Open Journal of Pediatrics, 2011, 1, 12-16
doi:10.4236/ojped 2011.12004 Published Online June 2011 (http://www.SciRP.org/journal/OJPed/
OJPed
).
Published Online June 2011 in SciRes. http://www.scirp.org/journal/OJPed
Association between intestinal helminthiasis and serum
ferritin levels among school children
Olufunmilayo Vi ctoria Adebara1, Samuel Kolade Ernest2*, Isaac Ayodele Ojuawo2
1Federal Medical Centre, Iddo-Ekiti, Nigeria;
2Department of Paediatrics and Child Heath, University of Ilorin, Ilorin, Nigeria.
Received 10 April 2011; revised 24 May 2011; accepted 16 June 2011.
ABSTRACT
Background: significant iron deficiency anaemia is a
major concern in children with helminthiasis, because
it may eventually contribute to the growing health
challenges of severe anaemia. This descriptive cross
sectional study was carried out to determine the asso-
ciation between serum ferritin levels and intestinal
helminthiasis among school children. Methods: a
structured questionnaire was used to collect the study
population data. Stool specimens were obtained and
examined on the same day using the sedimentation
method for identification of the parasite. Blood sam-
ples were also obtained for full blood count and serum
ferritin measurement. Results: a total of 246 school
children were studied with a response rate of 82%.
The prevalence of intestinal helminthiasis was 29.7%.
The different helminthes identified included Ascaris
lumbricoides, Necator americanus, Trichuris trichi-
ura, Strongyloides stercoralis. Of the population
studied, 36.2% were anaemic, 15.9% had microcyto-
sis, and 47.6% had hypochromia. The prevalence of
exhausted iron stores was 3.7%. Serum ferritin levels
were significantly lower in children with intestinal
helminthiasis compared with controls. Conclusions:
The findings in this study demonstrate an inverse re-
lationship between intestinal helminthiasis and serum
ferritin levels and this is more marked in pupils with
hookworm infections. The control of intestinal hel-
minthiasis and prevention of iron deficiency anaemia
should be given high priority in the implementation of
the school health programme.
Keywords: Intestinal Helminthiasis; Serum Ferritin;
School Children
1. INTRODUCTION
Children are generally at risk of iron deficiency since the
iron requirements for growth are high and the intake of
iron is likely to be less than their requirements. Thus,
any condition that increases the need for iron, decreases
its intake or increases its loss will precipitate its defi-
ciency [1].
Several factors contribute to iron deficiency such as
insufficient dietary intake, malabsorption and infections
[2]. Helminthic infections may influence iron status by
reducing nutrient intake and by interfering directly or
indirectly with iron metabolism and transport [2]. In
school-aged children, both infections and iron deficiency
can lead to anorexia. Infections inhibit the absorption of
iron from the gastro-intestinal tract and iron deficiency
lowers resistance to infections. This process creates a
vicious circle of inadequate nutrition [2,3].
Iron deficiency is very common in Nigeria, occurring
in approximately 36% of children younger than 5 years
of age [4]. Helminthiasis is also a common problem
among Nigerian school children and has a negative im-
pact in their physical and mental development by many
mechanisms including malabsorption [6] blood and pro-
tein loss [7], anorexia, vomiting and diarrhoea. These
effects can lead to aggravation of protein energy malnu-
trition [8], anemia and other nutrient deficiencies [8] (io-
dine, vitamin A, iron deficiency) [9] which indirectly
affect cognitive development and performance. Iron defi-
ciency impairs children’s cognitive abilities, and inter-
ventions to prevent and correct iron deficiency may en-
hance children’s learning potential in school [5,6]. Im-
proving the iron status of school children will also ame-
liorate their fitness and work capacity [11], and im-
provements in girls’ iron status during the school age
may help prevent anemia during their reproductive years.
The school setting is ideal for public health interven-
tions, such as health education, iron supplementation and
treatment or prevention of parasitic infestations [12] The
aim of this study was to study the association of helmin-
thic infections and serum ferritin among school children.

