Nigerian Journal of Paediatrics

Prevalence and pattern of intestinal parasites among pupils of private and public primary schools in an urban centre Nigeria

Niger J Paediatr 2017; 44 (2): 56 – 62

ORIGINAL

Ajayi EO

Prevalence and pattern of intes-

Elechi HA

tinal parasites among pupils of

Alhaji MA

Adeniyi OF

private and public primary

schools in an urban centre,

Nigeria

DOI:http://dx.doi.org/10.4314/njp.v44i2.3

Accepted: 10th March 2017

Abstract : Background : Intestinal

vate schools respectively. The pu-

parasitic infection is highly preva-

pils from the public schools were

Elechi HA (

)

lent among children in the tropics.

17.23 times more likely to have

Alhaji MA

Identifying the most at risk group

intestinal parasitic infestation com-

Department of Paediatrics,

and subsequent targeted interven-

pared to those from private schools

University of Maiduguri,

tion will lead to cost effective and

(OR =17.23, 95% CI = 10.6-28.01,

Maiduguri, Nigeria.

easy to implement control pro-

p = <0.0001). Ascaris lumbri-

Email: h2elechi@gmail.com

gramme. We thus aim to deter-

coides was the most frequent iso-

mine the prevalence and pattern

late in both the public (62.8%) and

Ajayi EO

of intestinal parasite among pupils

private (66.7%) schools. The

Adeniyi OF

from public and private schools.

prevalence of multiple parasitic

Department of Paediatrics,

Material and Method : This was a

infestation was 14.8% in the public

Lagos University Teaching

cross-sectional survey. Partici-

schools and none in the private

Hospital, Lagos, Nigeria.

pants were recruited through mul-

schools. Socioeconomic status and

tistage stratified random sam-

source of water were the main fac-

pling. Information were collected

tors with significant effect on the

using a questionnaire and early

prevalence of intestinal parasite

morning freshly passed stool sam-

(p<0.0001).

ple was collected and processed

Conclusion : Intestinal parasitic

from each participating pupil.

infestation remains a very common

Stool microscopy was done using

health issue among the children

saline and iodine preparations.

particularly in the public schools.

Eggs were counted using Stoll’s

Distribution of free antiparasitic

method. Data obtained was ana-

drugs to pupils at the beginning of

lyzed using EPI INFO version

every term should be incorporated

3.5.1.

into the school health program.

Results : Four hundred and twenty

pupils were studied, 210 pupils

Key words: Intestinal Parasites,

from each school type.

Preva-

Ascaris

lumbricoides,

public

lence of 78.1% and 17.1% were

school, private school, socioeco-

recorded for the public and pri-

nomic status.

Introduction

The prevalence and intensity have been found to be

highest in communities in which poverty, poor environ-

mental and personal hygiene are endemic. In such com-

Intestinal parasitic infestations are highly prevalent in

developing countries, particularly in the tropics, and

munities, faecal disposal is indiscriminate, resulting in

contamination of the soil, water, food and vegetables

5,6

pose serious medical and public health problems. The

World Health Organization (WHO) estimates that over

and the prevalent habit of walking bare footed and eat-

two billion people are infected with one or more types of

ing unwashed fruits further enhance high transmission

rates. The frequency of intestinal parasitisation can be

soil-transmitted intestinal parasites. Infection in man is

by parasites belonging to either the nematodes (round

regarded as a general indicator of the level of develop-

worm) or platyhelminthes (flat worm) phylum. The

ment, as high prevalence rates are almost invariably

associated with poor living conditions.

basis of aggregation of soil-transmitted parasites in

population is unknown. It may be related to the hetero-

geneity of the parasites, differences in susceptibility of

Children are particularly vulnerable to intestinal helmin-

human population, social behavioral or nutritional fac-

thic infections, which may affect their mental and physi-

tors.

cal developments through several mechanisms including

malabsorption, blood and protein loss, anorexia and

The values for P1 and P2 (20.9% & 53.5%) were taken

from a previous study. The calculated minimum sam-

chronic dyspeptic syndromes, all of which compromise

nutrition in these children.

ple size was 41 from each study group. However, two

hundred and ten (210) pupils were studied from each

Several studies in Nigeria have shown that the preva-

type of school to increase the power of the observation

lence of intestinal parasitic infestation is high, especially

as resources allowed.

among children: Saka et al reported a prevalence of

47.4% among primary school pupils from Ilorin, North-

Sampling method

central Nigeria, Salawu et al , on the other hand, found a

higher prevalence of 59.2% among pupils from Ife,

Multistage stratified random sampling was used. There

Southwest Nigeria, while Odinaka et al

reported a

were 114 registered private primary schools and 32 pub-

prevalence of 30.3% from Imo State, Southeast Nigeria.

lic primary schools in Ikeja Local Government Area as

Low socioeconomic status was a common factor found

at the time of the study. The schools were stratified into

among these children with helminthic infestation in the

private and public schools. Two schools were selected

various studies.

