Nigerian Journal of Paediatrics 2012;39(1): 7 - 13
ORIGINAL
Nwaneri DU
Prevalence of intestinal helminthiasis in
Sadoh AE
children with chronic neurological
Ofovwe G.E
Ibadin MO
disorders in Benin city, Nigeria
DOI: http://dx.doi.org/10.4314/njp.v39i1.2
Received: 4thApril 2011
Abstract Background:
It is
intestinal helminthiasis in children
Accepted: 23rd October 2011
envisaged that the care for the child
with CND was 31.0% compared
with chronic neurological disorder
with 19.4% found among the
Nwaneri DU ( )
(CND) compared with his
apparently healthy controls (p =
Ofovwe GE,Ibadin MO
apparently healthy counter-part
0.03). This prevalence increased
Department of Child Health,
may be sub-optimal, predisposing
with increasing age in both subjects
University of Benin Teaching
him to increase disease morbidities
and comparative group. Intensity of
Hospital,
including intestinal helminthiasis.
infections in both groups was light.
PMB 1111, Benin City, Edo
To evaluate this hypothesis, a
Ascaris
lumbricoides , Trichuris
State, Nigeria.
comparative cross sectional study
t r i c h i u r a
and A n c y l o s t o m a
E-mail: damiannwaneri@yahoo.com
was carried out to determine the
duedenale
were the intestinal
Tel: +234
prevalence, intensity, and specie-
helminths isolated in both subjects
SadohAE
specific prevalence of intestinal
and control groups. A. lumbricoides
Institute of Child Health,
helminthiasis in children with
alone had the highest specie-
University of Benin,
CND such as cerebral palsy,
specific prevalence in both the
Benin City Nigeria.
epilepsy, and mental retardation
subjects (20.0%) and comparative
seen at the University of Benin
groups (15.5%). Mixed infection
Teaching Hospital, Benin City
was found only among the children
between November 2008 andApril
with CND.
2009.
C o n c l u s i o n :
I n t e s t i n a l
Subjects and Methods : Fresh stool
helminthiasis is common and more
samples from 155 children with
prevalent in children with CND
CND and from 155 age
and sex
than in healthy children. It is
matched apparently healthy
recommended that regular de-
nursery and primary school
worming be incorporated into the
children in Benin City, Edo State
routine care of children with CND.
were analysed using the Kato-Katz
technique for the detection of ova
Key words: chronic neurological
of helminths.
disorders, helminthiasis, intestinal
Results: The prevalence of
helminths, intensity
Introduction
Worldwide prevalence of intestinal helminthiasis
among school children varies from 8.9% to 89.0%.
3
Intestinal helminths are groups of parasites which
live and feed on living hosts, receiving nourishment
In Nigeria, the prevalence ranges from 14.4% to
and protection while disrupting the hosts' nutrient
71.1%, depending on location and methodology
absorption, causing weakness and diseases. It is
1
employed in the study.
4-7
estimated that more than one billion people in the
world are infected with one or more of these
Major risk factors for high levels of intestinal
parasites with pre-school and school aged children
helminthiasis still remain poverty, poor
often presenting with heavy worm infection.
2-4
environmental sanitation, personal hygiene,
8
lack of potable drinking water, inadequate health
obtained from the Ethics and Research Committee of
care, over-crowding and poor health education
UBTH, Benin City.
which characterise most communities in developing
countries including Nigeria.
3-7
For the purpose of this study, CND included cerebral
palsy (CP), epilepsy and mental retardation (MR).
8
Children with chronic neurological disorders (CND)
The diagnostic criteria for the CND was based on the
have been found to have sub-optimal care when
Diagnostic Statistical Manual (DSM) IV (American
compared with the apparently healthy children
PsychiatricAssociation, 1994).
16
perhaps due to stress of taking care of them and
socio-economic implications on the care-givers.
8,9
Children who had been known to have taken
Coupled with already outlined risk factors, these
anthelminthic drug(s) in the preceeding 3 months
children may be predisposed to increased intestinal
were excluded. Children who were younger than two
helminthic infections and may stand a greater risk of
years old were also excluded. This was because the
impaired physical and intellectual development from
diagnostic tool and criteria for diagnosis of CND
both their underlying disorders and from heavy
studied were not applicable to children less than two
helminthic infections.
10,11
years.
16,17
Available published data show varying ranges of
Fresh stool sample, collected in the mornings from
prevalence of intestinal helminthiasis in children
subjects and controls were examined the same day
with CND.