O. V. Adebara et al. / Open Journal of Pediatrics 1 (2011) 12-16 13
2. MATERIALS AND METHODS
The study was a descriptive cross sectional study con-
ducted over a four month period in Ilorin metropolis, a
typical urban city in the middle belt of Nigeria. The
town has pipe-borne water that is supplied erratically on
some days of the week with augmentation from other
sources such as well, streams and bore-holes. Most of
the homes have pit latrines and water closets used by
both the adults and children [13]. There are 98 public
schools and 71 private schools within Ilorin metropolis;
a few have school clinics managed by nurses or trained
teachers that can offer first aid treatment [13].
The study population consisted of primary school
children aged between 5 and 12 years from 3 private
sand 3 public schools Children who had taken anti-
helminthic drugs within 6 months of study or those who
received a blood transfusion or iron containing medi-
cines within 3 months preceding the study or those who
were febrile were excluded.
Multistage sampling technique was employed in se-
lecting subjects for this study. Selection of schools was
done by a simple random sampling technique. Selection
of classes in each school was done by a proportionate
sampling technique. Selection of pupils was done by a:
systematic random sampling. Controls of the study were
age and sex matched children without helminthiasis.
A structured questionnaire was used to collect socio-
demographic characteristics such as age, sex, level of
education of the parents and socieconmic status. An-
thropometric measurements (i.e., weights and heights)
were performed.
Fresh stool sample was collected using precoded
specimen bottles. Samples were analyzed within an hour
of collection or preserved using 10% formol saline when
immediate analysis was not possible. However, all
analysis was done within 24 hours. Each stool sample
was microscopically examined using saline and iodine
preparations and formyl ether for the identification of the
parasite species [14,15].
Under strict aseptic conditions a 5 ml specimen of
venous blood was withdrawn. 3 ml of the blood was
decanted into a sample bottle containing ethylene dia-
mine tetra acetate (EDTA) and gently mixed to prevent
clotting while the remaining 2 ml was decanted into a
heparinized bottle which was to stand for 2 hours and the
serum was separated into another bottle and stored fro-
zen at –20˚C.
Hemoglobin concentration was determined using a
Sysmex 18 parameter autoanalyser. Anaemia was de-
fined as a hemoglobin of less than 11 g/dl and severe
anaemia was defined as an haemoglobin of less than 5
g/dl [16]. Serum ferritin concentration was analyzed by
enzyme-linked immunoadsorbent assay using the CLI-
NOTECH® human ferritin enzyme immunoassay test kit.
[17] Exhaustion of iron stores was defined as a serum
ferritin of less than 20 µg/L.
Data entry and analysis were carried out with the Epi
info version 6.0 software for epidemiology developed by
Centers for Disease Control and Prevention [18]. A
p-value of less than 0.05 was considered as significant.
3. RESULTS
A total of 300 primary school children from 6 selected
schools were recruited into the study but 246 (82%) re-
turned with suitable stool and blood specimens. The
characteristics of these children are presented in Table 1.
The overall prevalence rate of intestinal helminthic in-
fections was 29.7%. In addition, 26.5% of the males and
31.9% of females had parasitic infections (Table 1). The
mean age, weight and height according to sex are sum-
marized in Table 2.
Anaemia was recorded in 36.2% of the pupils studied.
No pupil had severe anaemia. Serum ferritin in the total
population studied was 77.6 ± 32.6 μg/L. Serum ferritin of
less than 20 µg/L (iron stores exhaustion) was observed in
3.7% of the studied population. Serum ferritin in males
was 72.0  29.9 µg/L compared to 83.2  35.4 µg/L in
females (p = 0.01). Serum ferritin, did not differ signifi-
cantly in pupils in the various age-groups (Table 3). Serum
ferritin levels were significantly lower in children with
intestinal helminthiasis compared with controls. However
there was no significant difference in total protein and se-
rum albumin levels between the groups (Table 4).
Ta bl e 1. The sex distribution of pupils according to age in the
total population studied.