8-10

This reported high prevalence under-

by simple random sampling from the list of public

scores the need for appropriate public health interven-

schools and three from the list of private schools. Sev-

tion aimed at controlling the infestation in children. In

enty and 105 pupils were studied from each of the par-

Nigeria, particularly in the urban centres like Lagos,

ticipating private and public schools respectively. In

dichotomisation of school system into private and public

each participating school the total number was propor-

schools naturally selects the children along socioeco-

tionally distributed across all levels based on the number

nomic lines, with the low socioeconomic ones concen-

of pupil in each level. Participants were selected by

trated in the public schools. This may provide a good

simple random sampling method using the class register

opportunity in reaching the most vulnerable population

as a template in each of the classes of the selected

with any interventional programme. We thus undertook

schools.

a survey to determine the prevalence and pattern of para-

sitic infestation among pupils in private and public

Ethical consideration

school in Ikeja- Lagos which is an urban centre in Nige-

ria.

Written permission was sought and obtained from the

Ikeja LGA Education Authority. The head teachers of

the selected schools also gave well-informed expressive

approval after receiving appropriate information. All the

Materials and Method

selected pupils were given consent form and introduc-

Study area

tory note to the study to their parents for their signature

or thumbprint. There was no consequence for the pupil

The study was carried out in public and private primary

if he or she refused to participate or parents refused con-

schools in Ikeja Local Government Area (LGA) of La-

sent. Data obtained were treated with confidentiality and

gos State, Nigeria. Ikeja is the capital city of Lagos state,

only for the purpose of this research. All children whose

the most populated and urbanized state in Nigeria with

stool sample tested positive were given appropriate pre-

over 10 million residents. There are 114 registered

scription.

private primary schools and 32 public primary schools

in Ikeja LGA as of the time of the survey.

Data collection method

Study design

Information for the study was obtained via an author

This was a cross-sectional survey.

administered structured questionnaire. All the participat-

ing pupils were interviewed at school and sent home

Study population

with the section of the questionnaire to be completed by

They consisted of pupils in public and private primary

their parents and were returned the following day. Infor-

schools in Ikeja LGA.

mation obtained included sociodemographic data such

as age, gender, parents’ occupation, average monthly

Sample size determination

income, and educational attainment. Information on type

Minimum sample size for each type of school was deter-

of housing, mode of sewage and refuse disposal and

mined using the formula:

source of water were sought as indicators of sanitary

condition of the family. Socioeconomic status was as-

sessed using the model of Ogunlesi et al. Weight was

measured in kilogram to one decimal place using a bath-

room weighing scale with sensitivity of 0.5 kg. Height

Where N = Minimum sample size

was measured in meters to two decimal places using a

Za = Standard deviate (1.96)

stadiometer. Nutritional status was determined using

Zb = Critical value depending on power usually

body mass index (BMI) percentile in accordance with

1.28 at 90% power.

the National Centre for Health Statistics/Center for Dis-

P1 &P2 = Proportion of pupils estimated to be

ease Control and Prevention.

Children with BMI be-

infected in each group

low the 5 percentile were classified as underweight, 5

q = 1-p

to less than 85 percentile as normal, 85 to less 95

Looking at the sanitary indicators of the household of

percentile as overweight and 95 and above as obesity.

the pupils, more than half, 121 (57.6%) of those from

public schools lived in a single room apartments – toilet

The children were given specimen bottles to collect

detached and shared with several other households - as

fresh stool with the help of their parents and bring the

compared to 207 (98.6%) from the private schools who

same to school the same morning. The samples were

lived in block of flats or bungalow. There was statisti-

received and transported in ice pack to the laboratory

cally significant difference between the housing type of

where it was subsequently store in a refrigerator at -4 C

the pupils from the two groups (p < 0.0001). Mode of

until analysis. Stool examination was done by an experi-

sewage and refuse disposal was similar among the two

enced Laboratory scientist in the parasitology laboratory

groups: Majority of the pupils 195(92.9%) and 208

of Lagos University Teaching Hospital within four

(99.0%) from public and private school respectively,

hours of sample collection. Saline preparations were

used water closet as mode of sewage disposal (P =

used to detect vegetative forms, eggs and larval, while

0.0743), while 168 (80%) and 160 (76.2%) from public

iodine preparations detected cyst. Eggs were counted

and private schools used refuse trucks (P=0.3710). In

using Stoll’s method. Identification of any of egg, larva,

contrast however, source of drinking water differed sig-

cysts and active forms on microscope were considered

nificantly between the two groups (P=0.0005) table 2.

positive.