12-15
A prevalence of 88.0% was observed
with the Kato-Katz method in Research Laboratory,
18
among children aged 3-14 years with CND (CP, MR,
Department of Child Health, University of Benin
and epilepsy) in Mississippi, USA,
12
while a
Teaching Hospital, Benin City. Stool samples passed
prevalence of 76.6% was recorded in a 1998 study of
over night were stored in a temperature of 4 C (which
o
parasitic infections among adolescents with MR, in
is the temperature of conventional refrigerator) up to
Egypt. These data did not compare the prevalence
14
the morning and it was then analysed. Such stool
18
of intestinal helminthiasis with those obtained from
sample can be analysed at least 24 hours after the stool
sample was collected.
18,19
apparently healthy children. Thus it is not clear
In order to ensure proper
whether or not there is a higher prevalence of
identification of hookworm ova, the preparation of
intestinal helminthiasis in children with CND when
each stool slide was read not later than 4-6 hours after
taking the samples.
19,20
compared with apparently healthy children within
All stool slides were prepared
the same locality.
and read by the researchers assisted by medical
microbiologist specialised in parasitology.
A large number of children suffer from CND.
8,9
If
Consistency of the readings was assured by second
indeed these children are at increased risk of
readings performed in 20.0% of the slides randomly
intestinal helminths not only are they at risk for more
selected. Another reading was done after 24 hours for
search for ova of Schistosoma mansoni .
19,20
morbidity from the helminths, but they also serve as
Intensity
sources for dissemination of helminths to members
of infections for each worm was defined according to
of their communities. This study therefore sets out to
the thresholds proposed by the WHO Expert
Committee in 1987.
19
evaluate the prevalence, specie-specific prevalence
and intensity of intestinal helminthiasis in children
with CND compared with apparently healthy age and
Data analysis
sex matched control group.
The data obtained was entered into a spread sheet
using the Microsoft Excel 2007 and the analysis was
done using the Statistical Package for Social Sciences
(SPSS) version 13.0 (SPSS Inc Chicago, Illinois,
Subjects and Methods
USA). The overall prevalence, specie-specific
prevalence, and intensity of intestinal helminths in
This was a comparative cross-sectional study.
both the subjects and the control group were
Children aged 2-17 years with CND on follow-up in
calculated and comparison made. Social class of both
the child neurology clinic, University of Benin
subjects and comparative group was done as
documented by Oyedeji.
21
Teaching Hospital (UBTH), Benin City were
Quantitative variables
recruited consecutively. Age and sex matched
were summarized using means and standard
apparently healthy children (control group) were
deviations. Frequency tables, graphs and charts were
recruited from registered public nursery and primary
constructed as appropriate. The significance of
schools in Benin City using multistage sampling
association between variables was tested using chi-
technique.
square and Fisher's exact tests where appropriate for
comparison of proportions while student t-test was
The study was carried out between 1 November
st
used for comparison of means. The level of
2008 and 30 April 2009. Ethical approval was
th
significance of each test was set at p < 0.05.
9
Results
The prevalence of intestinal helminthiasis in children
with CND (31.0%) was significantly higher than the
19.4% observed in control group ( χ = 4.95, p = 0.03,
2
There were 155 subjects and 155 age/sex matched
control group whose stool samples were suitable for
95%C.I = 1.07-1.67). Among the 90 children with
analysis. These consisted of 93(60.0%) males and
CP, 29(32.2%) had intestinal helminthiasis,
62(40.0%) females; mean age 5.6 years ± 3.8 years.
11(20.8%) of the 53 with epilepsy and 8(66.7%) of
Of the 155 subjects, 90(58.1%) had CP, 53(34.2%)
the 12 with MR had intestinal helminthiasis
had epilepsy and 12(7.7%) had MR. One hundred
respectively. There was a significant difference in
and three (66.5%) of the subjects belonged to the
prevalence of intestinal helminthiasis and type of
upper social class and 52(33.5%), lower social class.
CND ( χ = 9.81, df = 2, p = 0.01).
2
T here was no statistical significant difference in the
social class status of subjects and the apparently
Thirty (32.3%) of the 93 male and 18(29.0%) of the
healthy group (χ = 0.00, p = 1.00, 95%C.I = 0.62-
2
62 female subjects had intestinal helminthiasis while
1.60, OR = 1.00). Table 1 shows the socio-
the corresponding values for the control group were
demographic characteristics of the subjects and the
20(21.5%) for males and 10(16.1%) for females.
control group in relation to gender.
Gender was not significantly associated with
intestinal helminthiasis in both subjects and control
Table
1:
Socio-demographic characteristics of
group (subjects: χ = 0.06, p = 0.80; control group: χ
2
2
subjects and controls
= 0.39, p = 0.53).
