International Journal of MCH and AIDS (2012),Volume 1, Issue 1, Pages 73-82

INTERNATIONAL JOURNAL
of MCH and AIDS
ISSN 2161-864X (Online)
ISSN 2161-8674 (Print)
Available online at www.mchandaids.org

ORIGINAL ARTICLE
The Impact of Intestinal Parasitic Infections on the Nutritional Status of
Rural and Urban School-Aged Children in Nigeria
Kenneth N. Opara, PhD1 *; Nsima I. Udoidung, PhD1; Dominic C. Opara, PhD2; Okpok E. Okon, PhD3;
Evelyn U. Edosomwan, PhD4; Anietie J. Udoh, BSc1
1
Department of Zoology, University of Uyo, Uyo, Akwa Ibom State, Nigeria
2
Department of Community Health, University of Uyo, Uyo, Nigeria
3
Department of Zoology and Environmental Biology, University of Calabar, Cross River State, Nigeria
4
Department of Animal and Environmental Biology, University of Benin, Benin City. Nigeria
*
Corresponding author e-mail: [email protected]

ABSTRACT
Objectives
Intestinal parasitic infection and undernutrition are still major public health problems in poor and developing
countries.The objective of this study was to assess the relationship between intestinal parasitic infection and
nutritional status in 405 primary school children from rural and urban areas of Akwa Ibom State, Nigeria.
Methods
This cross-sectional survey in 2009 obtained anthropometric data, height-for-age (HA), weight-for-height (WH)
and weight-for-age (WA) Z-scores from each child and fecal samples were also collected and screened for
intestinal parasites using standard parasitological protocols.
Results
The prevalence of infection with any intestinal parasite was 67.4%. A total of six intestinal parasites
were detected; hookworm (41.7%) had the highest prevalence. The prevalence of intestinal parasites and
undernutrition was significantly higher in rural than in urban children (P<0.001). The prevalence of stunting
(HAZ < -2), underweight (WAZ < -2) and wasting (WHZ < -2) for rural and urban children were 42.3%
vs. 29.7%; underweight 43.2% vs. 29.6% and wasting 10.9% vs. 6.4%, respectively. With respect to nutritional
indicators, the infected children had significantly (P<0.05) higher z-scores than the uninfected children.
Multivariate logistic regression analysis showed that only Hookworm and Ascaris lumbricoides were each
significantly (P<0.05) associated with stunting, wasting, and underweight.
Conclusions and Public Health Implications
Since intestinal parasitic infections are associated with malnutrition, controlling these parasites could increase
the physical development and well-being of the affected children.
Key Words
Intestinal parasites • malnutrition • children • rural-urban • Nigeria.

© 2012 Global Health and Education Projects Inc.

