato-Katz method and formol-ether concentration. All of these
have limitation either in terms of cost, rapidity, simplicity or applicability (WHO, 1991;
Ahmadi, 2007).
Direct saline wet mount provides economical and rapid diagnosis for intestinal parasites if
they are present in sufficient density in the stool samples (Ukaga et al., 2002). The formolether concentration procedure is efficient in recovering protozoan cyst, helminth eggs, larva,
schistosome eggs (Peters et al., 1980) and increases the sensitivity and specificity of stool
microscopy to allow the detection of low numbers of organisms, thereby facilitating
identification (Ahmadi et al., 2007). It also allows the concurrent diagnosis of intestinal
protozoa, and is sometimes used in combination with the Kato-Katz method to enhance
diagnostic sensitivity for helminths, and hence to deepen our understanding of polyparasitism
(Raso et al., 2004; Steinmann et al., 2010). Moreover, the concentration technique uses for
preservation of stool samples, fixed in either sodium acetate-acetic acid-formalin (SAF)
(Marti and Escher, 1990), or diluted formalin (Cringoli et al., 2010), thus allowing sample
storage and analysis at later time. However, considerable inter-laboratory discrepancies have
16
been noted for helminth and particularly intestinal protozoa diagnosis (Bogoch et al., 2006). It
reduse the risk of infection from bacteria and viruses because they may not be able to survive
the concentration process (Akujobi, 2005). Limitation of the method is that, it is expensive or
costly, labor intensive and time consume.
The Kato-Katz technique (Katz et al., 1972) is useful for the quantitative estimation of worm
burdens (Markell et al., 1999). It is especially useful for field surveys for helminth infections
since it provides estimates of the intensity of infection (Martin and Beaver, 1968). According
to Martin and Beaver (1968), the technique entails the examination of a standard sample
(determined by the size of the template) of fresh faeces pressed between a microscope slide
and a strip of cellophane that has been soaked in glycerin (Ukaga et al., 2002).
Schistosomiasis infection is detected by the presence of eggs excreted in stools for intestinal
strains (S. mansoni, S. japonicum) and in the urine for urinary strains (S. haematobium).
Recently the fecal thick smear or Kato-Katz method (Katz, 1972) is considered as a gold
standard for diagnosis of Schistosome eggs. This method is used to know the number of eggs
excreted and to determine the intensity of infection. Kato-Katz thick smears also have
limitation because collection of specimen is tedious especially in areas with low intensity of
infection as repeated examinations are needed to obtain reliable data (WHO, 1998).
Diagnosis of Giardia infections has been carried out using microscopic identification of cysts
or trophozoites in stool specimens. The sensitivity of Giardia detection increase by using
standard method includes Iodine-stained wet smears, cyst concentrates prepared by Formalin
ethyl acetate centrifugation (Broke, 1977).
Immunofluorescence (IF) and enzyme-linked immunosorbent assay (ELISA) assays have
been developed for detection of Giardia antigens in the stools. Both assays are based on the
use of Giardia-specific antibodies. They are much easier and require less experience than
microscopy. Moreover, it permits large numbers of stool samples to be tested rapidly and may
reduce technician’s time and bias among observers (Addiss et al., 1991).
17
2.6. Prevention and control of schistosome and Giardia lamblia infections
2.6.1. Prevention
It is well known that prevention is better than cure. Intestinal diseases arise due to lake of
hygiene especially improper defecation. Improved sanitation and proper disposal of fecal
materials are the most important measures for prevention and control of disease transmission
by reducing water contamination.
Prevention of schistosomiasis depends on avoiding skin exposure to fresh water contained
with the cercaria, proper disposal of faeces, preventing untreated human faeces from entering
fresh water (Nestel et al., 2001), by using Endod (Lemma et.al., 1975) and molluscicide, to
control the snail intermediate host.
Currently, there is no vaccine to protect humans from acquiring giardiasis, nor does
chlorinating municipal water to protect against Giardia. Thus, various public health and
prevention strategies should be taken to decrease risk of infection (Schrader, 2005). The
important strategies include effective water treatment options such as boiling, chemical
treatment (iodine tablets), and filtering water for drinking (Jack, 1988), proper hand washing
before handling food and after visiting toilet, maintaining good personal hygiene, and proper
disposal of fecal materials (Backer, 2000).
2.6.2. Treatment
The recommended drug to control schistosome infection is praziquantel (Kabatereine 2004).
Due to lack of resources, drug treatment can not cover every infected human host in the area.
To achieve the best result, one needs to identify the high-risk groups and concentrate on them.
School-age children constitute a high-risk population and as children, they typically have the
highest intensity of schistosomiasis infection of any age group. In general, children are easier
to cover with mass drug treatment because they are readily available to be reached through
18
schools which offer a sustained infrastructure with a skilled workforce that is in close contact
with the community. Child-treatment reduces disease transmission; hence infection levels in
community declin. By reducing transmission of schistosomiasis infections, deworming can
improve the health and school participation of children (Adams et al., 2004).
There are different groups of drugs available to treat giardiasis (Gardner and Hill, 2001). The
most commonly used anti Giardia drugs include metronidazole, Furazolidone and
Paromomycin. Metronidazole is the most common drug used for the treatment of giardiasis
worldwide. Unlike other drugs, it is quickly and completely absorbed and penetrates body
tissues and secretions such as saliva, breast milk, semen, and vaginal secretions (Gardner and
Hill, 2001). Of the common anti-Giardia therapeutics Furazolidone is the only one available
in a liquid suspension and is an important therapeutic agent worldwide and it has been widely
used in pediatric populations (Lerman and Walker, 1982). Paromomycin has been proposed as
a treatment for G.lamblia in resistant infections and during pregnancy (Kreutner et al., 1981).
2.6.3. Health education
Health education by encouraging healthy behaviors such as use of latrines and change in
defecation habits can play a key role in reducing the incidence of infection. It can decrease
costs, increase levels of knowledge, and decrease re-infection rates. Health education efforts
can build trust and engage communities, aspects that are crucial to the success of public health
initiatives (Lansdown et al., 2002).
19
3. MATERIALS AND METHODS
3.1. Study area
The study was conducted in Adwa town (Figure 3). It is found at the central zone of Tigray
region. Adwa is located in northern part of Ethiopia at a distance of 1006 km away from
Addis Ababa. Altitudinal ranges of the area extend from 1800-1900 meters above sea level.
The average annual rainfall ranges between 500mm and 600mm, the peak rainfall occur
during July to August every year. The temperature is relatively warmer and it ranges from
27°C to 28°C (Adwa district Meteorology Department, 2011). The area is traversed by
streams and rivers which constitute major source of S. mansoni infection and it is known as
endemic area for intestinal schistosomiasis. Adwa town covers a total area of 2294 sq.km
(Adwa municipal, 2008) and has a population of approximately 60,748 inhabitants of whom
27,454 are males and 33,294 are females (AFEDB, 2009).
.
F.g.3. Adwa town
Source: - Tigray Finance and Economic Development Bureau
20
3.2. Study design
The study was cross sectional survey to determine the prevalence and intensity of S. mansoni
and Giardia lamblia infections among the children in primary schools of Adwa town,
northern Ethiopia. Relation of the infections with physical growth and socio-demographic
factors of school children as well as major risk factors associated with the infections were also
identified. The study was conducted from February-April 2012.
3.3. Study population
Students from grade 1-8 found in the selected schools who volunteers to participate in the
study and attending classes at the time of sample collection were included in the present
study.
3. 4.Exclusion criteria
According to the information obtained from the parents and the children themselves, those
that have been treated for S. mansoni and diarrhoea infections before 3 months at the time of
survey were not included in the present study.
3.5. Sample size determination and sampling procedure
Sample size (n) was determined based on the previous prevalence report of S. mansoni (60%)
in Adwa as reported by Lemlem (2008). The minimum sample size required at analysis stage
was calculated using the 95% confidence level with 5% marginal error. The sample size was
estimated using the following statistical formula (Naing et al., 2007):
N=
Z2 P (1-P)
d2
Where, N = minimum sample size required
Z = 1.96 at 95% confidence level
21
d = margin of sampling error tolerated (5% marginal error was used)
P = an estimate previous prevalence of S. mansoni (60%)
Based on the above formula 369 sample size was obtained. Considering the criteria of
accessibility, and limitation of resources only six (6) primary schools were selected randomly
from twelve primary schools in the first step. The second step was selection of sections
(include grade 1-8) out of the selected schools with proportional allocation to size of the
population; and lastly, random sampling technique was employed to select study subjects by
using class rosters as the sample frame.
3.6. Methods of data collection
3.6.1. Questionnaire survey
A total of 369 structured questionnaires were distributed to gather information regarding age,
sex, source of water for drinking, private latrine, defecation practices, swimming practices etc.
It was prepared in English, and later translated into Tigrigna. Brief explanation was given to
the students how to fill it. For small grade children (grade 1-3), it was filled by their parents.
The entire questionnaire should completely be filled and returned before sample collection.
3.6.2. Stool sample collection and examination
A clear instruction was given to the selected pupils to bring sizable fresh stool sample of their
own (Booth et al., 2003). The school children were provided with small plastic sheets and
clean wooden applicator stick. The code, age, sex and school name of each student was
recorded for the samples collected and then labeled. A small amount of each fresh stool
specimen was processed by direct wet mount technique using normal saline (0.85% NaCl
solution) to examine the presence of egg, cyst and motile parasites under light microscope at
10x and 40x magnification within the schools. In addition, a portion of the specimen was
processed using 41.7 mg Kato-Katz template (WHO, 1991). Accordingly, the method
followed.
22
A portion of the fecal specimen was taken by clean plastic spatula and forced through the
nylon screen to separate fecal materials from the large debris. The screened fecal material was
transferred to the template which was laid flat centrally on a microscope slide. The template
hole was completely filled with screened faecal material. The spatula was passed over the
filled template to remove excess faeces from the edge of the hole. The template was removed
carefully and a cylinder of faeces was left on the slide. Then the fecal material was covered
with a cellophane square which was pre soaked in malachite green-glycerin solution. The
slide was inverted and the fecal sample was pressed firmly against the hydrophilic cellophane
strip to spread evenly. The slide was then placed on the bench with cellophane upwards to
enable the evaporation of water while glycerol cleared the faces. The slide was kept at room
temperature to clear the fecal material, prior to microscopic examination.