Socio-demographic
Subjects
Controls
characteristics
Male
Female
Male Female
The mean age of 5.9 ± 3.7 years in the infected CND
n(%)
n(%)
n(%)
n(%)
group was significantly lower than the 8.6 ± 4.7 years
in the control group (t = 2.70, p = 0.009). Among the
Age Group (Years)
age group (2-5 years), the subjects had significantly
2-5
59(63.4) 39(62.9) 59(63.4) 39(62.9)
more intestinal helminthiasis when compared with
the controls ( χ = 6.53, p = 0.01). The peak age group
2
6-9
13(14.0) 12(19.4) 13(14.0) 12(19.4)
10-13
14(15.1)
9(14.5)
14(15.1) 9(14.5)
specific prevalence in infected subjects was 6-9
14-17
7(7.5)
2(3.2)
7(7.5)
2(3.2)
years, 11/25(44.0%); and thereafter a decline in
Total
93(100.0) 62(100.0) 93(100.0) 62(100.0)
prevalence was observed with increasing age. In
infected controls, there was increase in prevalence
Social class
with increasing age (Table3).
Upper
61(65.6) 42(67.7) 59(63.4) 44(71.0)
Lower
32(34.4)
20(32.3) 34(36.6) 18(29.0)
Table 3: Age-specific prevalence of infected and
Total
93(100.0) 62(100.0) 93(100.0) 62(100.0)
non-infected subjects and control group
χ =0.01, p = 0.92, OR= 0.9
2
χ = 0.64, p = 0.42, OR = 0.7
2
Subjects
Control group
Age(Years) Infected Not infected Infected Not infected
Table
2:
shows the socio-demographic
χ
2
(%)
(%)
(%)
(%)
p – value 95%C.I
characteristics of the different types of CND. Half of
2-5(n=98) 26(26.5) 72(73.5) 11(11.2) 87(88.8) 6.53 0.01
1.32 – 6.18
the children with MR belonged to the lower social
6-9(n=25) 11(44.0) 14(56.0) 5(20.0) 20(80.0) 2.30 0.12
0.89 – 11.07
class. All subjects and the control group were living
10-13(n=23) 9(39.1) 14(60.9) 7(30.4) 16(69.6) 1.47 0.76
0.43 – 4.98
with their parents or care-giver.
14-17(n=9) 2(22.2)
7(77.8) 7(77.8)
2(22.2)
*
0.06
0.09 – 0.75
Total (n=155)48(31.0) 107(69.0) 30(19.4) 125(80.6)
Socio-demographic Cerebral palsy
Epilepsy
Mental
Retardation
*Fisher's exact test, C.I = Confidence interval
features
n= 90 (%)
n = 53(%) n= 12 (%)
Intestinal helminthiasis was significantly higher
Gender
among the children from the lower social class and
Male
48(53.3)
38(71.7)
7(58.3)
these children were three times more likely to acquire
Female
42(46.7)
15(28.3)
5(41.7)
intestinal helminthic infection compared to the
Age (years)
children from the upper class in both subjects and
2-5
73(81.1)
25(47.2)
0(0.0)
control group. ( χ = 6.39, p = 0.01, 95CI = 1.38-8.04,
2
6-9
11(12.2)
10(18.9)
4(33.3)
10-13
5(5.6)
12(22.6)
6(50.0)
O.R = 3.3) (Table 4).
14-17
1(1.1)
6(11.3)
2(16.7)
Social class
Upper
64(71.1)
33(62.3)
6(50.0)
Lower
26(28.9)
20(37.7)
6(50.0)
10
Table 4: Social class of infected and non-infected subjects and control group
Subjects
Control group
Social class Infected
Not infected
Infected Not infected
(%)
(%)
χ
2
(%)
(%)
p – value 95%C.I
O.R
Upper (n = 103) 25(24.3)
78(75.7)
20(19.4)
83(80.6) 0.45
0.50
0.68 – 2.59 1.3
Lower (n = 52)
23(44.2)
29(55.8)
10(19.2) 42(80.8)
6.39
0.01
1.38 – 8.04 3.3
Total (n = 155)
48(31.0) 107(69.0)
30(19.4) 125(80.6)
A lumbricoides , T. trichiura , and Ancylstoma
wears regularly. The corresponding values for
duodenale were the intestinal helminths isolated
epilepsy and MR were 5/11(45.5%) and 3/8(37.5%)
from both the subjects and control group in this
respectively. All 12 subjects (8 with CP, 2 with
study. Although the species-specific prevalence
epilepsy and 2 with MR) and all three controls that
seemed higher for all 3 helminths among the subject s
had A. duodenale infections; did not use footwear
compared to the control group but the differences
regularly. There was statistically significant
were not statistically significant ( χ = 0.80, p = 0.37).