 Infection and Nutritional Status of Nigerian Children

Introduction Methods
In developing countries, intestinal parasitism Study Sites
is a major public health problem that is often The study was carried out in two primary schools
neglected. In these less developed countries, in Akwa Ibom State, Nigeria. The schools are
poor environmental and personal hygiene, poor Methodist Primary School, Mbiabong Ikot Udofia
nutrition, overcrowding and climatic conditions in Ini Local Government Area (LGA), a typical
that favor the development and survival of these rural setting and Government Primary School, Ikot
parasites are some of the factors contributing to Ntuen Oku, Uyo in Uyo Local Government Area
the high level of intestinal parasites transmission[1-3]. (an urban setting). The two LGAs are in Akwa Ibom
School children carry the heaviest burden of the State. The State lies between latitudes 4°33’ and
associated morbidity[4], due to their dirty habits 5°33 North and longitudes 7°35’ and 8°25 East. It is
of playing or handling of infested soils, eating with characterized by humid tropical climate with annual
soiled hands, unhygienic toilet practices, drinking rainfall reaching 23,000mm per annum.Temperature
and eating of contaminated water and food[5]. regime is uniform with annual values of 20.4°C to
There are documented reports implicating 35.7°C.The State has two distinct seasons, the rainy
intestinal parasitic infection with poor nutritional season from May to October, and the dry season
status in children of school age[6-10]. Amoebiasis, from November to April. Pit latrine is common,
Giardiasis, Acariasis, Hookworm infection, and while open air defecation is freely practiced.
Trichuriasis are among the most common intestinal
parasitic infection worldwide. These infections
Subjects
are associated with decreased child growth, low
plasma vitamin A, loss of weight, chronic blood The study was carried out between April and
loss, iron deficiency anemia, diarrhea, and stunted November 2009. The study employed stratified
growth[4,11,12]. Alteration of the normal gastro- random sampling to select the study subjects. For
intestinal flora by intestinal parasites has been eligibility to participate in the study, a child had to be
found to be associated with diarrhea, a major attending one of the selected schools. Each enrolled
cause of childhood morbidity and mortality in child’s date of birth, age, gender, and occupation
developing countries[13]. of parents was obtained from the class teacher’s
There is a plethora of publications on prevalence registers and recorded on a standardized field form.
and intensity of intestinal parasites in Nigeria,[2,3,14]. In each selected class, at least 40 pupils from each
Surprisingly, there is paucity of information on of the 6 educational grades were chosen at random.
the impact of these parasites on the nutritional
status of their host, especially children. This study Ethical Clearance
therefore aims to fill this gap in knowledge by Prior to any enrollment of the children, permission
investigating the association between intestinal was sought and obtained from the head-teacher of
parasitic infection and nutritional status of primary the respective schools and parents and/or guardian
school children in rural and urban settings of Akwa of the children.The study protocol was approved by
Ibom State, Nigeria. The outcome may strengthen the State Ministry of Health.
the global shift in the control of neglected tropical
diseases. Anthropometric Measurement
Anthropometric measurements were carried out
by a nutritionist (DCO) in the research team.

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Opara et al International Journal of MCH and AIDS (2012),oV l. 1, No.1, Pages 73-82

The subjects were weighed barefooted and in between intestinal parasitic infection and nutritional
light clothing on a bathroom scale accurate to indicators was tested using multivariate logistic
0.1kg. The scale was standardized before use regression. All statistical analysis was performed
with 11kg weight. Height was measured to the using version 14.0 of the SPSS for windows software
nearest 1cm, with a paper stadiometer attached package (SPSS Inc., Chicago IL).
to a vertical wall. Subjects stood barefooted with
their scapula, buttocks and heels’ resting against a
wall, the neck was held in a natural non-stretched Results
position, and the heels were touching each other.
A total of 418 children (228 rural and 190 urban)
Nutritional status indicators were classified
were initially enrolled, the result presented below
and standardized into sex-specific Z-scores for
are the data for 405 children (220 rural and 185
height-for-age (HAZ), weight-for-height (WHZ)
urban) who returned suitable stool specimen after
and weight-for-age (WAZ) in EPI Info (version
their anthropometric data were collected. There
3.2) relative to the CDC/WHO 1978 reference
were 100 males and 120 females for rural areas
curves recommended for international use[15,16].
and 105 males and 80 females for urban areas. The
Children were classified as stunted, wasted, and
subjects were aged between 2.9 and 14 years, with
underweight if their HAZ, WHZ and WAZ was
a mean (SD) age of 8.5 (4.7). Table 1 summarizes
< - 2 SD respectively.
the prevalence of intestinal parasite in the children.
At least one species of intestinal parasite was
Parasitological Examination found in 273 (67.4%) of the children examined.
Each enrolled child was asked to provide a fresh Prevalence of infection was significantly (P<0.001)
fecal sample in cleaned and dried specimen bottles higher among the rural (80.9%) children than
provided. The pupils were adequately instructed among the urban (51.4%) children. Prevalence
on how to get a little portion of their stool into the of hookworm was higher (55.9% vs. 24.9%) than
bottles. Their class teachers ensured compliance. all other parasites encountered from rural and
The samples collected on each occasion were urban children respectively (P<0.05). The other
all examined in the University of Uyo Medical parasites were A. lumbricoides (30.5% vs. 16.8%);
Center laboratory without preservation. Each T. trichiura (4.1% vs. 5.4%); G. lamblia (3.2% vs. 2.2%)
fecal sample was examined as a smear stained and E. histolytica (0.9% vs. 4.3%). The prevalence
with Lugol’s iodine, as a direct wet smear in of polyparasitism is further shown in Table 1, one
physiological normal saline and by formol-ether species of intestinal parasite were found in (49.1%
concentration technique[17-18]. Diagnosis was vs. 32.4%) for rural and urban children respectively.
based on the identification of helminth ova and The subjects co-infected with two species of
protozoan cyst in the sample during microscopic parasites were (23.6% vs. 14.6%), while 8.2% vs.
analysis. A child was considered to have a 4.3% were with 3 or more species of parasite in
polyparasitic infection if they were found to be rural vs. urban children.
positive for more than one species. The age-specific prevalence of infection in rural
children is presented in Table 2. Prevalence tends
Data Analysis to increase with age, with the highest infection
Categorical variables are presented as percentages occurring in the age group of 12–14 years, for
and continuous variables as means and standard Hookworm and Ascaris infection. In urban children,
deviation (SD). Univariate analysis was carried out the age group of 3–8 years had the highest infection
using the c2 test for proportion. The association rate (Table 3). The overall prevalence of nutritional