After clearing, the slides were examined systematically under the middle (10X) and high
power (40X) objectives of the microscope by the experienced laboratory technicians for the
detection of parasite ova particularly ova of S. mansoni in Adwa Hospital laboratory. The
number of eggs observed were recorded and later multiplied by 24 to obtain the number of
eggs per gram of faeces (EPG). If “n” number of eggs of parasite species are found in 41.7 mg
of stool specimen, then 1000 mg (i.e. 1 g) of the faecal specimen contains “n” X (1000/41.7)
or (“n” X 24) EPG. An egg count of 1-99, 100-399 and ≥400 EPG was considered as light,
moderate and heavy infection respectively, WHO, 1987.
3.6.3. Anthropometric measurements
Body weight and height was measured using the standardized procedures following Gibson
(2005); and body mass index (BMI) was calculated using the following formula:
BMI= weight in kg/ [height in m] 2). The school children were weighed without shoes and
wearing light cloth using weighing scale to the nearest 0.1 Kg. The height was measured to
the nearest 0.1 cm using a measuring tape. The age of each child was recorded during sample
collection.
23
Anthropometric indices or nutritional indicators, such as height-for-age (HAZ) or stunting,
weight-for-age (WAZ) or underweight and weight-for-height (WHZ) or wasting were
calculated and used as indicators of growth status of the children using anthropometry
software (Epi Info) in accordance with the recommendations of World Health Organizations
(WHO, 2007), on the basis of the reference data of National Center for Health and Statistics.
Under-nutrition was defined for a child, who had less than -2 Z-scores (-2SD) from the
National Center for Health Statistics (NCHS) median reference population values (WHO,
2007). This was used as cut-off point to determine malnourishment. Since wasting for those
children with age above 9 years cannot be evaluated through Epi Info, BMI-for-age value less
than 5th percentile of reference data was considered as thinness or underweight (WHO, 2006).
3.7. Data analysis
Statistical analysis was carried out using the SPSS Windows version 16. Anthropometry
indices were computed using the calculator mode of anthropometry calculating software
program (WHO, 2007). Wasting, stunting and underweight were defined as Z-score values of
less than -2SD (Standard Deviation), which was below what is expected on the basis of the
international growth reference scale (WHO, 2007). Descriptive statistics were applied to
indicate the prevalence of S. mansoni and G. lamblia infections, and nutritional status as
percentages and proportions. Association of risk factors with S. mansoni and G. lamblia was
made using chi-square test. Odds ratio (OR) was used to determine the association of S.
mansoni and G. lamblia with nutritional indicators. 95% CI level was used to show the
accuracy of data analysis. P-value<0.05 was considered statistically significant.
3.8. Data quality control (QC)
To ensure quality control, all the libratory procedures including collection and handling of
specimens were carried out in accordance with standard protocols (NCCLS, 1997; WHO,
1991). Reagents were checked by known positive and negative samples from the clinic before
stool sample preparation and examination.10% of the total slides were randomly be selected
and read by a second experienced laboratory technician. The weight scale was checked at the
24
beginning of each working day and calibrated to the zero before taking every measurement.
Beside to this, all the questionnaires were checked for accuracy and completeness by the
investigator.
3.9. Ethical considerations
Ethical clearance was obtained from the Ethical Committee of health science Mekelle
University. Permission to conduct the study was also obtained from Educational authorities
and school principals. Prior to stool collection, the objectives of the study and procedure of
sample collection was explained to school principals, teachers, students and other concerned
authorities. Sample collection was carried out using sterile and disposable materials. All
activities in clinical examination as well as stool sample collection and laboratory
parasitological examination were done by laboratory technician. Ethical consideration was
addressed to treat individuals with positive results for any intestinal parasites and the required
treatment and drugs administered by the site health officer.
25
4. RESULTS AND DISCUSSION
4.1 Prevalence of Schistosoma mansoni and Giardia lamblia infections in school children
4.1.1. Prevalence of S. mansoni infection in school children
A total of 369 school children were selected to participate and all of them were (100%)
provided proper stool samples. The prevalence of S. mansoni infection among the children
was 52.6% (194/369), of these 60% were males and 40.8% females (Table 1). This result was
comparable to previous study conducted in Adwa reported 58.7% prevalence of S. mansoni
infection (Lemlem, 2008) and 54.3% prevalence of the infection was reported from Adarkay
district by Jemaneh (1997). But lower prevalence of S. mansoni was obtained when compared
to data of Bushulo village, southern Ethiopia reported as 73.7% (Ashenafi et al., 2007).
The prevalence of S. mansoni infection in the present study was higher than the previous
reports in different parts of Ethiopia such as in Dire-Dawa, 1.0% (Dawit, 2006), in
Benishangul-Gumuz, 6.3% (Eyasu, 2007), in Babile, 4.3% (Girum, 2005), in Jimma, 26.3 %
(Mulugeta, 2008) and in Hayk, 45%, (Gashaw, 2010). These variable results could be due to
differences in sampling technique and study population. Moreover, at the local level, disease
endemicity is often the product of place-specific factors both in time and space, and hence
disease transmission foci are not the same (Stothard, 2009).
The prevalence of S. mansoni infection was found to be higher in boys (60%) than that of
girls (40.8%) (P = 0.014). This gender-associated difference has also been found in other
studies, such as Birrie (1986) from Borkena river basin, Tadesse et al. (2009) from Waja,
Lemlem (2008) from Adwa, Mulugeta (2008) from Jimma, Pontes et al, (2003) from Egypt.
On the contrary, a study conducted among students in primary schools near Lake Victoria of
Kenya showed that prevalence was slightly higher in females than male participants (Handzel
et al., 2003). The observed difference in the present study might be due to the fact that, males
stay most of the time outdoors and swimming in streams as compared to females. The
association of schistosomiasis and sex is well documented (Brooker, 2007).
26
The present study revealed peak prevalence among age group of 10-14 years followed by the
age group of 6-9 and 15-18 years (Table 1). The prevalence in this age group was 56.6 %,
38.5% and 33.3%, respectively. Children in the age group of 10-14 years was highly affected
as compared to other groups (P = 0.001). The result of the present study agreed with previous
epidemiological study conducted in Gonder by Mengstu (2010). On the other hand, other
investigators reported peak infection of S.mansoni in the age group of 10-14 years followed
by the age group of 15-19 and 5-9 years (Mulugeta, 2008) from Jimma. The higher infection
in the age group of 10-14 years observed here might be attributed to the high water contact
behavior of children this age group than the rest age groups. In addition to this, degree of
exposure to infection decreases with rise in age (Scot et al., 2003). It is probably due to the
gradual development of immunity and differences in the extent of exposure in adults (Abebe
et al., 2003; Montresor et al., 2002, Barbosa, 2006).
.
27
Table 1. Prevalence of S. mansoni by age and sex of examined children in Adwa schools during February-April, 2012
Age
Male
group
(in years) No.
No. positive
examined
(%)
Female
Both sex
No. examined
No.positive
(%)
No.
examined
No.positive
(%)
X2
p-value
6-9
51
23 (45.1)
27
7 (26)
78
30 (38.5)
2.742
0.098
10-14
174
112 (63.4)
114
51 (44.7)
288
163 (56.6)
10.805
0.001
15-18
2
1 (50)
1
-
3
1 (33.3)
0.750
0.386
All age
groups
227
136 (60)
142
58(40.8)
369
194 (52.6)
8.545
0.014
28
4.1.2. Prevalence of Giardia lamblia infection in school children
As showen in Table 2, the overall prevalence of giadiasis (23.6%) observed in the current
study area was much higher than the overall prevalence of the same disease in south Gonder
(7.8%) reported by Amha (2007), in south Wollo (9.4%) by Fentaw (2010), in south Gonder
(14.0%) reported by Mengstu (2010), in north Shewa (13.8%) reported by Teklu (2009). It
was comparable to the findings of Eyasu (2007) with prevalence of 26.6% from BenishangulGumuz. On contrary, it was far lower than the prevalence of giardiasis reported from DireDawa, by Dawit (2008) as 38.0% and from India, with prevalence of 53.8% reported by
Gagandeep (1998). The possible explanations for the discrepancy between the present and
previous study finding might be the result of variation in sampling techniques used, the
difference in the quality of drinking water source, and personal as well as environmental
sanitation.
In this study, the prevalence of giardiasis was found to be similar in males (22.9%) and in
females (24.6%) (P=0.502). This was in agreement with a study in Philippines (Natividad et
al., 2008) and in Dire-Dawa (Dawit, 2006). On the other way, studies conducted in northern
Jordan (Nimri, 1994) and in Egypt (Mahmud et al., 1995) revealed that prevalence of
G.lamblia infection was higher in males than females. Eyasu (2007) from BenishangulGumuz was also recorded more prevalence of giardiasis in females than male students. The
possible reasons for the absence of sex-related difference in the present study might be due to
their similar exposure risk of giardiasis and the pattern of hygienic practices.
In the present study, prevalence of giardiasis in the age groups of 6-9, 10-14 and 15-18 years
old was 28.2%, 22.2% and 33.3%, respectively (Table 2). All age groups showed no marked
difference as it has been demonstrated in Pawi district (Eyasu, 2007). But slightly higher
proportion of G.lamblia infected individuals were observed in age group of 15-18 years old. It
is similar with the report from Ghana (Bernard and Samuel, 2011) recorded that high infection
being observed in 15-17 years old than other age groups. The current finding was opposite to
the report by CDC (2000) that the age-specific prevalence of giardiasis was greatest in
children aged 1-4 years followed by children aged 5-14 years in Los Angeles. This lack of
29
age-related difference in the present cases might be attributed to similar exposure risk of
Giardia infection among these age groups. It is also strengthened by the suggestion that
giardiasis was not clustered in a particular age group (Lindo et al., 1998). That indicates the
disease is not limited to some age groups so, it can infect individuals regardless of their age.
30
Table 2. Prevalence of G. lamblia infection by age and sex among school children in Adwa town, northern Ethiopia
from February-April, 2012
Age group
(in years)
Male
Female
Both sex
X2
p-value
No.
examined
No.