2
association between A. duodenale infection and use
A. lumbricoides alone had the highest specie-specific
of footwear in subjects (p < 0.001 Fisher's Exact) as
prevalence of 31/155 (20.0%) among the subjects
well as in controls (p = 0.04 Fisher's Exact). All
and 24/155(15.5%) among control group, T.
children with CP and who had mixed infections did
trichiura
and
A.
duodenale
were observed in
not use footwear regularly.
12/155(7.7%) subjects respectively while among the
control groups; the prevalence was 3/155(1.9%) for
Table 6: Use of footwear among the different types
both helminths respectively.
of chronic neurologic disorders
Regular use Cerebral palsy
Epilepsy
Mental
Table 5: showed species of intestinal helminths and
retardation Total
different types of CND studied. There was no
Of footwear
(%)
(%)
(%)
(%)
significant association between types of CND and
species of intestinal helminths in subjects ( χ = 8.13,
2
Yes
39(43.3)
36(67.9)
7(58.3)
82(52.9)
df = 6, p = 0.23). Mixed infections was observed in
No
51(56.7)
17(32.1)
5(41.7)
73(47.1)
7/155(4.5%) of subjects and were among children
Total
90(100.0)
53(100.0) 12(100.0)
155(100.0)
χ = 8.25, df = 2, p = 0.016
2
with CP. The different combination of mixed
infection were A. lumbricoides and A. duodenale
4/7(57.1%),
A.
lumbricoides
and
T.
trichiura
2(28.6%) and T. trichiura and A. duodenale 1
(14.3%). Mixed infection was not observed among
Discussion
the control group.
This study revealed a significantly higher prevalence
The intensity of infection was light for all species
(31.0 %) of intestinal helminthiasis in children with
of intestinal helminths in both subjects and control
CND (CP, epilepsy, and MR) compared to 19.4% in
group.
age and sex matched apparently healthy control
group. The prevalence is comparable to finding by
Lohiya et al
13
Table 5: Species of intestinal helminths and types
who observed a prevalence of 31.0%
of CNDs
(for Enterobius vemicularis only) in a long term care
Specie of
Cerebral palsy Epilepsy
Mental
facility for a population of 997 consisting of both
Retardation
adults and children with epilepsy, cerebral palsy,
Intestinal helminths
n = 29 (%)
n = 11 (%)
n = 8 (%)
mental retardation, and autism in New York. This
prevalence is however lower than the 88.0% found
Ascaris lumbricoides
15(51.7)
7(63.6)
3(37.5)
among children aged 3-11 years with CND in a
3(37.5) developmental centre in Mississippi, USA.
12
Trichuris trichiura
4(13.9)
2(18.2)
All
Ancylostoma duodenale
3(10.3)
2(18.2)
2(25.0)
subjects in these studies were institutionalised. The
Mixed infections
7(24.1)
0(0.0)
0(0.0)
lower prevalence in this study may be because all the
studied children lived with their parents/care-giver
Table 6: shows use of footwear among the different
who may
have provided them with better care.
types of CND. Children with CP significantly did not
Reasons proffered for the high prevalence rates in the
use footwear regularly when compared with the
two studies in USA were poor housekeeping, poor
other forms of CND (ep ilepsy and MR) (χ = 8.25, df
2
general hygiene, poor toilet facilities, inaccessibility
= 2, p = 0.016). Of the 29 children with CP who had
to adequate potable water supply as well as length of
intestinal helminthiasis, 21(72.4%) did not use foot-
year of stay within the institution.
11
These factors havebeen documented as major risk
These species were comparable with those observed
by some authors in children with CND.
12,13
factors to intestinal helminthiasis and characterise
Ekundayo
most communities with low socioeconomic status.
10
et al (2007) as in this study showed that in over a 30
4
It was also observed from this study that most
year period that the triad of A . lumbricoides , T .
infected subjects were from low social class. In fact
trichiura and A. duodenale species were the common
children from low social class were three times more
intestinal helminths isolated among pre-school and
likely to be infected compared to their counter-part
school aged children in Nigeria. This indicates that
from upper social class. This finding was in
these are predominant helminths in the environment
consonance with previous findings that lower social
to which both children with CND and their apparently
economic class is a major contributor to intestinal
healthy counter-parts are exposed. The prominence of
helminthiasis.