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 Infection and Nutritional Status of Nigerian Children

indicators is presented in Table 4, stunting (42.3% significantly (P<0.001) associated with low height-
vs. 29.7%); underweight (43.2% vs. 29.6%) wasting for-age (stunting), weight-for-height (wasting) and
(10.9% vs. 6.4%) for rural and urban pupils weight-for-age (underweight). With respect to the
respectively. Rural children were significantly nutritional indicators, the infected children had
(P<0.001) more malnourished than urban children. a significantly (P<0.05) higher Z-score than the
Only Hookworm and A. lumbricoides were uninfected children.

Table 1. P
 revalence of Intestinal Parasites among Children in Rural and Urban Communities

Rural children Urban children All children

Parasite No (%) infected No (%) infected No (%)
n = 220 n = 185 n = 405
Any 178 (80.9) 95 (51.4) 273 (67.4)
Hookworm 123 (55.9) 46 (24.9) 169 (41.7)
A. lumbricoides 67 (30.5) 31 (16.8) 98 (24.2)
T. trichiura 9 (4.1) 10 (5.4) 19 (4.7)
G. lamblia 7 (3.2) 4 (2.2) 11 (2.7)
E. histolytica 2 (0.9) 8 (2.3) 10 (2.4)

No. of intestinal parasite per child

1 108 (49.1) 60 (32.4) 168 (41.5)
2. 52 (23.6) 27 (14.6) 79 (19.5)
>= 3 18 (8.2) 8 (4.3) 26 (6.4)

Table 2. The Age-Specific Prevalence of Intestinal Parasite among 220 Rural children

Age (years)
3 – 5 6 – 8 9 – 11 12 - 14

No. of children investigated 32 84 66 38

No. infected with:
Hookworm 15 (46.9) 47 (56.0) 36 (54.5) 25 (65.8)
A. lumbricoides 5 (15.6) 26 (30.9) 21 (31.8) 15 (39.5)
T. trihiura 0 (0) 7 (8.3) 2 (3.0) 0 (0)
G. lamblia 1 (3.1) 4 (4.8) 1 (1.5) 1 (2.6)
E. histolytica 1 (3.1) 0 (0) 1 (1.5) 0 (0)

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Opara et al International Journal of MCH and AIDS (2012),oV l. 1, No.1, Pages 73-82

Table 3. The Age-Specific Prevalence of Intestinal Parasite among 185 Urban Children