Positive (%)
No.
examined
No.
Positive (%)
No.
examined
No.
Positive (%)
6-9
51
13 (25.5)
27
9 (33.3)
78
22 (28.2)
0.536
0.464
10-14
174
38 (21.8)
114
26 (22.8)
288
64 (22.2)
0.037
0.847
15-18
2
1 (50)
1
-
3
1 (33.3)
0.750
0.386
All age
groups
227
52 (22.9)
142
35 (24.6)
369
87 (23.6)
1.379
0.502
31
4.2. Intensity of S. mansoni infection in school children
Intensity of S. mansoni infection was determined by calculating the number of eggs per gram
of faeces, using the 41.7 mg templates according to the modified kato-katz technique (Peters
et al., 1980). Categorization of intensity of S. mansoni infection was done as WHO (1987)
recommended. That means, an egg count of 1-99, 100-399 and ≥400 epg was considered as
light, moderate and heavy infection, respectively.
Table 3 showed the mean intensity of S. mansoni infection in the study subjects. Egg count
per gram of faeces ranged from 24 to 840, and the highest epg (840) was found in one male
student. Overall mean intensity of S. mansoni infection among children was 141.53 (152.28
for males and 116.31 for females). The result of the present study was comparable with the
study conducted in Jimma, by Mulugeta (2008) recorded that 108.18 epg for the same
parasite. In contrast to the present study, however, higher mean intensity of S. mansoni
infection (643.3 epg for males and 336.4 epg for females) was reported by Ashenafi et al.,
(2007).
The peak intensity of S. mansoni infection was observed in the age group of 15-18 years (840
epg) followed by 10-14 years which indicated 144.88 epg (157.27 epg for males and 117.69
epg for females) and in children of aged 6-9 years as 100 epg (98.09 for males and 106.29 for
females) (Table 3). This was in agreement with the study carried out in southeast of Ethiopia
(Ashenafi et al., 2007). On the other hand, a study conducted in Jimma (Mulugeta, 2008)
showed that the peak of intensity of S. mansoni infection was observed in the age group of 1014 followed by 15-19 years. As the present study indicated, the mean intensity of S. mansoni
infection among children in the age group of 6-9 was similar between males and females
(98.09 epg and 106.29 epg), respectively. On the other hand, slightly different mean intensity
of S. mansoni infection was observed among the age group of 10-14 years old .The mean epg
of faeces of the above parasite in this age group was 157.27 epg for males ,while 117.69 epg
for females. Similarly, overall higher proportion mean intensity of S. mansoni infection was
showed among males (152.28) than females (116.31) (Table 3).
32
Table 3. Mean ± SEM egg per gram of facese of S. mansoni identified in examined school
children in Adwa town during February-April, 2012
Age group
(in years ) )and sex
No. examined
Mean ± SEM
T- test
Range
Male
51
98.09 ± 16.931
17.5
24- 264
Female
27
106.29 ± 33.064
25.0
24 -288
Total
78
100.00 ±14.830
174
157.27 ± 14.016
48.2
24 -720
114
117.69 ± 14.749
14.1
24 - 480
288
144.88 ± 10.750
2
840
-
840
1
-
-
-
3
840
227
152.28 ± 13.058
41.7
24-840
142
116.31 ± 13.488
21.3
24 -480
6-9
24 -288
10 -14
Male
Female
24 -720
Total
15 -18
Male
Female
840
Total
All age group
Male
Female
369
Total
SEM: - Standard Error of mean
141.53 ± 10.054
24- 840
In this study, the overall prevalence and intensity of S. mansoni were not directly related.
Although the prevalence of infection was higher in the children (Table 2), data on egg count
revealed that low intensity of infection (Table 3). Analysis of the intensity of S. mansoni
infection showed that most of the pupils were found lightly and/or moderately infected with
33
rare heavy infection. It reflects the general pattern of schistosomiasis infection, the effects of
which are to be minimal or ill defined (Assis et al., 1998). It is also supported by the findings
of Palmer & Bundy (1995), they suggested the fact that, the infection is over dispersed, but
majority of the population will excrete very few eggs (light infection) while minority, excrete
large amounts of eggs (heavy infection). The current result was contrary to the idea of
Hoffman et al., (1979), who confirmed that prevalence and intensity are related and,
generally, populations with high prevalence of infection tend to have high intensity. The
justification for the variation of results among studies might be due to difference in sampling,
and frequency of exposure to infested water body.
4.3. Socio-demographic characteristics of the study children
Out of 369 participants, 227 (61.5%) were males and 142 (38.5%) were females. The age
distribution among them ranges from 6 to 18 years. Table 4 shows that 78 (21.2) of the study
participants were 6-9 years old, 288 (78.0%) were 10-14 years old and 3 (0.8%) were 15-18
years old.
Tap water supply was the major source (95.1%) of water for drinking. Only few, 18 (4.9%) of
the students obtained water for this purpose from stream. 287 (77.8%) of the children take
bath at home, while the remaining 82 (22.2%) of the total study subjects bath their body in
streams. 158 students (42.8%) wash their cloth in streams, while the other 211(57.2%) wash
their cloth at home. Among the selected students, 284 (77.0%) swam in streams, but the
remaining 85 (23.0%) did not. Majority of the study subjects (84.6%) had body contact with
the stream while crossing it. Only few, 57 (15.4%), avoid that activity (Table 4).
More than half of the students (63.7%) defecated in the open fields, and the remaining 134
(36.3%) practiced in latrine. 314 (85.1%) of the children had toilet in their house, while only
55 (14.9%) had no access to toilet. Out of the total students, 304 (82.4%) regularly practiced
hand washing after defecation, while 65 (17.6%) of them had no that habit (Table 4).
34
Table 4. Socio-demographic characteristics of the study participants in Adwa elementary
schools, northern Ethiopia from February-April, 2012
Socio-demographic
variables
Sex
Male
Female
Age groups
6-9
10-14
15-18
Number
Percent
227
142
61.5
38.5
78
288
3
21.2
78.0
0.8
351
18
95.1
4.9
287
82
77.8
22.2
158
211
42.8
57.2
284
85
77.0
23.0
312
57
84.6
15.4
235
134
63.7
36.3
314
55
85.1
14.9
304
65
82.4
17.6
Source of water for drinking
Tap
Stream
Bathing
Home
Stream
Washing cloth in stream
Yes
No
Swimming habit in stream
Yes
No
Contact of water during crossing
stream
Yes
No
Open defecation habit
Yes
No
Presence of latrine in home
Yes
No
Washing of hands after
defecation
Yes
No
35
4.4. Anthropometric measurements
Two different sets of indicators were used as recommended by WHO for the age group of 6-9
years and 10-18 years (teenage). Nutritional indicators help to provide different information
about growth and body composition of a child, which are used to assess nutritional status
(WHO, 1995).
4.4.1. Prevalence of stunting, underweight and wasting status among the study subject
aged 6-9 Years
According to the recommendation of WHO (2007), the anthropometric measurements of
children in the study area were compared with an international reference population defined
by the National Centre for Health Statistics (NCHS) and accepted by the Centers for Disease
Control and Prevention (CDC).
Taking age and sex into consideration, height and weight of the children were expressed in
terms of Z-scores relative to NCHS reference data recommended by WHO (2007). Thus, for
children 6-9 years age group, those below -2SD of the NCHS median reference for WHZ,
HAZ, and WAZ are defined as wasted (indicator of present undernutrition), stunted (indicator
of past or long term undernutrition) and underweight (indicator of both present and past
malnutrition), respectively (CSO, 2005).
As shown in Table 5, the prevalence of wasting, underweight and stunting in the age group of
6-9 years was 12.8% (10/78), 32.1% (25/78) and 25.6% (20/78), respectively of whom, 11.8%
were males and 14.8% were females for wasting; 33.3% were males and 29.6% were females
for underweight; and 27.5% were males and 22.2% were females for stunting. The prevalence
of underweight and stunted was found to be higher among boys than girl participants, while
wasting was higher in girls than boys in this age group. However, the observed differences in
the present study were not statistically significant (P>0.05). Another study that could support
the current finding was conducted in northwest Ethiopia by Tilahun (2010) who reported that
36
the prevalence of underweight in boys and girls was 24.1% and 17.3%, respectively.
Similarly, the same author also reported the prevalence of stunted as 14.8% and 3.8% in
males and females, respectively; and prevalence of wasted as 14.8% and 19.2% in males and
females, respectively (Tilahun, (2010). On the contrary, a study conducted in Arsi revealed
that prevalence of underweight and wasted was higher in females than male study subjects;
and the prevalence of wasting showed statistically significant difference between male and
females (P=0.005) (Fayo, 2010).
As indicated in Table 5, the prevalence of underweight and stunted observed in the present
study (32.1% and 25.6%), respectively was higher than the prevalence of the same nutritional
indices in Arsi school children (17.6%, 19.8%) reported by Fayo (2010), in Achefer, north
west Ethiopia (20.8%, 9.4%) by Tilahun (2010) and in Babile town, eastern Ethiopia (5.2%,
5.4%) by Girum (2005), respectively. On the other hand, the prevalence of wasting in the
study area was in agreement with the previously reported in Arsi, in which 11.0% school
children were wasted (Fayo, 2010). Similar results also reported from Babile, by Girum
(2005) as 11.6% of school children were wasted, but lower than the previous study conducted
in Achefer reveald that 17.9% of school children were wasted (Tilahun, 2010).
Table 5. Prevalence of stunting, underweight and wasting status by sex among the study
children aged 6-9 years in Adwa elementary schools during February-April, 2012
Sex
Total examined
No. (%)
Male
51 (22.5)
Nutritional indicators
Weight- for-height
Weight-for-age
WHZ (%)
WAZ (%)
( wasting)
(underweight)
6 (11.8)
17 (33.3)
Female
27 (19.0)
4 (14.8)
8 (29.6)
6 (22.2)
Total
78 (21.1)
10 (12.8)
25 (32.1)
20 (25.6)
Height-for-age
HAZ (%)
(stunting)
14(27.5)
X2
_
0.782
0.744
0.060
P –value
_
0.676
0.689
0.971
37
4.4.2. Prevalence of underweight and/or thinness in the age group of 10-18 years by
gender
Weight-for-age is not particularly sensitive nutritional indicator in teenage and adolescence,
when there is a marked increase in growth velocity (Pollitt, 1990). For children 10-18 years,
BMI-for-age were calculated, and
value less than 5th percentile of reference data was
considered as thinness or underweight (Flegal et al., 2002; WHO, 1995).