Table 2: Sanitary indicators of the respondent’s family

Sanitary Indica-

Public

Private

Data analysis

P-value

tors

Schools

The data obtained were entered and analysed using EPI

n (%)

INFO version 3.5.1 (developed by Centres for Disease

Type of house

Control and Prevention (CDC), Atlanta, Georgia

Single room

121 (57.6)

3 (1.4)

174.0

<0.0001

Block of flats

85 (40.4)

140 (66.7)

(USA)). Tables were used in data presentation. Chi-

Bungalow/

4 (2.0)

67 (31.9)

square and Fisher’s exact test were used in comparing

Duplex

frequencies

Type of toilet

Open defecation

4 (1.9)

1 (0.5)

3.186

0.0743

Pit latrine

8 (3.8)

1 (0.5)

Results

Water closet

195 (92.9)

208 (99.0)

Others

3 (1.4)

0 (0.0)

A total of 420 children were studied, 210 pupils from

Refuse disposal

each school type. The children from the private schools

Burning/

32 (3.3)

12 (1.9)

0.8002

0.3710

were younger with a mean age of 7.7 ± 1.9 years com-

dumping

Cart pushers

10 (4.8)

38 (18.1)

pared to 10.3 ± 2.6 years for those in public school (P ≤

Refuse trucks

168 (80.0)

160 (76.2)

0.001). The female pupils (113 & 111 in public and pri-

Source of drinking water

vate schools respectively) were slightly more than the

Bore hole

56 (26.7)

153 (72.9)

12.10

0.0005

male (97 & 99 in public and private schools respec-

Pipe borne wa-

138 (65.7)

25 (11.9)

tively) with M: F ratio ≈ 1:1.1 in both groups. Majority

ter

176 (83.3%) of the pupils from the private schools were

Well water

3 (1.4)

of high socioeconomic class whereas those from public

Others

13 (6.2)

29 (13.8)

schools were predominantly of the middle socioeco-

nomic class (P ≤ 0.001). Table 1 shows the sociodemo-

*, Chi-square test for trend

graphic features of the study population.

A total of 123 (58.6%) pupils from the public schools

Table 1: Sociodemographic features of the study population

were dewormed at least once in a year which is not sig-

Variable

Public

Private

P-value

nificantly different from 119 (56.7%) pupils from pri-

School

vate school (P=0.6929). Further categorization of the

n (%)

deworming practice into three monthly, six monthly and

Age

yearly also showed no statistically significant difference

5 – 6

14 (6.7)

63 (30.0)

97.81

<0.0001*

between the two groups (p – 0.5565).

7 – 8

46 (21.9)

59 (28.1)

9 – 10

50 (23.8)

81 (38.6)

Table 3: Use of anthelminthic among the respondents

11 – 12

59 (28.1)

7 (3.3)

De-worming

Public

Private

>13

41 (19.5)

0 (0)

Frequency

School

Sex

n (%)

Male

97 (46.2)

99 (47.1)

0.0382

0.844

Female

113 (53.8)

111 (52.9)

Every 3 months

72 (34.3)

62 (29.5)

0.3459

0.5565

Socioeconomic status

Every 6 months

25 (11.9)

32 (15.2)

Low

49 (23.3)

6 (2.9)

233.7

<0.0001*

Once in a year

24 (11.4)

23 (11.0)

Middle

157 (74.8)

28 (13.3)

Others

2 (1.0)

High

4 (1.9)

176 (83.8)

Total

123 (58.6)

119 (56.7)

*, Chi-square test for trend

*, Chi-square for trend

Underweight was three times more frequent in the pub-

proportion (14.4%) was among those from high socio-

lic schools, 33 (15.7%), when compared to the private

economic class. Low socioeconomic status was signifi-

schools, 10 (4.8%). On the other hand, overweight/

cantly associated with higher prevalence of parasitosis

(X = 148.7. P = <0.0001). In contrast, use of anthelmin-

obesity was three and half times more frequent in the

private school, 57 (27.1%), when compared to the public

thic in the last one year was associated with statistically

significant lower prevalence of parasitosis (X = 119.3,

school, 16 (7.7%). This nutritional pattern was signifi-

cantly different (P = <0.0001).