Age (years)
3 – 5 6 – 8 9 – 11 12 - 14

No. of children investigated 57 51 45 32

No. infected with:
Hookworm 16 (28.0) 14 (27.5) 9 (20.0) 7 (61.9)
A. lumbricoides 15 (26.3) 9 (17.6) 4 (8.9) 3 (9.4)
T. trihiura 5 (8.8) 3 (5.9) 1 (2.2) 1 (3.1)
G. lamblia 0 (0) 0 (0) 4 (8.9) 0 (0)
E. histolytica 3 (5.3) 1 (2.0) 0 (0) 0 (0)

Table 4. Summary of Nutritional Indices (Z-scores) of Rural and Urban Children

RURAL URBAN
Height-for-age Weight-for-age Weight-for-height Height-for-age Weight-for-age Weight-for-height
(stunting) (underweight) (wasting) (stunting) (underweight) (wasting)
No. examined 220 220 220 185 185 185
No. below –2SD 93 95 24 55 55 12
% below –2SD 42.3 43.2 10.9 29.7 29.7 6.5
Mean z-score -1.602 -1.717 -1.511 -1.942 -1.834 -1.501
SD 1.70 1.11 1.41 1.53 1.44 1.23
SEX
No. (%) of boys
Below –2SD 40 (40.0) 48 (48.0) 14 (14.0) 33 (31.4) 36 (34.3) 7 (6.7)
No. (%) of girls
Below –2SD 53 (44.2) 47 (39.2) 10 (8.3) 22 (27.5) 18 (22.5) 5 (6.3)

Discussion significantly more infected than children from the

urban areas (51.4%). This finding corroborates the
Generally intestinal parasitic infection abounds report of Hurtado et al.[25] that a high prevalence
in developing countries[18], with school children of intestinal parasites is consistent with what is
carrying the heaviest burden of the associated found throughout indigenous population in the
morbidity[20, 21]. rural tropical areas. The prevalence obtained for
The prevalence of 67.4% recorded in this study is intestinal parasites in the rural areas of the present
consistent with 70%, 70.8%, 62.0% obtained in Kwara, study is consistent with 82.6% obtained by Ukpai
Ogun and Plateau States of Nigeria respectively[22-24]. and Ugwu[26] in Southern Nigeria. In rural areas,
Such high prevalence has been attributed to poor ignorance, unhealthy socio-cultural and religious
environmental and personal hygiene, shortages of practices, lack of basic public amenities, poor
clean potable water and indiscriminate defecation[13]. sanitation, poverty and inadequate access to health
School children from the rural areas (80.9%) were care are major predisposing factors to intestinal

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 Infection and Nutritional Status of Nigerian Children