Based on this, in the current study, the prevalence of BMI-for-age under 5th percentiles
(underweight) in the age group of 10-18 years was 38.8% (113/291), of which 40.9% were
males and 35.7% were females. Moreover, BMI-for-age percentiles of 5th-85th, and >85th were
also calculated for analyzing the status of normal growth and to assess risks for overweight
and/or obesity, respectively. As a result the prevalence of normal weight and risks for
overweight among the school children were 59.8% and 1.4%, respectively (Table 6).
The prevalence of underweight in the present study (38.8%) was higher than the prevalence of
underweight (5.1%) reported from south Gonder (Amha, 2007). On the other way, it was
lower than the result that had been conducted in Nigerian primary school (47%) reported by
Abidoye (2000). Similarly, the prevalence of risk-for-over weight observed (0.6% male and
2.6% females) in this study was found to be lower than previous studies carried out in school
children of Baltimore City (14.1% of boys and 15.3% of girls) (Megan, 2006) and in south
Gonder (9.9% male and 10.1% female) (Amaha, 2007). Variations in nutritional status among
the studies may be probably due to differences in adequate food and nutrient intakes as well
as recurrent infections (Shetty, 2006).
Generally, in the present study, the prevalence of underweight (32.1%) among age group of 59 years was lower than the report of the national figure, 35.7% (CSO, 2005). On the other
hand, wasted (12.8%) was found to be slightly higher than the data of national figure, 9.7%
(CSO, 2005). However, stunting (25.6%) was not a serious problem in comparison with the
Ethiopian Demographic and Health survey (EDHS) report, which showed as 51.3% (CSO,
2005). Overall, the prevalence of malnutrition from the anthropometric indices of the present
38
study subjects was not very critical compared to the national figures. But the rate is still high
and requires immediate intervention of concerned body. The higher rate of malnutrition
observed in the study area might be due to inadequate dietary intake that might be insufficient
to support growth, low awareness of the community towards nutrition, low socio-economic
status of the community, poor environmental and personal hygiene, or other factors.
Table 6. Prevalence of underweight and/or thinness in the age group of 10-18 years by gender
among school children in Adwa town, northern Ethiopia from February to April, 2012
176 (77.5 )
BMI-for-age
under 5th
percentiles
72 (40.9%)
BMI-for-age 5th
– 85th
percentiles
103 (58.5%)
BMI-for-age
above 85th
percentiles
1(0.6)
Female
115 (81)
41 (35.7%)
71 (61.7%)
3(2.6)
Total
291 (78.9)
113 (38.8%)
174 (59.8%)
4(1.4)
Sex
Total examined
(%)
Male
BMI= Body Mass Index
4.5. Association of intestinal schistosomiasis and giardiasis with anthropometric
measurement and socio-demographic characteristics of school children
This study has also analyzed the association of S. mansoni and G. lamblia infections with
anthropometric scores of the study subjects. The prevalence of nutritional status and the above
two parasitic infections among the participants was shown in Table 7. With regard to age
group of 6-9 years, the total prevalence of wasting was 12.8%, of whom 50%, 50% were
positive and negative for S. mansoni; 40%, 60% were positive and negative for G. lamblia
infection, respectively. The prevalence of underweight was 30.1%, of these 56%, 32.8% were
encountered with schistosomiasis and gardiasis, but 44%, 68% were free of them,
respectively. Besides, there were 25.5% stunting. Of which 45%, 20% were infected by S.
mansoni and G. lamlia parasites, while the other 55%, 80% stunted children were not infected
by the two parasites, respectively. With respect to age group of 10-18 years, the total
prevalence of underweight/thinness was 38.8%, of whom 77% and 39.8% were infected by
39
schistosomiasis and gardiasis while 23% and 60.2% were not encountered with them,
respectively.
Anthropometric scores were found to be independent of the overall prevalence of S. mansoni
and G. lamblia infections. These parasitic infections were observed among children with or
without stunting, wasting and underweight. At the same time, malnutrition was also observed
in children with or without the parasites (Table 7). In the present study, significant association
was not observed between the two parasitic infections and nutritional status (p>0.05). The
occurrence of wasting, underweight and stunting was not due to these parasites under
investigation. Similar results have also been reported from the study conducted in Aynalem
village, north Ethiopia (Asfaw and Goitom, 2000), in Achefer, northwest Ethiopia (Tilahun,
2010) and in Babile, eastern Ethiopia (Girum, 2005). All these previous studies revealed that
an independence of anthropometric scores on the prevalence of intestinal infections. On
contrary, other studies have shown improvement in the growth of children after the treatment
of helminths. This revealed that malnutrition is related with parasitic infections. A study in
Mexican (Quihui-Cota et al., 2004), Thailand (Egger, 1990), and Brazil (Tsuyuoka et al.,
1999) demonstrated the associations between intestinal parasitic infections and nutritional
indicators among school children. The difference between the studies could suggest that other
factors like variation in socio-economic status, dietary intake, knowledge of nutritional
matters (CSO, 2005), parasite species and burden (Chan et al., 1994; Oberhelman et al., 1998)
and host immune response (Eckmann and Gillin, 2001) may affect the nutritional status.
40
Table 7. Relationship between schistosomiasis and giardiasis with nutritional indicators among the participant children aged 6-9
and 10-18 years in Adwa town, northern Ethiopia during February to April, 2012
Nutritional
indicators
Age group
6-9
Wasting
(WHA)
Yes
No
Underweight
(WAZ)
Yes
No
Stunting
(HAZ)
Yes
No
Age group
10-18
Underweight
(thinness)
Yes(<5th)
No(≥5th)
OR= Odds ratio
OR
(95%,CI)
X2
OR
(95%,CI)
X2
P-value
4 (40.0)
18 (26.5)
1.090
(0.41-1.25)
1.440
0.487
0.088
8 (32.0)
14 (26.4)
1.540
(0.30-1.77)
2.074
0.355
0.155
4 (20.0)
18 (31.0)
1.251
(0.88-1.46)
0.281
0.869
1.581
(0.39-1.80)
1.573
0.455
Number
examined
(%)
S. mansoni
positive
(%)
P-value
78 (21.1)
30 (38.5)
10 (12.8)
68 (87.2)
5 (50.0))
25 (36.8)
1.080
(0.24-1.18)
2.728
0.256
25 (30.1)
53 (69.9)
14 (56.0)
16 (30.2)
1.481
(0.09-1.63)
4.869
20 (25.6)
58 (74.4)
9 (45.0)
21 (35.6)
1.360
(0.16-1.50)
3.735
291(78.9)
164 (56.4)
113 (38.8)
178 (61.2)
87 (77.0)
77 (43.3)
G. lamblia
positive
(%)
22 (28.2)
65 (22.3)
1.481
(0.12-1.63)
4.304
41
0.116
45 (39.8)
20 (11.2)
4.6. Associated risk factors with S. mansoni and G. lamblia infections in school children
The result of statistical analysis on the detection of risk factors for the infection by S. mansoni
and G. lamblia also add a better understanding about the spread of these parasites. Because
some of the risk factors linked significantly with one of the parasites, but not the others. As
data from laboratory result revealed, male students and children in the age group of 10-14
years were highly associated with schistosomiasis (Table 1), but no such type of difference
was observed for G. lamblia infection among the participants (Table 2). Analysis of the risk
factors for these parasitic diseases also proved similar results (Table 8). The reason for these
similar findings could be due to their mode of transmission and exposure of the study subjects
toward the risk of these parasites.
Regarding to S. mansoni infection among the potential risk factors, age groups, sex and water
contact habits was associated with high risk of S. mansoni infection. On the other hand, risk
factors such as source of water for drinking, open defecation habit, presence of latrine at
home, and washing of hands after defecation was not significantly associated (Table 8).
Statistical significant association was observed between prevalence of S. mansoni and age
groups. The prevalence of infection among age group of 10-14 years was found to be higher
than that of the rest age groups (P=0.014) (Table 8). This result showed that age difference
serve as a major risk factor for the infection of S. mansoni. This age related association has
also been observed in other studies ( Mulugeta, 2008, Mengstu, 2010).
As the result indicated (Table 8), sex was considered as a major risk factor for the infection of
S. mansoni. The proportion of infected males with S. mansoni was higher than the proportion
of infected females in the present study (Table 8); and the association was statistically
significant (P=0.000) (Table 8). The finding of the current study on the association of S.
mansoni and sex was well documented in the previous studies (Tadesse et al., 2009; Lemlem,
2008; Mulugeta, 2008; Pontes et al., 2003; Handzel et al., 2003) who cleared that
schistosomiasis was more common among males than females. This might be due to the fact
that, males stay most of the time outdoors and swimming in steams as compared to females.
42
Further analysis which was made on water contact habits of the study subjects confirmed that,
washing cloth and swimming habit in stream as well as contact of water during crossing the
stream was significantly associated with high risk of S. mansoni infection (P<0.05) (Table 8).
This result was in accordance with the findings of the study conducted in Jimma (Mulugeta,
2008), in Kenya (Handzel et al, 2003), in Malawi (Bowie et al., 2004) and in Adwa (Lemlem,
2008). In addition, Kloos and David, (2002) and Gurarie and Seto, (2009) also stated that,
overall, schistosomiasis transmission depends on the active role of the human and direct
contact with infected water containing cercariae. This revealed exposure to polluted water by
washing utensils and clothes, bathing, swimming, and other contact activities increase the risk
of S. mansoni infection.
