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Malnutrition and intestinal helminth
infections in schoolchildren from Dibanda,
Cameroon
J.V. Mbuh* and N.E. Nembu
Department of Plant and Animal Sciences, Faculty of Science, University
of Buea, Cameroon
(Received 18 April 2011; Accepted 22 December 2011; First Published Online 25 January 2012)
Abstract
Intestinal helminth infections and malnutrition constitute a major health
burden in developing countries, with infants and children being the most
vulnerable groups. The extent of the burden of intestinal helminth infections and
malnutrition was investigated in a cross-sectional study involving 265 children
aged between 4 and 14 years residing in Dibanda, a semi-rural area located in
Buea, South West Region, Cameroon. The prevalence of intestinal helminth
infections was determined microscopically after faecal samples were prepared
by the formol-ether sedimentation concentration technique of stool analysis.
Nutritional status was determined using age and the anthropometric parameters
of weight and height. Standard deviation (SD) or Z scores of height-for-age
(HAZ), weight-for-age (WAZ) and weight-for-height (WHZ) were computed
based on the World Health Organization 2006 growth reference curves. Anaemia
was assessed by packed cell volume (PCV). The prevalence of intestinal
helminth infection in the study population was 47.2% (125/265). All infections
were of low intensity, with Ascaris recording the highest geometric mean egg
count (GMEC) ^SEM of 363.51 ^60.35 (egg count range: 76 – 3000 eggs/gram
of stool). Overall, 42.3% of children had PCV ,31%. Also, 47.2% of those
with intestinal helminth infections also had PCV ,31%. The prevalence
of malnutrition was 30.2% (80/265). Of 80 malnourished children, 5.3%
were wasted (,22SD weight-for-height Z-score), 7.2% underweight (,22SD
weight-for-age Z score) and 24.2% stunted (,22SD height-for-age Z score). The
mean values of all the anthropometric indices were lower in helminth-infected
children. Findings from this study are strongly suggestive that intestinal
helminth infections and malnutrition exist in children residing in Dibanda and
constitute a major health problem that needs to be addressed immediately to
reduce morbidity and mortality.
Introduction
Malnutrition and intestinal parasitic infections (IPIs)
are common public health problems of children in
developing countries, causing thousands of avoidable
deaths each year (Garba & Mbofung, 2010). IPIs are
globally endemic and have been described as constituting
the greatest single worldwide cause of illness and
disease (Steketee, 2003). For reasons not well understood,
compared with any other age group, preschool and
school-aged children (including adolescents) tend to
harbour the greatest numbers of intestinal worms and, as
a result, experience growth stunting, diminished physical
fitness as well as impaired memory and cognition
(Crompton & Nesheim, 2002). These adverse health
consequences combine to impair childhood educational
*E-mail: judithmbuh@yahoo.com
Journal of Helminthology (2013) 87, 46–51 doi:10.1017/S0022149X12000016
qCambridge University Press 2012
performance, reduce school attendance and account
for the observation that hookworms, and presumably
other diseases caused by parasitic worms, reduce future
wage-earning capacity (Bleakley, 2007). Even mild to
moderate-intensity helminth infections during childhood
have been associated with undernutrition and reduced
physical fitness.
Observational data suggest an inverse relation between
intestinal helminthiasis and haemoglobin concentrations.
While the aetiology of anaemia is complex and multi-
factorial, iron deficiency due to parasitic diseases has
long been recognized as a major contributor in endemic
countries. Hookworms have for a long time been
recognized as an important source of blood loss leading
to iron deficiency anaemia (Hotez et al., 2005).