Age
(years)
Total
n (%)
Male
n (%)
Female
n (%)
Odd
Ratio p
5 - 7 67 (27.2)22 (21.6) 45 (31.3) 1.65NS
8 - 10 116(47.2)49 (48.0) 67 (46.5) 0.94NS
11 - 12 63 (25.6)31 (30.4) 32 (22.2) 0.65NS
Total 246 102 (41.5) 144 (58.5) NS
Table 2. The mean age, weight and height according to sex.
Male
n = 102
Female
n = 144 T p
Age (yrs) 9.2  2.07 8.7  2.18 1.7 NS
Weight (kg) 23.4  5.7 23.2  6.4 0.3 NS
Height (cm) 121.5  11.23120.07  12.85 0.87 NS
NS: no significant
Tabl e 3. Ferritin levels amongst the different age-groups in the
population of the study.
Serum ferritin (µg/L)
Age-group (years) Mean Range
5 - 7 74.12  34.13 15 - 140
8 - 10 75.78  33.66 5 - 150
11 - 12 83.69 ±32.96 20 - 150
F = 1.02; p = NS; NS: no significant
C
opyright © 2011 SciRes. OJPed

O. V. Adebara et al. / Open Journal of Pediatrics 1 (2011) 12-16 14
Ta ble 4. Comparison of serum ferritin, serum protein and se-
rum albumin levels in the infected and non-infected groups.
N Serum Ferritin
(μg/L)
Total Protein
(g/L)
Serum albumin
(g/L)
Non-infected 173 83.6 ± 36.56 66.3 ± 0.92 35.17 ± 0.52
Infected 73 72.4 ± 25.26 65.8 ± 0.90 35.63 ± 0.52
F =5.7; p = 0.01; p = NS; p = NS; NS: no significant
Table 5. Comparison of the serum ferritin levels of the non
infected group with the levels of children with different intes-
tinal helminthes.
Serum ferritin levels
Mean  SD F p
Non-infected: 83.6  36.56
Helminth detected:
Ascaris lumbricoides 81.9  30.91 0.1 NS
Hookworm species 50.9  27.91 8.47 NS
Trichuris trichiura 66.7  14.43 0.64 NS
Polyparasites 72.5  53.03 0.35 NS
Strongyloides stercoralis 90.00 ± 0.00 2.43 0.04
NS: no significant
In Tab le 5 the results of the serum ferritin levels with
different intestinal helminthes are presented and are
compared with those of the control group. It is of interest
that 4 of 11 patients (36%) of patients with hookworm
infection had exhausted iron stores.
4. Discussion
This study showed an overall prevalence of 29.7% of the
common intestinal helminthic infections among primary
school children in Ilorin. This value is comparable to the
findings of similar studies in other parts of Nigeria
[19-22] and Africa [23]. While higher prevalence rates of
between 50% and 97% [24-30] as well as lower preva-
lence rates of less than 20% [23,31-34] have been re-
ported. These differences in the prevalence rates could
be attributable to the locations of the studies, the season
of the year the study was carried out and the method of
stool analysis. The high prevalence rate in this study
therefore confirms that intestinal helminthic infection is
a common problem in the school aged children.
In this study, the female children had a higher preva-
lence of intestinal helminthic infections prevalence than
the males. This is in consonance with studies previously
documented [34,35]. The influence of gender on preva-
lence of helminthic infection may or may not play a role
depending on the regional and environmental factors.
The overall prevalence rate of anaemia among the
school children studied was high. More than a third of
the pupils had their haemoglobin levels less than 11 g/dl.
It is noteworthy to state that no pupil had severe anaemia.
This is in consonance with previous publications [16].
The mean haemoglobin value is higher than values ob-
tained in previous studies [36-39]. Childhood anaemia
appears to be increasing in the country due to the de-
clining nutritional status secondary to a dwindling na-
tional economy.
In this study, a comparison of the haematological
status between the intestinal helminthic-infected and
non-infected children showed that the mean haemoglo-
bin indices of the latter were higher.
The iron store of the population in this study was
adequate with only 3.7% having exhausted iron stores.