The result of statistical analysis which was made on source of water for drinking against G.
lamblia infection showed significant difference between water source types and this parasite
infection (Table 8). Giardiasis was higher among individuals (55.6%) who used stream water
for drinking than individuals (21.9%) who used tap water for similar purpose (P=0.001). This
finding showed that use of stream water for drinking was the major risk factor for G. lamblia
infection in the study area. The reason could be due to the fact that stream water might be
contaminated by faeces containing cyst of that parasite. Observation from the sociodemographic characteristics of the study children also revealed that, although latrines may
have been constructed, majority of the students were not utilized. This action may be increase
contamination of streams by rain and wind that carrying faeces from fields containing Giardia
cysts (Baker, 2007). The present result is in agreement with similar studies conducted on the
prevalence and risk factors of intestinal parasites among children in Benishangul-Gumuz and
in south Wollo (Eyasu, 2007; Fentaw,2010), respectively. Investigation in British Columbia
also showed that giardiasis was more frequent in drinking water using surface supplies (IsaacRenton et al., 1999).
On the other hand, as revealed in Table 8, risk factors including age groups, sex, bathing,
washing cloth in stream, swimming habit in stream, contact of water during crossing the
stream, open defecation habit, presence of latrine at home, and washing of hands after
defecation were not statistically associated (P>0.05). The reason for the absence of
43
association between these risk factors and G. lamblia infection in the current study might be
due to the fact that giargiasis is caused by ingestion of G. lamblia cyst. It is strengthened by
Thompson, (1994) who stated that acquiring of giargiasis is dependent upon the ingestion of
cysts (excreted in the faeces of infected persons or animals) from contaminated water and/ or
food. It implies that without the concern of age, sex and other factors, any person who ingests
Giardia cyst with polluted water and/ or food might have a chance of infection by that
parasite.
44
Table 8. Major risk factors related with S.mansoni and G.lamblia infections in school children, Adwa town from February-April,
2012
Risk factors
Age
Alt.
6-9
10-14
15-18
Sex
Male
Female
Source of water
Tap
for drinking
Stream
Bathing
Home
stream
Washing cloth in
Yes
stream
No
Swimming habit
Yes
in stream
No
Contact water during Yes
crossing stream
No
Open defecation
Yes
habit
No
Presence of latrine
Yes
at home
No
Washing hands
Yes
after defecation
No
Alt. =Alternatives
Freq.
78
288
3
227
142
351
18
287
82
158
211
284
85
312
57
235
134
314
55
304
65
S.mansoni
Positive
Negative
(%)
(%)
30(38.5)
48(61.5)
163(56.6)
125(43.4)
1(33.3)
2(66.7)
136(59.9)
91(40.1)
58(40.8)
84(59.2)
188(53.6)
163(46.4)
6(37.5)
12(62.5)
140(48.8
147(51.2)
54(65.9)
28(34.1)
94(59.5)
64(40.5)
100(47.4)
111(52.6)
161(56.7)
123(43.3)
33(38.8)
52(61.2)
176(56.4)
136(43.6)
18(31.6)
39(68.4)
125(53.2)
110(46.8)
69(51.5)
65(48.5)
164(52.2)
150(47.8)
30(54.5)
25(45.5)
165(54.3)
139(45.7)
29(44.6)
36(55.4)
Freq. =Frequency
45
X2
P-value
8.545
0.014
12.737 0.000
2.810
0.094
7.456
0.006
5.305
0.021
8.375
0.004
11.918 0.001
0.099
0.753
0.101
0.751
2.005
0.157
G.lamblia
Positive
Negative
(%)
(%)
22(28.2) 56(71.8)
64(22.2) 224(77.8)
1(33.3)
2(66.7)
52(22.9) 175(77.1)
35(24.6) 107(75.4)
77(21.9) 274(78.1)
10(55.6) 8(44.4)
64(22.3) 223(77.7)
23(28.0) 59(72.0)
35(22.2) 123(77.8)
52(24.6) 159(75.4)
62(21.8) 222(78.2)
25(29.4) 60(70.6)
76(24.4) 236(75.6)
11(19.3) 46(80.7)
55(23.4) 180(76.6)
32(23.9) 102(76.1)
74(23.6) 240(76.4)
13(23.6) 42(76.4)
75(24.7) 229(75.3)
12(18.5) 53(81.5)
X2
P-value
1.379
0.502
0.147
0.702
10.740
0.001
1.170
0.279
0.312
0.577
2.087
0.149
0.685
0.408
0.011
0.917
0.000
0.991
1.146
0.284
5. SUMMARY, CONCLUSION AND RECOMMENDATIONS
5.1. Summary
The objective of the present study was to determine the prevalence, intensity and associated
risk factors of S. mansoni and Giardia lamblia infections and their association with
anthropometric measurements of school children, in Adwa town, northern Ethiopia. The study
was a cross-sectional parasitological survey involving a sample population of 369 school
children from grade 1-8 aged 6-18 years old. It was carried out during February- April, 2012
in the study area.
A total of 369 stool samples were collected and examined using Kato-Katz and direct wet
mount techniques. After screening the stool specimens, the overall prevalence of
schistosomiasis and giardiasis was 52.6% (194/369) and 23.6% (87/369), respectively.
Among the cases, the higher prevalence of S. mansoni was observed in males and in the age
group of 10-14 years, but no such type of difference was observed for giardiasis among
gender and age groups.
This study has also analyzed the intensity of S. mansoni infection of the study subjects. It
showed the overall mean egg count of 141.53 (ranged from 24-840) and the peak of intensity
in the age groups of 15-18 (840 EPG). In addition to this, anthropometric indices of the
participants were also measured and analyzed the relationship with the two parasitic
infections. However, this study did not find any association between the two parasitic
infections and malnutrition. The observed problems could be due to other factors such as
shortage of appropriate diet.
Besides, the current study was indicated significant association between S. mansoni infection
and age groups, sex, bathing, washing cloth in stream, swimming habit in stream, and contact
of water during crossing the stream. At the same time, source of water for drinking, revealed
significant relation with G. lamblia infection.
46
5.2. Conclusion
S. mansoni and G.lamblia were the major intestinal parasites diagnosed in the school children
of Adwa town. S. mansoni was found as dominant parasite in the students. Overall mean
intensity of S. mansoni infection among children was 141.53, and it does not directly related
with the prevalence of that infection. The result of the present study also showed high
prevalence of malnutrition among the participants. Factors such as age, sex and direct body
contact to stream water were associated with high risk of S. mansoni infection, while source
of water for drinking was the risk factor which contributes to the high prevalence of
giardiasis. Although significant difference was not observed between the above two parasites
and malnutrition in the present study, this does not mean that they do not have a role in the
effect of under nutrition. Since they are parasites, it is must to share the important nutrients of
the host. Moreover, as malnutrition is a multifactorial problem, hence, detailed studies are
required to investigate the association of S. mansoni and G. lamblia infection with
malnutrition.
47
5.3. Recommendations
The higher prevalence of S. mansoni, G.lamblia and malnutrition in school children calls for
immediate measures such as prevention, treatment, control of parasitic infections and
improvement of diet. So, we suggested that health workers need to give serious consideration
and mobilize the community to improve health situations.
 Adequate and safe water supply should be provided by the concerned body.
 Health education on personal and environmental hygiene, specially, the use of latrine and
change in defecation habit has to be delivered.
 Mass drug treatment focusing on school children must be encouraged. Because, childtreatment reduces disease transmission; hence, infection levels in community declines.
 Awareness should be created on the negative impacts of intestinal parasitic infestation on
health and about balanced diet and its advantage.
 Further studies should be conducted, preferably involving pre and post test treatment analysis,
for positive cases in order to estimate the relative contribution of intestinal parasites to
malnutrition in the area.
48
6. REFERENCES
Abebe, F., K.I. Birkeland, P.I. Gaarder, B. Petros and S.G. Gundersen, 2003. The
Relationship between dehydroepiandrosterone sulphate (DHEAS), the intensity of
Schistosoma mansoni infection and Parasite specific antibody responces.APMIS.111:319-328.
Abebe, F., Tedla, S., Birrie, H. and Medhin, G., 1995. Transmission dynamics of Schistosoma
mansoni in an irrigation setting in Ethiopia. Ethiopian Journal of Health Development.
9(3):147 - 156.
Abidoye, R.O and D.I. Eze, 2000. Comparative school performance through better health and
nutrition in Nsukka, Enugu, Nigeria. Nutrition Research. 20(5): 609.
Adams, R.D., 1991. The biology of Giardia spp. Microbiol. Rev. 55:706- 732.
Adams, V. J., C. J. Lombard, M. A. Dhansay, M. B. Markus and J. E. Fincham, 2004.
“Efficacy of Albendazole against the Whipworm Trichuris Trichiura—A Randomized,
Controlled Trial.” South African Medical Journal. 94: 972–76.
Addiss, D.G., H.M. Mathews and J.M. Stewart 1991. Evaluation of commercially available
enzyme-linked immunosorbent assay for Giardia lamblia antigen in stool. J. Clin. Microbiol.
29(6): 1137-1142.
Ahmadi, N.A., L. Gachkar, K. Pakdad and O. Ahmadi , 2007. Potency of wet mount,
formalin-acetone and formalin-ether methods in detection of intestinal parasitic infections.
Iranian J. Infect Dis Trop Med. 12:43-47.
Akujobi, C.N., K.C. Iregbu and T.O. Odugbemi, 2005. Comparative evaluation of direct stool
smear and formol-ether concentration methods in the identification of Cryptosporidium
species. Nigerian Journal of Health and Biomedical Sciences. 4(1): 5-7
Amha, A., 2007. Effect of intestinal parasitic infection and nutritional status on academic
performance of school children in Arb-Gebeya Town, T/Gayint woreda,south Gondar,
Ethiopia. Pp.34-40.
Anderson, R.M and R.M. May, 1979. Prevalnce of schistosome infection within molluscan
populations:observed patterns and theoretical observations. Parasitol.79:63-94.
Asfaw, T.S., Goitom L., 2000. Malnutrition and enteric parasitoses among under-five children
in Aynalem village, Tigray. Ethiop J Health Dev.14:67-75.
Ashenafi, T., Techalew, S., Mulugeta, M., Asrat, H., Berhanu, E., 2007. Schistosomiasis
mansoni and soil-transmitted helminthiasis in Bushulo village, southern Ethiopia. Ethiop J
Health Dev. 25(1): 47-48.