Cameroon launched the National Programme for the
Control of Schistosomiasis and Intestinal Helminthiasis
(PNLSHI) (MINSANTE, 2004) in 2003. As priority
projects, PNLSHI ensures that anthelmintic drugs are
always available in all health centres, educates commu-
nities about worms and the risks of infection, and
promotes hygiene, good water and sanitation systems
in communities. However, intestinal helminth infections
still remain a major heath burden with no up-to-date
epidemiological data available for intestinal helminth
infections in many parts of the country. This is a serious
handicap to the attempt to control the disease. This
study therefore aimed at investigating the impact of
intestinal helminth infections on the nutritional status
of school-aged children living in Dibanda. It established
the prevalence of soil-transmitted helminth (STH)
infections and malnutrition in school-aged children and
assessed the extent to which their coexistence influences
each other.
The major factor that favours intestinal helminth
transmission in Dibanda is poor environmental sani-
tation, with many households lacking basic toilet
facilities. Most of the inhabitants are subsistence farmers
with limited financial resources. Although grains, tubers,
fruits and vegetables are abundantly grown in this
locality, most of them are sold to traders from the nearby
economic capital of Douala rather than consumed locally,
thereby contributing to poor diets. These factors made
Dibanda an important site for this investigation of the
interrelation between intestinal helminth infections and
nutritional status.
Materials and methods
Study site and population
Dibanda is located some 22 km from the Atlantic Ocean
at the Golf of Guinea, and on the eastern flank of the
active volcanic Mt Cameroon. It is a semi-rural setting
with a heterogeneous and multi-ethnic population of
approximately 5000 inhabitants, with about 1500 of these
being children #14 years of age. Poor environmental
and hygiene practices place inhabitants at higher risk
of STH infections. As a result of poverty, most fruits
and vegetables, although grown abundantly, are sold
rather than consumed locally, thus exaggerating the poor
nutritional status of these children. This study included
265 primary schoolchildren (119 boys and 146 girls)
between the ages of 4 and 14 years. Ethical and
administrative clearance for the study was obtained
from the South West Regional Delegation of Public Health
and Basic Education, respectively. The objectives and
advantages of the study were explained to teachers
and pupils. Only pupils who presented consent forms
signed by their parents or guardians were recruited in this
survey. All pupils diagnosed positive for intestinal STHs
were treated free of charge using single-dose meben-
dazole (500 mg). This study was carried out between
January and August 2010.
Collection and analysis of faecal samples
Pupils were given clean stool collection bottles and
faecal samples were collected on the same day. The
consistency of each faecal sample was noted as hard, soft,
diarrhoeic or watery. Labelled samples were transported
on ice in a cool box to the University of Buea Life
Science laboratory, preserved with 10% formalin, and
subsequently examined for the presence of intestinal
helminth species.
The formol-ether sedimentation concentration pro-
cedure is recommended as being the easiest to perform,
allowing recovery of the broadest range of organisms,
and being the least subject to technical error (Lynnes &
Bruckner, 1997). This procedure leads to the recovery of
all eggs and larvae present. The protocol developed by
Ritchie (1948) and described by Ash & Orihel (1991)
was followed using 1 g of stool; all of the sediment was
examined. The mean number of eggs/gram (epg) of stool
was used as the quantitative measure of infection status,
based on the average egg count for each specimen.
World Health Organization (WHO) criteria were used
to classify each infected sample as being of low, moderate
or high-intensity infection. For A. lumbricoides infection,
light ¼1 –4999 epg, moderate ¼5000– 9999 epg, and
severe $10 000 epg. For hookworm infection, light
¼1 –1999 epg, moderate ¼2000 – 3999 epg, and severe
$4000 epg. For Trichuris trichiura, 1 –1999 epg represented
light, 2000 –3999 epg moderate and $4000 epg severe
worm burden (World Health Organization, 2002).