3-7
A . lumbricoides over the other helminths in this study
may be due to embryonated eggs, having enormous
Intestinal helminthiasis was more in children with
capacity to withstand extremes of environmental
temperatures.
2,10
MR compared to those with epilepsy and CP.
Thus within the context of the
weather during which the study was carried out
Although, the number of children with MR was
(November to April), thriving of the ova of A .
small, this finding still may suggest that children
lumbricoide
could be said to be enhanced in
with MR were at higher risk of acquiring intestinal
comparison with those of T . trichiura
and A.
helminthiasis compared with other types of CND
duodenale .
(epilepsy and CP). This is corroborated by other
authors who have also found higher prevalences of
Presence of A. duodenale infection is seen as an index
intestinal helminthiasis in this group.
13,14,22
This
of environmental contamination with human waste.
10
higher prevalence could be attributed to underlying
These helminths constitute more of the mixed
impaired neurological dysfunction which is usually
infection observed in this study and were seen only in
more profound in children with MR when compared
children with CP. Use of footwear especially while
with those with CP and epilepsy. This profound
11
going to farm, schools or at play grounds have been
neurological dysfunction may translate to poor level
known to be protective against hookworm
of care and possible neglect of these children,
8,9,13-15
infections.
5,10
Mixed infections and A. duodenale
hence may put them at higher risk of acquiring
infection occurred significantly more in subjects, as
intestinal helminthiasis when compared with other
against the apparently healthy comparative group. It
CNDs (CP and epilepsy).
12-15
The lower intelligence
was observed in this study that children with CP
in this group may also be annotated with poorer peri-
significantly did not use footwear regularly when
anal hygiene at an age when they are expected to take
compared with children with epilepsy and MR. Some
care of themselves.
children with CP may not have used footwear and so
many others may have been crawling on the ground
The prevalence figure (19.4%) observed in
due to the associated disorder of posture and
movement.
8,9
apparently healthy control group in this study is
comparable with previously documented findings in
Nigeria.
4-7,23
The present study as in others,
4-7,23
An ambulatory child who does not use footwear
demonstrated no significant gender difference in
regularly at school or at play ground, or a non-
intestinal helminthic infection in subjects as well as
ambulatory child who crawls regularly on the ground
in control group..The study also demonstrated
is at risk of penetration of hookworm larvae through
the skin.
10
increase in prevalence of intestinal helmitnhiasis
And judging by the fact that A.
with increasing in age in both the children with CND
lumbricoides
and A.
duodenale
were the most
and in apparently healthy children as has been
prevalent species of helminths in the mixed infection,
observed by most authors.
3-7,12,13
This could be
it could be postulated that poor care (for non-
attributed to sheer stress encountered in care for
ambulatory children who sit or crawls on the ground
children with CND. Generally, personal care for
regularly) as well as lack of regular use of foot-wear
children tend to decrease with increase in age as
for ambulatory children could have contributed to the
mothers/caregivers pay more attention to the
mixed infections found among the children with CP.
younger children. The stress of caring for children
8,9
with CND as they grow older is enormous. Coupled
8,9
The intensity of infection in both the CND and
with already compromised neurological status, these
apparently healthy group was light, perhaps
children may be predispose to increased intestinal
underscoring the fact that both groups irrespective of
helminthic infections with increase in age.
primary health conditions are exposed to the same
environment and therefore the same range of
The species of intestinal helminths isolated in both
helminthes. Though one would have expected heavy
subjects and control group in this study included A .
intensity of intestinal helminthiasis in children with
lumbricoides,T. trichiura andA. duodenale.
CND, the possible explanation for light intensity
12
among such children and against expectations could
made available for children with CP to reduce the risk
be attributed to exposure to regular health care
of hook worm infection.
services compared to previous documentations.
8
This study was hospital based, and majority of the
subjects were on regular follow-up in child
neurology clinic. During such regular follow-up
visits, the subjects and their mothers/caregivers
Acknowledgment
could have benefitted from health education which
constituted part of such routine clinic visits.
The authors wish to thank the interns in child
neurology unit who participated in sample
With one in every three children with CND having
collections. Special thanks to Mr. Oladipo and
intestinal helminthiasis, it is recommended that
Fatima, the laboratory scientists in Department of
regular de-worming exercise be incorporated into the
Child Health Research Laboratory, University of
routine care of children with CND. Special
Benin Teaching Hospital, Benin City for their
protective footwear and special carrier cot could be
assistance in stool analysis for ova.
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