49
Assis, O., L. Barreto, S. Prado, G. Reis, M. Parraga and E. Blanton, 1998. Schistosoma
mansoni infection and nutritional status in school children: a randomized, double-blind trial in
northeastern Brazil. Am. J. Clin. Nutr. 68:1247-53.
Azim, S., F. Dojki, S. Ahmad, and A. Beg, 2008. Role of human behavior and parasitic
diseases. Inf.Dis. J. Pak. 17: 129.
Backer, D. H., 2000. Giardiasis. An elusive cause of gastrointestinal distress. The Physician
and Sports med. 28(7).
Baker, J.R., 2007. Advances in Parasitology. Elsevier Science & Technology Books. p. 131.
Barbosa, CS., TC. Favre, TN. Wanderley, AC. Callou and OS. Pieri, 2006. Assessment of
Schistosomiasis, through school surveys, in the Forest Zone of Pernambuco, Brazil. Mem Inst
Oswaldo Cruz 101: (Suppl 1)55–62
Barnes, K.I., P.Chanda and G.Barnabas, 2009. Impact of the large-scale deployment of
artemether/lumefantrine on the malaria disease burden in Africa: case studies of South Africa,
Zambia and Ethiopia. Mala J. 8 (Suppl 1).
Bergquist, N.R., 2002. Schistosomiasis: from risk assessment to control. Trends in Parasitol.
18:309-314.
Bernard, N., and B. N. Samuel, 2011. Giardia lamblia: a major parasitic cause of childhood
diarrhoea in patients attending a district hospital in Ghana. Parasites and vectors. 4(1): 163
Birrie, H., 1986. Survey of Schistosoma mansoni in Borkena river basin, Ethiopia. Ethiop.
Med.J. 24:159-167.
Birrie ,H., Woldemichael. T., Redda, A. and Chane, T., 1994. The status of Schistosoma
mansoni and snail hosts in Tigray and Northern Wello regions, Northern Ethiopia. Ethiop
Med J. 32:245- 253.
Birrie, H. and Erko, B.,1995. Giardiasis in Ethiopia. Ethiop. J. Health Dev. 9(1): 77-80.
Birrie, H., Lo, C.T., Erko, B., Redda, A. and Gemeda, N., 1995. Further investigations on
fresh water snails of Ethiopia. Ethiop. J. Sci. 18: 195–206.
Birrie, H., Medhin, G., Erko, B., Beshah, G. and Gemechu, T., 1997. Intestinal helminth
infections among the current residents of the future Finchaa Sugar plantation area, Western
Ethiopia. Ethiop J. Health Dev. 11: 219-228.
Boelee, E. and H. Madsen, 2006. Irrigation and schistosomiasis in Africa: Ecological aspects.
IWMI, Colombo, SriLanka. Pp.177-184
50
Bogoch, II., G. Raso, E.K. N'Goran, H.P. Marti and J. Utzinger, 2006. Differences in
microscopic diagnosis of helminths and intestinal protozoa among diagnostic centres. Eur. J.
Clin Microbiol Infect Dis. 25: 344–347.
Booth , M., P. Vounatsou, E.K. N. Goran, M. Tanner and J.Utzinger, 2003. The influence of
of sampling effort and the performance of the kato- katz technique in diagnosing Schistosoma
mansoni and Hookworm co-infections in rural Coted’ivoire. Parasitology. 127: 525-531.
Bowie, C., B. Purcell, B. Shaba, P. Makaula, M. erez, 2004. A national survey of the
prevalence of schistosomiasis and soil transmitted helminths in Malawi. Biomedical Central
Infectious Diseases, 10(4): 2334 – 2349.
Broke, J. A., 1977. The clinical and laboratory diagnosis of Giardiasis. Crit. Rev. Clin. Lab.
Sci. 7:373-391.
Brooker, S., 2007. Spatial distribution of human schistosomiasis in Africa risk models
transmission dynamics and control. Trans. R.Soc. Trop.Med. Hyg.101:1-8.
Centers for Disease Control (CDC) and Prevention, 2000. Giardiasis Surveillance United
States,
1992-1997. MMWR. 49 (SS-7):1-13.
Center for Disease Control (CDC) and Prevention of Schistosomiasis disease;[cited 2009
December 11]; available from : http://www.dpd.cdc.gov/dpdx/html/schistosomiasis.htm
Central Statistic Office (CSO), 2005. Ethiopia Demographic and Health Survey (EDHS).
Preliminary report. Addis Ababa, Ethiopia, Pp.1-34.
Chacon-Cruz, E. and D.K. Mitchell, 2007. Intestinal protozoal diseases. http://www.
emedicine.com/ped/TOPIC1914.HTM
Chan, M.S., G.F. Medley, D. Jamison and D.A. Bundy, 1994. The evaluation of potential
global morbidity attributable to intestinal nematode infections. Parasitology. 109: 373
Chitsulo, L., D.Engels, A. Montresor and L.Savioli, 2000. The global status of
schistosomiasis and its control. Acta Tropica 77: 41-51.
Cox, F.E., 2002. "History of human parasitology". Clin. Microbiol. Rev. 15 (4): 595–612.
Cringoli, G., L. Rinaldi, M.P. Maurelli and J .Utzinger, 2010. FLOTAC: new multivalent
techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals
and humans. Nat. Protoc. 5: 503–515.
Crompton, D.W. and M.C. Nesheim, 2002. Nutritional impact of intestinal helminthiasis
during the human life cycle. Ann Rev of Nutrit. 22:35-59.
51
Davis, A., 2003. Schistosomiasis. In: Manson's Tropical Diseases. (Cook, G.C.and Zumla,
A.I. eds). Elsevier Science Limited, UK, London. pp.1431-1463
Dawit, A., 2006. Association of Cryptosporidium parvum, Giardia lamblia and Entamoeba
histolytica/dispar infection with drinking water sources among children in rural part of DireDawa, eastern Ethiopia. Pp.53-54.
Eckmann, L. and F.D. Gillin, 2001. Microbes and microbial toxins, paradigms for microbialmucosal interactions 1. Pathophysioiogical aspects of enteric infections with thelumendwelling protozoa pathogen Giardia liamblia. American Journal of Physiology and
Gastrointestinal Liver Physiology. 280: G I -G6.
Egger, R.J., 1990. Association between intestinal parasitosis and nutritional status in 3-8 years
old children in Northeast Thailand. Pp.22-29.
Endeshaw, T., Mohamod. H.M. and Tilahun.W., 2004. Cryptosporidium parvum and other
intestinal parasites Among Diarrhoeal Patients Referred to EHNRI in Ethiopia. Ethiop Med J.
42: 195-198.
Engels, D., L. Chitsulo, A.Montresor and L.Savioli, May 2002. The global epidemiological
situation of schistosomiasis and new approaches to control and research. Acta Tropica, Vol.
82 Issue 2
Erko, B., Gemetchu, T., Medhin, G. and Birrie, H., 1997. Re-infection of school children with
Schistosoma mansoni in Finchaa valley, Western Ethiopia. Ethiop J Health Dev. 11(3): 266273.
Erko, B., Gemetchu, T., Gemeda, N. and Dessie, S., 1996. Transmission of intestinal
schistosomiasis in Addis Ababa, Ethiopia. E. Afr. Med.J. 73:732-734.
Eyasu, T., 2007. Drinking water source and the prevalence of Giardia lamblia
andCcryptosporidium parvum among children in selected villages of Pawi special district,
Benishangul-Gumuz region. Pp.36-38.
Farting, M.J.G., 1994. Giardiasis as a disease. In: Thompson, R.C.A.; Reynoldson, J.A. &
Lymbery, A.J. ed. Giardia: from molecules to diseases. Oxon, CAB International. pp. 15-37.
Farthing, M., 1997. The molecular pathogenesis of giardiasis. J. Pediatr. Gastroenterol. Nutr.
24: 79-88.
Fayo, W., 2010. Assessment of the association of Soil-Transmitted Helminthiasis and
Nutritional status with Anemia among school children, the case of Arsi Dodota, Oromia
regional state, Ethiopia. Pp.34-36.
52
Fentaw, B., 2010. Assessment of Malaria and intestinal parasites as public health problems
based on clinical record, parasitological surveys and kap in Borena district, south wollo,
central-north Ethiopia. Pp.30-36.
Filice, F.P., 1952. Studies on the cytology and life history of a Giardia from the laboratory
rat. University of California Publications on Zoology. 57:53-146.
Flanagan, P.A., 1992. Giardia - diagnosis, clinical course and epidemiology. A review.
Epidemiol. Infect. 102:1 - 22.
Flegal, K.M., R.Wei and C.Ogden, 2002. Weight-for-stature compared with body mass index
for- age growth charts for the United States from the Centers for Disease Control and
prevention. Am J Clin Nutr. 75(4):761-766.
Gagandeep, K., M. S. Mathew, D. Prasanna Rajan, J. D. Daniel, M. M. Mathan, V. I. Mathan
and J. P. Muliyil, 1998. Prevalence of intestinal parasites in rural Southern Indians. Tropical
Medicine and International Health. 3(1) 70–75.
Gardner, T. B. and D. R. Hill, 2001. Treatment of giardiasis. Clin. Microbiol. Reviews. 14(1):
114 -128.
Gashaw, A., 2010. Epidemiology of intestinal schistosomiassis in Hayk town, northeast
Ethiopia. Pp.28-29.
George, Y.W.U., and H.Mohb, 2000. Schistosomiasis progress and problems. WJG. 6: 12-19.
Gibson, R.S., 2005. Principle of nutrition assessment. Second editioned. Oxford: Oxford
University Press.
Girum Tadesse, 2005. The prevalence of intestinal helminthic infections and associated risk
factors among school children in Babile town, eastern Ethiopia. Ethiop.J.Health Dev.
19(2):140-145.
Gurarie, D. and Y.W. Seto, 2009. Connectivity sustains disease transmission in environments
with low potential for endemicity: modeling schistosomiasis with hydrologic and social
connectivities. J. R. Soc. Interface, 6:495-508.
Hadju, V., L.S. Stephenson, K. Abadi, H.0. Mohammed, D.D. Bowman and R.S. Parker,
1996. Improvements in appetite and growth in helminth-infected school boys three and seven
weeks after a single dose of pyrantel pamoate. Parasitologv. 113: 497-504.