Anthropometric measurements for nutritional status
assessment
Nutritional status was determined using age and
anthropometric parameters of weight and height. Ages of
children were obtained from school records with the
permission of the head teacher. Weights were measured
using a Tarraillon weighing scale (Terraillon, Paris) and
heights using a height measuring board. Heights, weights
and ages were then related to references as standard
deviation (SD) scores or Z scores. The Z score values of
height-for-age (HAZ), which is an indicator of chronic
malnutrition and is used to identify stunted children,
weight-for-age (WAZ), which is an indicator of both acute
and chronic malnutrition, and weight-for-height (WHZ),
which is an indicator of acute malnutrition, were
calculated. These Z scores were computed based on the
WHO 2006 growth reference curves (World Health
Organization, Multicentre Growth Reference Study
Group, 2006). For the purposes of descriptive analyses,
Malnutrition and intestinal helminth infections in schoolchildren from Cameroon 47
individuals were classified as stunted, underweight and/
or wasted if the HAZ, WAZ and WHZ scores were
respectively more than 2SD below the WHO mean
international growth reference standard values.
Packed cell volume
Packed cell volume (PCV) was used to screen for
anaemia. Blood samples were collected from study
participants by a finger prick, and used for the
determination of PCV. Each heparinized PCV tube was
filled to about three-quarters its length, sealed at one
end with plasticine, labelled with the subject’s ID number
and spun in a microhaematocrit centrifuge (Hettich,
Zentrifugen, Germany) at 12,800 rpm for 5 min to obtain
constant packing of red cells. PCV values were then read
from the spiral scale of the microhaematocrit reader and
results expressed as percentages (Cheesbrough, 2005).
Statistical analysis
Statistical analysis was conducted using the Statistical
Package for Social Sciences, SPSS
TM
version 17.0 for
Windows (SPSS Inc., Chicago, Illinois, USA). Chi-square
(
x
2
) tests were used to test for differences in nutritional
status and prevalence of helminth infections and anaemia
among the sexes and age groups. Anthropometric
indicators were calculated using an SPSS macro designed
and made available by WHO. This macro uses the
WHO 2006 international growth reference standard. The
anthropometric indices: HAZ, WAZ and WHZ were
expressed as mean and SD to describe the patterns of
nutrition in the different age groups. One-way ANOVA
and two-tailed t-test, where necessary, were used to
compare means, and also to examine the relationship
between anthropometry (or nutritional status) and
the presence of polyparasitic infections and anaemia.
Correlation analysis was used to predict the relation-
ship between anthropometric indices and intestinal
helminthiasis, and also the relationship between PCV
,31% and helminth infections. All results were con-
sidered to be significant at the 95% probability level
(P,0.05).
Results
A total of 265 schoolchildren (119 males and 146
females) were selected for the survey. The children were
placed in the following three age groups: #5 years (46),
5.1–9 years (100) and 9.1– 14 years (119). Data gathered
from the questionnaire are summarized in table 1.
Prevalence of intestinal helminth infections
Of the 265 children who provided stool samples for
examination, 47.2% (125) were infected with at least one
of the soil-transmitted helminth species. Male and female
prevalences were respectively 48.7% (58/119) and 45.9%
(67/146). Gender did not significantly influence the
prevalence of helminth infections (table 2). The highest
prevalence of helminth infection, 50.0% (23/46),
was recorded in the #5 years age group. Egg load
ranged from 76 to 3000 epg for Ascaris and 100 – 400 for
Trichuris. Ascaris recorded the highest geometric mean
egg count (GMEC) ^SEM of 363.51 ^60.35 (table 2).
There was a significant difference (P,0.05) in the
distribution of hookworm egg load in the different age
groups and gender. No child was heavily infected with
any of the helminth species.
Helminth infection and packed cell volume
Of the 125 children who were infected with intestinal
helminths, 47.2% had PCV values ,31%. The mean PCV
in each case was lower for helminth-infected than for non-
infected children, and this difference was significant for
hookworm infection. A significant negative correlation
was observed between hookworm egg load and PCV
(r¼20.382).
Prevalence of malnutrition
The prevalence (table 3) of malnutrition in school-
children in Dibanda stood at 30.2%, with females
recording a higher (33.6%), though not significant,
prevalence than males (26.1%). Prevalence ranged from
21% in the 5.1–9-year-old age group to 36.1% in the
9.1–14-year-old age group. Age significantly influenced
the prevalence of malnutrition in the study population
(P,0.05).