This is at variance with studies done in other parts of
Africa [2,3] where the degree of exhausted iron stores
were high. This could be attributed to the low prevalence
of hookworm infection observed. The serum ferritin
level was higher in females than males. This has also
been documented in a previous study [3]. The reason for
this could be attributed to the higher number of boys
infected with hookworm species. The serum ferritin
level was higher in pupils aged 10 years and above and
lower at the age of 8 years. This is in agreement with
previously documented studies where it was attributed to
the high iron demands of early childhood [2,3].
The serum ferritin levels were lower in children with
hookworm infection. In addition, 36% of pupils with
hookworm had exhausted iron stores. No relationship
was found between Ascaris lumbricoides and iron status
in this study. This is similar to the study done in Western
Kenya but not with that done in Zanzibar, where low
serum ferritin levels were associated with Ascariasis. Iron
is absorbed through the intestinal wall in the duodenum
and jejunum and it is believed that iron absorption could
be impaired by the presence of Ascaris lumbricoides in
this part of the intestine [40]. Trichuris trichiura infection
was not related to any of the iron status indicators. This is
because Trichuris trichiura lives in the luminal epithe-
lium, mainly the large intestine, and trichuriasis has a
specific association with anaemia which is mediated
through erythrocyte loss from the gut [41].
The high prevalence of intestinal helminthic infection
and anaemia observed in this study calls for a compre-
hensive public health intervention. The most important
application of the findings is to guide the development
of appropriate interventions to minimize the predispos-
ing factors to parasitic infections and prevent iron defi-
ciency anaemia in school children. There is a strong ba-
sis for helminthics control as a strategy to control iron
deficiency in the population group. Antihelminthic drugs
are safe and cheap and periodic delivery of these drugs
through the school system is a highly feasible public
health intervention [42].
REFERENCES
[1] Schwartz, E. (2000) Iron deficiency anaemia. In: Behrman,
R.E., Kliegman, R.M. and Jenson, H.B., Eds., Nelson
C
opyright © 2011 SciRes. OJPed

O. V. Adebara et al. / Open Journal of Pediatrics 1 (2011) 12-16 15
Textbook of Paediatrics, W.B. Saunders Company,
Philadelphia, 1469-1471.
[2] Olsen, A., Magnussen, P., Ouma, J.H. and Friis, H. (1998)
The contribution of hookworm and other parasitic
infections to haemoglobin and iron status among children
and adults in western Kenya. The Transactions of the
Royal Society of Tropical Medicine and Hygiene, 92,
643-649. doi:10.1016/S0035-9203(98)90795-7
[3] Stoltzfus, R.J., Chwaya, H.M., Tielsch, J.M. and Schulze,
K.J. (1997) Epidemiology of iron deficiency anaemia in
Zanzibar schoolchildren: The importance of hookworms.
The American Journal of Clinical Nutrition, 65, 153-159.
[4] Maziya-Dixon, B., Sanusi, R.A., Akinyele, I.O. and
Oguntona, E.B. (2004) Iron status of children under 5 in
Nigeria: Results of the Nigeria food consumption and
nutrition survey. Proceedings of Iron Deficiency in Early
Life and Challenges and Progress, Lima, 18 November
2004, 43.
[5] Hendrickse, R.G. (1991) Disorders of the blood. In:
Hendrickse, R.G., Barr, D.G.D., Matthews and T.S., Eds.,
Paediatrics in the Tropics, Blackwell Scientific Pub-
lications, London, 336-372.
[6] Adedoyin, M.A., Awogun, I.A. and Juergensen, T. (1990)
Prevalence of intestinal parasitoses in relationship to
diarrhea among children in Ilorin. West African Journal
of Medicine, 9, 83-88.
[7] Montressor, A., Cromptom, D.W.T., Gyorkos, T.W. and
Savioli, L. (2002) Helminthic control in school aged
children. A guide for managers of control programme.
WHO, Geneva, 1.
[8] Ikpeme, E. and Anochie, K. (1999) Intestinal helminthic
infestations. In: Azubuike J.C. and Nkanginieme, K.E.O.
Eds., Pediatrics and Child Health in a Tropical Region,
African Educational Services, Port Harcourt, 438-444.