Haile, G., Jirra, C. and Mola, T., 1994. Intestinal parasitism among Jiren elementary and
junior secondary school students, southwest Ethiopia. Ethiop J Health Dev. 8:37-41.
53
Handzel, T., DM. Karanaja and DG. Addiss, 2003. Geographic distribution of schistosomiasis
and soil transmitted helminthes in western Kenya: implication for anti helmenthic mass
treatement. American Journal of Tropical Medicine and Hygiene, 69(3): 318 – 323.
Heresi, G. and T. G. Cleary, 1997. Giardia. Ped. in Rev. 18 (7): 243-247
Hoffman, D., K.S. Warren, G. Webbe, V. Scott. And J.S. Lehman, 1979. Report of a
workshop on schistosomiasis control. Am.J.Trop.Med.Hyg. 28:249-59.
Hotez, P.J., D.H. Molyneux and A. Fenwick, 2007. Control of neglected tropical diseases. N
Engl J Med. 357: 1018–27
Isaac-Renton, J., J. Blatherwick, R.W. Bowie, M. Fyfe, M. Khan and A. Li, 1999. Epidemic
and endemic seroprevalence of antibodies to Cryptosporidium and Giardia in residents of
three communities with different drinking water supplies. Am. J. Trop. Med. Hyg. 60(4): 578583
Jack W., 1988. "Don't Drink the Water!". Field and Stream: 65–66.Retrieved 08/07/2012
http://books.google.com/books.
Jemaneh L., 1997. Intestinal helminth infections in school children in Adarkay District,
Northwest Ethiopia, with special reference to Schistosomiasis mansoni. Ethiop J Health Dev.
11:289-249.
Jordan, P., G. Webbe, and R.F. Sturrock, 1993. Human schistosomiasis. Wallingford: CAB
International, 7:159-183
Kabatereine, N.B., S. Brooker and E.M. Tukahebwa, 2004 . Epidemiology and geography of
Schistosoma mansoni in Uganda: implications for planning control. Trop Med Int Health.
9:372-380
Katz, N., A. Chaves and J. Pellegrino, 1972. A simple device for quantitative stool thicksmear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de Sao
Paulo. 14: 397–400.
King, C.H., 2007. Lifting the burden of schistosomiasis—defining elements of infectionassociated disease and the benefits of anti-parasite treatment. J Infect Dis. 196: 653–55
Kloos, H., Lo, C., Birrie, H., Ayele, T., Tedla, S. and Tsegay, F. 1988. Schistosomiasis in
Ethiopia. Soc. Sci. Med. 26: 803-827.
Kloos, H., 1993. Water resource development and Schistosomiasis in the Awash Valley,
Ethiopia. Soc Sci Med. 20: 609-625.
Kloos, H. and R. David, 2002. The paleoepidemiology of schistosomiasis in ancient Egypt.
Hum. Ecol. Rev. 9: 14-25.
54
Koroma, M.M., A.M. Williams, RR. De La Haye, and M. Hodges, 1996. Effects of
Albendazole on growth of primary school children and the prevalence and intensity of soiltransmitted helminths in Sierra Leone. J Trop Ped. 42: 371-372.
Kreutner, A. K., V. E. Del Bene and M. S. Amstey, 1981. Giardiasis in pregnancy. Am. J.
Obstet. Gynecol. 140:895- 901.
Kumie, A., and A. Ali, 2005. An overview of environmental health status in Ethiopia with
particular emphasis to its organization, drinking water and sanitation: a literature survey.
Ethiop J Health Dev. 19 (2):89-103.
Lansdown, R., A. Ledward, A.Hall, W. Issac, E.Yona & J.Matulu, 2002. “Schistosomiasis,
Helminth Infection, and Health Education in Tanzania: Achieving Behaviour Change in
Primary Schools.” Health Education Research. 17: 425–33.
Lemma, A., P. Goll, J. Duncan and B. Mazengia, 1975. Control of schistosomiasis by the use
of Endod in Adwa, Ethiopia. Results of a five year study. Proc Int Conf Schisto. 415-36.
Lemlem, L., 2008. Current status of Schistosoma mansoni and Soil-transmitted helminthiasis
in primary school Children of Adwa town, northern Ethiopia. Pp.36-39.
Lerman, S. J. and R. A. Walker, 1982. Treatment of Giardiasis. Literature review and
recommendations. Clin. Pediatr. 21:409 - 414.
Lindo, F.J., A.V. Levy, K.M. Baum and J.C. Palmer, 1998. Epidemiology of giardiasis and
cryptosporidiosis in Jamaica. Am. J. Trop. Med. Hyg. 59(5): 717-721.
Mahmud, M.A., C.Chappell, M.M. Hossain, M. Habib and H.L. Dupont, 1995. Risk factors
for development of first symptomatic Giardia infection among infants of a birth cohort in
rural Egypt. Am. J. Trop. Med. Hyg. 53: 84-88.
Markell, E.K. and M. Voge, 1971. Medical Parasitology.3rd Ed. W.B. sounders company.
Philadelphia London. Toronto, 173.
Markell, E.K., D.T. John and W.A. Krotoski, 1999. Markell and Voge’s Medical
Parasitology, 8th ed. W. B. Saunders Co., Philadelphia, Pa.
Martin, L.K. and P.C. Beaver, 1968. Evaluation of Kato thick-smear technique for
quantitative diagnosis of helminth infections. Amer. J. Trop. Med. & Hyg. (17): 382-389.
Marti, H. and E. Escher, 1990. SAF - an alternative fixation solution for parasitological stool
specimens. Schweiz Med Wochenschr. 120: 1473–1476.
McManus, P. and A. Loukas, 2008. Current Status of Vaccines for Schistosomiasis. Clin.
Microbiol.Rev.21:225-242.
55
Megan L., 2006. Prevalence of overweight among Baltimore City school children and its
associations with nutrition and physical activity. Obesity. 14: 989-993.
Mengstu, D., 2010. Malaria and intestinal parasite infections and co-infections in Tach gayint
district, south Gondar zone. Pp.27-28.
Meyer, E. A. and E. L. Jarrol, 1980. Giardia and giardiasis. Am. J. Epidemiol. 111:1- 12
Michael, G.F., 1997. This wormy world: Fifty years on. Parasitol Today, 13 (11): Poster
insert
Montresor, A., D.W.T. Cropton, D.A.P. Bundy, A.Hall and L.Savioli, 1998. Guidelines for
the evaluation of soil transmitted helminthiasis and schistosomiasis at the community level.
Geneva, World Health Organization. Document WHO /CTD /SIP/98.1.
Montresor, A., D.W.T. Crompton, T.W. Gyorkos and L. Savioli, 2002. Helminth control in
school- age children. World Health Organization, Geneva, Switzerland report.
Mulugeta, M., 2008. Prevalence of Schistosoma mansoni and other intestinal parasites among
individuals living nearby three rivers of Jimma Town and the risk factors involved. Pp.37-39.
Naing, L., T. Winn and B.N. Rusil, 2007. Practical issues in calculating sample size for
prevalence studies. Arch Orofac sci. 1: 9-14.
Natividad, F. F., C. C. Buerano, C. B. Lago, C. A. Mapua, B. B. de Guzman, E. B. Seraspe, L.
P. Lorena P Samentar and T. Endo, 2008. Prevalence rates of Giardia and Cryptosporidium
among diarrheic patients in the Philippines. Southeast Asian J. Trop. Med. Public Health. 39:
991-999.
Nester, E.W., D.G. Anderson, C.E. Roberts, N.N. Pearsall and M. Tester, 2001.
Microbiology: A Human Perspective,Third edition. Pp.613-614, 734-736.
NCCLS, 1997. Procedures for the Recovery and Identification of Parasites from the Intestinal
Tract. Approved guideline M28-A. National Committee for Clinical Laboratory Standards,
Wayne, Pa.
Nimri, L.F., 1994. Prevalence of giardiasis among primary school children. Child Care
Health Dev. 20: 231-237.
Nokes, C., S.T. McGarvey and L. Shiue,1999. Evidence for an improvement in cognitive
functionfollowing treatment of Schistosoma japonicum infection in Chinese primary school
children. Am.J. Trop.Med. Hyg. 60:556-65.
56
Oberhelman, R.A., E.S. Guerrero, M.L. Femandez, M. Silio, D. Mercardo, N. Comiskey, G.
Ihenacho, and R. Mera, 1998. Correlations between intestinal parasitosis, physical growth,
and psychomotor development among infants and children from rural Nicaragua. American
.Journal of Tropical Medicine and Hygiene. 58:470-475.
Okpala, H.O., E. Agwu, M.I. Agba, O.R. Chimezie, G.O. Nwobu and A.A. Ohihoin, 2004. A
survey of the prevalence of Schistosomiasis among pupils in Apata and Laranto areas
in Jos, Plateau State. J. Hlth. Allied Scs.1:1.
Olds, G.R., R. Olveda and G.Wu, 1996. Immunity and morbidity in schistosomiasis
japonicum infection.Am.J.Trop.Med.Hyg. 55: 121-126.
Ortega, Y., and R.Adam, 1997. Giardia: overview and update. Clin. Infect. Dis. 25(3): 545549.
Palmer, DR., and DA. Bundy, 1995. Epidemiology of human hookworm and Ascaris
lumbricoides infestations in rural Gambia. East Afr Med J. 72:527-530.
Partovi, F., G. Khalili, A. Kariminia and H.Mahmoudzadeh-Niknam, 2007. Effect of Giardia
lamblia Infection on the cognitive function of school children. Iranian J Publ Health. 36 (1):
73-78.
Peters, P., M. El Alamy, K. Warren and A.Mahmoud, 1980. Quick kato-smear for field
quantification of Schistosoma mansoni eggs. Am J Trop Med Hyg. 29:217-219.
Pollitt, E., 1990. Malnutrition and infection in the classroom. UNESCO, Belgium. P 1-198.
Pontes, LA., MC. Oliveira and Katz N, 2003. Comparison of PCR and the Katho-Katz
technique for diagnosing infection with S. mansoni. American Journal of Tropical Medicine
and Hygiene. 68(6): 652 – 656.