Helminth infections and anthropometric indices
In the entire sample, children who were positive for
at least a single helminth infection had lower mean values
of HAZ, WAZ and HAZ scores than children who were
not infected with helminths. These differences were,
however, not significant (table 4). There was a significant
difference in the mean HAZ between those who were
Table 1. Questionnaire responses (%) in relation to a
number of variables ranging from the history of
febrile illness to latrine care.
Variable Yes (%) No (%)
History of febrile illness 76.6 23.4
Vomiting 30.6 69.4
Anthelmintic use 59.2 40.8
Herbal drug use 67.2 32.8
Abdominal pain 79.2 20.8
Diarrhoea 43.8 56.2
Anti-malaria drug use 50.6 49.4
Geophagy 66.0 34.0
Mother’s education
Primary and below 68.3 31.7
Above primary 31.7 68.3
Mother’s working status
Non-working 4.5 95.47
Farmer 58.9 41.1
Others 36.6 63.40
Latrine care
Never 21.1 63.4
At most once a week 47.2 52.8
Daily 31.7 68.3
48 J.V. Mbuh and N.E. Nembu
helminth negative and those who harboured single or
multiple helminth infections. Children who were positive
for two or more species had lower mean values of
WAZ and HAZ than those with single, or no helminth
infections. The differences, however, were not statistically
significant.
Malnutrition, helminth infection and packed cell volume
Out of 125 children diagnosed positive for intestinal
helminths, 31.2% (39) were malnourished. Most of those
malnourished also had PCV ,31% (fig. 1). Mean
anthropometric indices were lower in all cases of
infection. Although there was no significant difference
in the prevalence of malnutrition between helminth-
infected and non-helminth-infected children, there was
a significant association between the most common
parasitic infection, Ascaris, and malnutrition.
Discussion
In this study, 265 schoolchildren in Dibanda were
successfully studied. The prevalence of intestinal
helminth infections stood at 47.2%. This high prevalence
of intestinal parasites is consistent with reports from
many indigenous populations in the rural tropics
(Hurtado et al., 2005), including those of Ndamukong
et al. (2000) and Mbuh et al. (2010) in Cameroon.
In Dibanda, poor socio-economic status, poor hygienic
practices and lack of proper sanitation propagate
intestinal helminth infections. Most of the toilets in
the schools were poorly sanitized, not equipped with
lavatories, and the number of users far outnumbered the
available facilities. As a result, some children were forced
to defecate in nearby bushes, and failed to wash their
hands because of overcrowding around taps or, in some
cases, taps with interrupted water supply. These do not
only propagate infection but also help children to develop
attitudes of poor hygiene which are practised later on in
life. Most children (66%) accepted that they will eat or
drink soil-contaminated materials. Also, 47.2% reported
that their latrines are never washed, while 21.1% have
their latrines washed at most once a week.
All helminth infections were of light intensity. All the
head teachers reported that their schools are beneficiaries
of the free donations of mebendazole by PNLSHI
in Cameroon. This occasional deworming could possibly
be responsible for the low worm burden. Analysis of
questionnaire data revealed that 59.2% of the pupils were
occasionally administered anthelmintics. As reported
by Hall, hosts tend to be infected for long periods of
time with slowly fluctuating numbers of worms and,
even if all children in a community are infected, the
majority are usually lightly infected (Hall, 1993).
Overall, 42.3% of children had PCV values ,31%.
There was a significant association (P,0.05) between
hookworm infection and PCV ,31%. Hookworms have a
high propensity to feed on blood because of their ability
to produce intestinal haemorrhage. Although there was
no significant association between low PCV values and
the prevalence of Ascaris and Trichuris infections, mean
PCV values were lower in helminth-positive than in
helminth-negative individuals.
Table 2. The prevalence (%) and intensity of infection with soil-transmitted helminths as affected by sex and age groups of pupils.