[9] Bundy, D.A.P., Hall, A., Adjei, S., Kihama, C. and Khoi,
H.H. (1997) Better health, nutrition and education for the
school aged child. The Transactions of the Royal Society
of Tropical Medicine and Hygiene, 91, 1-2.
doi:10.1016/S0035-9203(97)90370-9
[10] Hass, J.D. and Fairchild, M.W. (1989) Summary and
conclusions of the international conference on iron
deficiency and behavioural development. American
Journal of Clinical Nutrition, 50, 703-705.
[11] Stephenson, L.S., Latham, M.C., Adams, E.J. Kinoti, S.N.
and Pertet, A. (1993) Physical fitness, growth and appetite
of Kenyan school boys with hookworm, tricuris trichiura
and ascaris lumbricoides infections are improved four
months after a single dose of Albendazole. Journal of
Nutrition, 123, 1036-1046.
[12] Savioli, L., Bundy, D.A.P. and Tomkins, A. (1992)
Intestinal parasitic infections: A soluble public health
problem. The Transactions of the Royal Society of
Tropical Medicine and Hygiene, 86, 353-354.
doi:10.1016/0035-9203(92)90215-X
[13] Jimoh, L.A.K. (1994) Present day Ilorin. In: Ilorin: The
Journey So Far, Atoto Press Limited, Ilorin, 8-11.
[14] Cheesbrough, M. (1998) District laboratory practice in
tropical countries. Part 1. Tropical health technology.
Tropical Health Technology, Norfolk, 192-196.
[15] Markell, E.K. (1992) Examination of stool specimen. In:
Markell, E.K., Voge, M. and John, D.T. Eds, Medical
Parasitology, W.B. Saunders Company, Philadelphia,
406-428.
[16] Adewuyi, J.O. (1992) Current prevalence and some
clinical associations of childhood anaemia in urban
communities in central Nigeria. Central African Journal
of Medicine, 38, 66-72.
[17] Fairbanks, V.F. and Klee, G.G. (1999) Biochemical
aspects of haematology. In: Tietz Textbook of Clinical
Chemistry, W.B. Saunders Company, Philadelphia,
1703-1704.
[18] Dean, A.G. and Dean, J.A., Coulombier, D., et al. (1995)
Epi info version 6.0: A word processing data base and
statistics programme for public health on IBM—
Compatible micro computers. Center for Disease Control
and Prevention, Atlanta.
[19] Ighogboja, I.S. and Ikeh, E.I. (1997) Parasitic agents in
childhood diarrhea and malnutrition. West African
Journal of Medicine, 16, 21-25.
[20] Okafor, C.N. and Azubike, C.N. (1992) Studies in
intestinal parasitic disease agents in stools of people in a
rural area in Nigeria. West African Journal of Medicine,
11, 106-111.
[21] Agi, I.P. (1997) Comparative helminth infection of man
in two rural communities of the Niger delta, Nigeria.
West African Journal of Medicine, 16, 232-236.
[22] Fashuyi, S.A. (1992) The pattern of human intestinal
helminth infection in farming communities in different
parts of Ondo State, Nigeria. West African Journal of
Medicine, 16, 102-105.
[23] Curtale, F., Pezzotti, P., Saad, Y.S. and Aloi, A. (1999)
An analysis of individual, household and environmental
risk factors for intestinal helminth infection among
children in Qena Governate, Upper Egypt. Journal of
Tropical Paediatrics, 45, 14-17.
doi:10.1093/tropej/45.1.14
[24] Ibrahim, M., Odoemena, D.I. and Ibrahim, M.T. (2000)
Intestinal helminthic infections among primary school
children in Sokoto. Sahel Medical Journal, 3, 62-68.
[25] Omoigberale, A.I., Airauhi, L. and Ibadin, M.T. (1996)
Intestinal helminthiasis amongst school children in Benin
City, Nigeria. Nigerian Journal of Medicine, 30, 118-122.
[26] Meremikwu, M.M., Anita-Obong, O.E., Asindi, A.A. and
Ejezie, G.C. (1995) Nutritional status of pre-school
children: Relationship with intestinal helminthiasis.
Nigerian Journal of Medicine, 4, 40-44.