parasitic infections[27].This study observed the above possible that the longevity of hookworm eggs and
factors in the rural community where the school is larvae in soil and on vegetation might have been
located. The school used in the present study lack enhancing transmission. Other workers elsewhere
adequate toilet facility. There is complete absence have reported a high prevalence of hookworm
of potable water, student obtain their water from infection in their studies[3,30,32,33]. Hookworm and
nearby stream that might have been contaminated Ascaris infection increased with age among the
with fecal matter. Evidently, students defecate rural children, while children aged 3–5 years in
indiscriminately in the bushes around the school the urban area had the highest prevalence for the
premises as observed with fecal littering, which two parasites. No single age group had the highest
were likely to contain ova and/or cyst of parasites. prevalence for all the intestinal parasites detected.
The 51.4% prevalence obtained in urban children in This present study recorded a high degree of
this study, though lower than the rural prevalence, malnutrition among the children investigated for
is relatively high. The result is similar to the 54.7% intestinal parasitic infections. These findings agree
and 50.6% recorded by Egwunyenga and Ataikiru[2] with the publication of other investigators[6,8,9,33,34].
and Igbinaso et al.[28] in Delta and Anambra States The high rate (>=30%) of stunting and underweight
of Nigeria respectively. It is possible that the home recorded in this study might be due to high
communities of the urban children are more aware prevalence of hookworm, Ascaris and Trichuris. It has
of parasitic infections and have slightly better been documented by Crompton and Neisheim[34]
sanitation and improved personal hygiene than rural that growth and development during childhood
communities. Furthermore access to health care could be diminished by ascariasis, trichiuriasis and
is within the reach of the urban children. Despite hookworm infection. Multivariate analysis showed
all these factors, the relatively high prevalence a significant association between hookworm,
connotes continuous infection, re-infection and Ascaris and anthropometric parameters suggesting
transmission of intestinal parasites. that these helminths affect the nutritional status
The occurrence of poly parasitism in this study of the studied children. While this present study
is in line with what is obtained elsewhere in the did not obtain a significant association between
tropics and subtropics[4, 26, 29-30]. The commonest was nutritional indicators and protozoan parasites
the co-infection of hookworm and A. lumbricoides. (G. lamblia, E. histolytica), similar studies in Tehran and
No individual had up to four parasites. Hookworm Brazil by Nematian et al.[9] and Carvalho Costa et
was the most prevalent. The poor fecal disposal al.[8] respectively, recorded a significant association
system coupled with the fact that most of the between G. lamblia and nutritional status. According
children play barefooted might have exposed them to Assis et al.[35] the social, economic and physical
to infective stage of the hookworm larvae. The environment in which an individual lives are major
use of excreta as manure commonly practiced determinant of the degree of association between
by vegetable farmers might also be acting as a intestinal parasites and nutritional status. These
veritable source of infection since children and factors might be responsible for the difference
their mothers often go to the farm to tender the observed in this study when compared with others
vegetables[20]. Ukoli[31] described warmth, shade, elsewhere. Although causes of malnutrition are
moisture, optimum temperature of 230C to 300C multifactorial intestinal parasitic infections have
and loose humus soil as suitable environmental been associated with impaired growth[9,36,37] and
conditions for the survival of hookworm egg and stunting[12] in diverse population. There are several
larvae. Since these conditions are almost similar mechanisms by which intestinal parasitism may
to the climatic conditions of the study area, it is cause or aggravate malnutrition including impaired

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Opara et al International Journal of MCH and AIDS (2012),oV l. 1, No.1, Pages 73-82

nutrient absorption resulting from infection and malnutrition and the intensities of the infection, as a
reduced appetite[34]. Adult helminth worms residing consequence, the actual cause(s) of wasting recorded
in the small intestine are in an excellent position to in the study could not be ascertained. Intestinal
interfere with their host nutrition and can induce parasitism is one of the neglected tropical diseases
damage to the intestinal mucosa that may reduce that remain a common public health problem in
a person’s ability to extract and absorb nutrient most developing countries. With the current global
from food[38]. Intestinal parasitic infections can economic meltdown, dietary inadequacies and
cause vomiting, diarrhea, anorexia, abdominal pain other forms of nutritional stresses, the harboring
and nausea that may result in reduced food intake, of heavy intestinal parasites by children could have
thereby further reducing nutrient availability[36,39]. adverse health implications. Hence, there is the
The most significant cause of nutritional stress need for policy makers to intensify health education
resulting from helminth infection is hookworm program in schools. School-based education may be
associated iron-deficiency anemia. It is documented an effective way of reaching the larger population,
that light hookworm infections of 20 – 50 adults parents and families of the student and other
worms can result in significant iron losses[37]. Even members of the community. In view of the high
mild to moderate intensity helminth infection during prevalence of intestinal parasites recorded in this
childhood have been associated with undernutrition study, mass chemotherapy will be of immense benefit
and reduced physical fitness[39,40]. All these factors on child growth, development and cognitive abilities.
singly or collectively might have contributed to the Intestinal parasitic infections affect childhood
high degree of malnutrition observed in this study. development and morbidity in many developing
countries. Reducing the prevalence of parasitic
Conclusions and Public Health Implications infections in school children, may be of tremendous
A weakness of the present study is that no attempt benefit on child growth, development and
was made to determine biochemical indicators of educational outcome.

Acknowledgements: We express our sincere appreciation to the head-teacher, teachers, parents and
pupils of the study schools for their approval and cooperation throughout the duration of the study.

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