Intensity of infection (epg)
Ascaris Trichuris Hookworms
Description N% GMEC ^SEM Range GMEC ^SEM Range GMEC ^SEM Range
Male 119 48.7 323.01 ^101.73 96 –3000 154.98 ^27.87 100– 400 302.29 ^79.95 84– 1400
Female 146 45.9 415.04 ^68.49 76 –2100 210.74 ^20.0 100 –300 194.44 ^30.73 100 – 700
Level of significance P¼0.367 P¼0.164 P¼0.221 P¼0.019
#5 years 46 50.0 407.0 ^174.90 100 –2100 100 ^0.00 100– 100 514.10 ^170.33 200– 1400
5.1–9 years 100 47.0 340.16 ^85.47 100–2600 202.37 ^17.95 100 – 300 220.27 ^62.01 100 – 1200
9.1–14 years 119 46.2 367.22 ^91.85 76–3000 176.17 ^33.33 100 – 400 198.90 ^46.50 84 – 900
Level of significance P¼0.908 P¼0.636 P¼0.246 P¼0.01
Overall 265 47.2 363.51 ^60.35 76 –3000 178.22 ^18.00 100 –400 242.44 ^44.75 84 – 1400
N, Number of children examined; GMEC, geometric mean egg count; SEM, standard error of mean; epg, eggs per gram.
Table 3. The prevalence (%) of malnutrition relative to the sex and age of children.
Description
Number
examined
Malnourished
(%)
Not malnourished
(%)
Male 119 26.1 73.9
Female 146 33.6 66.4
Level of significance P¼0.117
#5 years 46 34.8 65.2
5.1–9 years 100 21.0 79.0
9.1–14 years 119 36.1 63.9
Level of significance P¼0.039
Overall 265 30.2 69.8
Malnutrition and intestinal helminth infections in schoolchildren from Cameroon 49
This study revealed that 48.8% of all those infected with
intestinal helminths were also malnourished. Helminth
infections have been reported to reduce the body’s ability
to use proteins and absorb fats, thus worsening protein–
energy malnutrition. Similar results have been reported
in previous studies (Stephenson, 1991). There was no
significant association between intestinal helminth
infection and anthropometric indices of short- and long-
term nutritional status. These results were similar for
multiple species infections and remained when control-
ling for age and sex. However, there was a statistically
significant association between the most common
parasitic infection, Ascaris, and malnutrition. There are
several possible explanations for these negative con-
sequences of helminths on nutritional status. First, it is
quite plausible that all school-aged children living in
Dibanda are faced with nearly unavoidable exposure to
the infectious stages of intestinal helminth parasites
throughout their childhood. In addition, Ascaris, the most
commonly encountered parasite in this sample, is often
associated with malnutrition. Ascaris infection can lead
to nutritional impairment and growth retardation in
children because the worm interferes with the absorption
of proteins, fats, carbohydrates, vitamin A and possibly
other nutrients. Previous research in Cameroon (Ratard
et al., 1991) found that Ascaris and other STH infections
appear to be endemic all year round, suggesting that
children would be continually infected and re-infected
throughout childhood. Maternal education has pre-
viously been found to be an important risk factor for
childhood malnutrition (Sakisaka et al., 2006). In this
study, mother ’s educational level could be an important
risk factor for children’s growth and development. Most
malnourished children (71.3%) had mothers who had not
been educated above primary school level. If mothers
have a better education and knowledge on health care,
they may better understand and implement proper health
and nutrition behaviours for their families.
In conclusion, this study established that low-burden
helminth infections and malnutrition prevail in school-
aged children in Dibanda. Mean PCV values were
lower in helminth-infected children and this difference
was significant in hookworm infection. Although this
cross-sectional study did not find any significant asso-
ciation between helminth infections and malnutrition,
suggesting that other factors important in the aetiology of
malnutrition also coexist in this locality, mean anthropo-
metric indices were, however, lower in helminth-
infected individuals. In consequence, helminth infection
is an important factor to consider in the aetiology of
malnutrition in helminth-endemic environments.
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