[27] Runsewe-Abiodun, T.I., Olowu, A.O., Akosode, F.A.
and Odetunde, O.S. (1995) Prevalence of helminthic
infestation in pre-school children. Nigerian Journal of
Paediatrics, 22, 81-82.
[28] Kabatereine, N.B., Tukahebwa, E.M., Brooker, S.,
Alderman, H. and Hall, A. (2001) Epidemiology of
intestinal helminth infestations among school children in
Southern Uganda. East African Medical Journal, 76,
283-286.
[29] De Carneri, I., Di Matteo, L. and Tedla, S. (1992) A
comparism of helminth infection in urban and rural areas
of Addis Ababa. The Transactions of the Royal Society of
Tropical Medicine and Hygiene, 86, 540-541.
doi:10.1016/0035-9203(92)90099-X
[30] Albonico, M., De Carneri, I., Di Matteo, L., Ghiglietti, R.,
Toscano, P., Uledi, M.K., et al. (1993) Intestinal parasitic
infections of urban and rural children on Pemba Island:
Implications for control. Annals of Tropical Medicine
C
opyright © 2011 SciRes. OJPed

O. V. Adebara et al. / Open Journal of Pediatrics 1 (2011) 12-16 16
OJPed
and Parasitology, 87, 579-583.
[31] Flores, A., Esteban, J., Angles, R. and Mas-Coma, S.
(2001) Soil transmitted helminthic infections at very high
altitude in Bolivia. The Transactions of the Royal Society
of Tropical Medicine and Hygiene, 95, 272-277.
doi:10.1016/S0035-9203(01)90232-9
[32] Gbakima, A.A., Sherpard, M. and White, P.T. (1994)
Intestinal helminth infections in rural school children in
Njala, Sierra Loene. East African Medical Journal, 71,
792-796.
[33] Phiri, K., Whitty, C.J.M., Graham, S.M. and Ssembatya-
Lule, G. (2000) Urban/rural differences in prevalence
and risk factors for intestinal helminth infections in
Southern Malawi. Annals of Tropical Medicine and
Parasitology, 94, 381-387.
[34] Musa, O.I. (1997) Intestinal Helminthiasis among students
seen during school entrance medical examination in Ilorin.
Journal of Community Medicine and Primary Health, 9,
35-41.
[35] Elekwa, D.E. and Ikeh, E.I. (1996) A survey of the
incidence of intestinal parasites amongst primary school
children in relation to socio-economic factors in Jos,
Nigeria. Nigerian Medical Practice, 31, 60-62.
[36] Azubike, J.C., Izuora, G.I. and Obi, G.O. (1977) Anaemia
in nonsickling children around Enugu. Tropical and
Geograogical Medicine, 29, 365-268.
[37] Fleming, A.F. and Werbinska, B. (1982) Anaemia in
childhood in the guinea savanna of Nigeria. Annals of
Tropical Paediatrics, 2, 161-173.
[38] Akenzua, G.I., Ihongbe, J.C., Imasuen, V.I. and Mwobi,
B.C. (1985) Anaemia on children: A survey in Obadan, a
rural community in the rain forest zone of Nigeria.
Journal of Tropical Paediatrics, 31, 20-24.
[39] Akinkugbe, F.M. (1977) Prevalence of anaemia in an
urban population (University College Hospital GOPD).
Journal of Tropical Paediatrics and Environmental Child
Health, 23, 271-275.
[40] Islek, I., Kucukoduk, S., Cetinkaya, F. and Gurses, N.
(1983) Effects of Ascaris infection on iron absorption in
children. Annals of Tropical Medicine and Parasitology,
87, 477-481.
[41] Bundy, D.A.P. and Cooper, E.S. (1989) Trichuris and
trichuriasis in humans. Advances in Parasitology, 28,
107-173. doi:10.1016/S0065-308X(08)60332-2
[42] Warren, K.S., Bundy, D.A.P. and Anderson, R.M. (1993)
Helminth infection. In: Jamison, D.T., Mosley, W.H.,
Measham, A.R. and Bobadilla, J.L., Eds., Disease
Control Priorities in Developing Countries, New York
University Press, New York, 131-160.