Quihui-Cota, L., M.E. Valenica, D.W.T. Crompton, S. Phillips, P. Hagen, S.P. Diaz
Camacho, A.T. Tejas, 2004. Prevalence and intensity of intestinal parasitic infections in
relation to nutritional status in Mexican school children. Trans R Soc Trop Med Hyg. 98:653659.
Raso, G., A. Luginbühl, C.A. Adjoua, N.T.Tian-Bi, K.D.Silué, B.Matthys, P.Vounatsou,
Y.Wang, M.E.Dumas, E.Holmes, B.H.Singer, M.Tanner, E.K.N’Goran and J. Utzinger, 2004.
Multiple parasite infections and their relationship to self-reported morbidity in a community
of rural Côte d'Ivoire. Int. J. Epidemiol. 33: 1092–1102.
Ruberanziza, E., L. Gahimbare, A. Musemakweri, T. Vervoort, J. Van Den Ende and
J.Clerinx, 2007. Schistosomiasis mansoni in children around Lake Ruhondo, Rwanda A
Clinico-epidemiological study. Rwanda Medical Journal. 66:34-53
57
Scott, J. T., M. Diakhate, K.Vereecken, A. Fall, M. Diop, A. Ly, D. De Clercq, S. J. de Vlas,
D. Berkvens, L.Kestens and B. Gryseels, 2003. Human water contacts patterns in schistosoma
mansoni epidemic foci in northern Senegal change according to age, sex and place of
residence, but are not related to intensity of infection.Trop. Med. Int. Health 8(2): 100-108.
Savioli, L., M.Albonico, D.Engels and A.Montresor, 2004. Progress in the prevention and
control of schistosomiasis and soil-transmitted helminthiasis. Parasitol. Int. 53:103-13.
Schrader,
B.,
2005.
"Giardiasis
Prevention".
Health.http://www.emedicinehealth.com/giardiasis/page9_em.htm#Prevention
EMedicine
Shetty, P., 2006. Malnutrition and undernutrition. Medicine 34(12): 524-529.
Smith, H.V., and T.Paget, 2007. "11. Giardia". In Simjee S. Infectious Disease: Foodborne
Diseases. Humana Press. pp. 303–336. doi:10.1007/978-1-59745-501-5. ISBN 978-1-59745501-5. http://www.springerlink.com/content/pt3g370001u66056/. Chapter-doi:10.1007/978-159745-501-5_11
Solomons, N. W., 1982. Giardiasis: Nutritional implications. Reviews of infectious Diseases.
4: 859-869.
Steinmann, P., J.Keiser, R.Bos, M.Tanner and J. Utzinger, 2006. schistosomiasis and water
resources development: systematic review, meta-analysis, and estimates of people at
risk.Lancet Infect. Dis. 6: 411–425.
Steinmann, P., J. Utzinger, Z.W. Du and X.N. Zhou, 2010. Multiparasitism: a neglected
reality on global, regional and local scale. Adv Parasitol. 73: 21–50.
Stephenson, L.S., M.C. Latham and E.A. Ottesen, 2000b. Malnutrition and parasitic helminth
infections. Parasiiology. 121:S23-S38.
Stoltzfus, R.J., H.M. chwaya. J.M. Tielsch, K.J.Schulze, M. Aibonico and L. Savioli, 1997.
Epidemiology of iron deficiency anemia in Zanzibari school children: importance of
hookworms. American Journal of Clinical Nutrition. 65:153-159.
Stoltzfus, R.J., M. Alhonico, H.B. Chwaya, J.M. Tielsch, K.J. Schulze and L. Savioli, 1998.
Effects of the Zanzibar school-based deworming program on iron status of children. American
Journal of Clinical Nutrition. 68:179-186.
Stothard, R., 2009. Improving control of African schistosomiasis:towards effective use of
rapid diagnostic tests within an appropriate disease surveillance model. Trans. R. Soc. Trop.
Med. Hyg. 103: 325-332.
58
Tadesse, D., Tsehaye, A. and Mekonen, T., 2009. Intestinal Helminthes Infections and ReInfections with Special Emphasis on Schistosomiasis Mansoni in Waja, North Ethiopia.
MEJS. 1(2):4-16.
Teklu, W., 2009.The prevalence of Giardia and Cryptosporidium species infection among
children and cattle in north Shewa zone, Oromia region, Ethiopia. Pp.28-29.
Tedla, S., 1986. Helminthiasis in man in Ethiopia. Helminthologia. 23:43-8.
Thompson, R. C. A., J. A. Reynoldson and A.H.W. Mendis, 1993. Giardia and giardiasis;
Adv. Parasitol. 32: 71-160.
Thompson, S.C., 1994. Infectious diarrhoea in children: Controlling transmission in a
childcare setting. J. Paediatr. Child Health. 30:210-219.
Tilahun, A., 2010. Study of the association of Soil-Transmitted Helminthiasis With
malnutrition and anemia among school children, Debub Achefer district, northwest Ethiopia.
Pp.40-49.
Tsuyuoka, R., J.W. Bailey, G.A.M. Nery, R.Q. Gurgel and L.E.Cuevas, 1999. Anemia and
intestinal parasitic infections in primary school students in Aracaju, Sergipe, Brazil,Cad
Saude Publica 15:413-421.
Ukaga, C.N., P.I. Onyeka and E.B .Nwoke, 2002. Practical medical Parasitology. 1st edition.
Avan Global publications, pp.18-26.
Van der Werf, M.J., S.J.de Vlas, S.Brooker, C.W. Looman, N.J. Nagelkerke, J.D.Habbema
and D.Engels, 2003. Quantification of clinical morbidity associated with schistosome
infection in sub-Saharan Africa. Acta Tropica 86: 125-139.
Wadood, A., A.Bari, A.Rhman and K.F. Qasim, 2005. Frequency of Intestinal Parasite
Infestation in Children Hospital Quetta. Pakistan J Med Res. 44 (2): 87-88.
Webbe, G., 1981. Schistosomiasis: some advances. Brit. Med. J. 283:1104-1106.
WHO, 1987. Prevention and Control of Intestinal Parasitic Infections. WHO Tec Rep Ser. No.
749: 12.
WHO, 1991. Basic Laboratory Methods in Medical Parasitology. World Health
Organization,Geneva.
WHO, 1995. Physical status. The use and interpretation of anthropometry. Reports of WHO
expert committee, Technical Report Series. No.854, Geneva, Swizerland, Pp.6-115.
World Health Organization, 1998. Control of tropical disease. WHO, Geneva report.
59
WHO, 1998. Report of the WHO informal consultation on schistosomiasis control. World
Health Organization, Geneva, WHO/CDS/CPC/SIP/99.2.
WHO, 2004. Prevention and Control of Schistosomiasis and Soil-Transmitted Helminthiasis.
WHO/CDS/CPE/PVC/2004.9.
WHO (2005) Deworming for health and development. Report of the third global meeting of
the partners for parasite control. World Health Organization, Geneva.
WHO, 2006. Child growth standards: length/height-for-age, weight-for-age, weight for-height
and body mass index-for-age: methods and development. Geneva: World Health
Organization.
World Health Organization, 2007. Growth reference data for 5-19 years. Geneva: World
Health Organization.
Wolfe, M.S., 1992. Giardiasis. Clin. Microbiol. Rev. 5: 93-100.
Wu, G.Y. and M.H.Halim, 2000. Schistosomiasis progress and problems. World J
Gastroenterology.6(1):12
60
7. APPENDICES
61
7.1 Appendix: I
Overall Prevalence of intestinal parasites among school children in Adwa town during
February-April, 2012
Parasite
identified
Males (n=227)
Number positive (%)
Females (n=142)
Number positive (%)
Both sex (n=369)
Number positive (%)
Schistosoma mansoni
Giardia lamblia
Hymnolepsis nana
Entamoeba
histolytica
136 (60.0)
52 (22.9)
40 (17.6)
21 (9.3)
58 (40.8)
35 (24.6)
9 (6.3)
15 (10.7)
194 (52.6)
87 (23.6)
49 (13.3)
36 (9.8)
Trituris trichiura
Ascaris lumbricoides
Entrobius
vermicularis
Taenia species
Any single infection
Double infection
Triple infection
Overall prevalence
1 (0.4)
1 (0.4)
1 (0.4)
_
3 (2.1)
_
1 (0.3
4 (1.1)
1(0.3)
1(0.4)
109 (40.0
69 (30.4)
2 (0.8)
180 (79.3)
_
70 (49.3)
25 (17.6
_
95 (66.9)
1 (0.3)
179 (53.4)
94 (25.5)
2 (0.5)
275 (74.5)
62
7.2 Appendix: II
Questionnaires to collect some demographic characteristics of the participants
HARAMAYA UNIVERSITY
Faculty of Education, Department of biology
Dear respondents, the main purpose of this study is to find out the impact of S. mansoni and
G.lamblia infections on the anthropometric measurement of school children. It is also very
important to create awareness on its prevalence and controlling measure among all concerned
bodies. So, this quationnaier helps to gather information about the status of these infections
among the students in Adwa town. The result of this study will be submitted to Haramaya
University, Department of Biology. Therefore, I kindly request you to give your genuine
response for each question. Last, but not least, I would like to thank for your cooperation.
1. Sex: M_______ F_______
2 .Age ______________
3. From where do you get water for drinking?
4. Where do you bath?
A. Stream
5. Do you wash cloth in the streams?
A. Tap
B. stream
B. Home
A. Yes
6. Do you swim in streams during rainy season?
B. No
A. Yes
B. No
7. Do you make contact with the river during you cross it? A. Yes
8. Do you have toilet at your home?
A. Yes
B. No
9. Do you defecate at open field? A. Yes
B. No
10. Do you wash your hands after defecation? A. Yes
63
B. No
B. No
7.3 Appendix: III
Laboratory data form
1. Results of stool examination
1.1 Microscopic Examination of stool
a. positive
b. negative
1.2 Kato –katz technique
Schistosoma mansoni eggs/slide
________________epg ___________
2. Anthropometric measuriment
a. height __________
b. Weight __________
64
7.4 Appendix: IV
65
66