P = <0.0001). Age and nutritional status had no statisti-

cally significant effect on the prevalence (P= > 0.05).

Table 4: Nutritional status of the respondents

BMI percentile

Public

Private

P-value

Table 6: Prevalence of Intestinal parasitosis by various factors

School

among the study population

n (%)

Variables

Parasitosis

P-value

Underweight (<

33 (15.7)

10 (4.8)

41.38

<0.000

Positive n

Negative

5 )

(%)

n(%)

Normal (5 to <

161 (76.7)

143 (68.1)

Age (Years)

85 )

5-6

37 (48.1)

40 (51.9)

3.971

0.4100

Overweight (85

14 (6.7)

28 (13.3)

7-8

45 (42.9)

60 (57.1)

to <95 )

9-10

70 (53.4)

61 (46.6)

Obese ( ≥ 95 )

2 (1.0)

29 (13.8)

11-12

32 (48.5)

34 (51.5)

Total

210 (100)

≥ 13

16 (39.0)

25 (61.0)

*, Chi-square test for trend

Socio-economic status

Low

50 (90.9)

5 (9.1)

148.7

<0.0001

One hundred and sixty-four (78.1%) pupils from the

Middle

124 (67.0)

61 (33.0)

public schools had intestinal parasites compared to 36

High

26 (14.4)

154 (85.6)

(17.1%) from the private schools. Pupils from the public

Types of Toilet

schools were 17.23 times more likely to have intestinal

Open defaeca-

3 (60.0)

2 (40.0)

3.918

0.2704

tion

parasitic infestation compared to those from private

Pit latrine

7 (77.8)

2 (12.2)

schools (OR =17.23, 95% CI = 10.6-28.01, p =

Water closet

189 (46.9)

214 (53.1)

<0.0001).The prevalence of multiple parasitic infesta-

Others

1 (33.3)

2 (66.7)

tion was 14.8% in the public schools and none in the

Nutritional Status

private schools. The commonest parasites seen in both

Underweight

22 (51.2)

21 (48.8)

0.2605

0.8779

the public and private schools was Ascaris lumbricoides

Normal

143 (47.0)

161 (53.0)

accounting for 62.8%and 66.7%of infestation in the

Overweight/

35 (47.9)

38 (52.1)

public and private schools respectively. The overall pat-

obese

tern of infestation was statistically different between the

Dewormed

public and private school (X =13.52, p = 0.0002). At

Yes

60 (24.8)

182 (75.2)

119.3

<0.0001

140 (78.7)

38 (21.3)

individual parasite level, only Trichuris trichura showed

Source of water

statistically significant different pattern between the two

Bore hole

120 (57.4)

89 (42.6)

21.95

<0.0001

groups (P = <0.0001).

Pipe borne

57 (35.0)

106 (65.0)

Well

5 (83.3)

1 (16.7)

Table 5: Frequency and Pattern of intestinal parasites isolated

Others

18 (42.9)

24 (57.1)

among the respondents

Type of parasite

Public

Private

P-value**

Schools

Schools (n

(n=164)

= 36)

n (%)*

n (%)

Discussion

Ascaris Lumbricoides

103 (62.8)

24 (66.7)

0.7066

Trichuris Trichura

11 (6.7)

12 (33.3)

<0.0001

The findings from this survey show that there is wide

Entamoeba coli

15 (9.1)

0 (0.0)

0.0778

disparity in the prevalence of intestinal parasitic infesta-

Hymanolepsi Nana

5 (3.0)

0 (0.0)

0.5875

tion between the pupils from private schools (17.1%)

Hookworm

10 (6.1)

0 (0.0)

0.2136

Entameba Histolytica

21 (12.8)

0 (0.0)

0.0165

and those from public schools (78.1%). This finding

Fasciola Hepatica

5 (3.0)

0 (0.0)

0.5875

agrees with the findings from previous studies; Og-

wurike et al reported prevalence of 16.6% and 46.6%

Schistosoma Mansoni

5 (3.0)

0 (0.0)

0.5875

from Jos in Nigeria, while Debalke et al from Ethiopia

Gardia Lamblia

5 (3.0)

0 (0.0)

0.5875

Strongiloides stercorales

5 (3.0)

0 (0.0)

0.5875

found prevalence of 20.9% and 53.5%, both in pupils

Enterobius vermicularis

10 (6.1)

0 (0.0)

0.2136

from private and public primary schools respectively.

However, the disparity observed in this study is much

*Some of the pupils had more than one parasites identified; **

wider than was documented by the two previous stud-

Fisher’s exact test

ies.

14,17

This is most likely due to the difference in spec-

X =13.52, p = 0.0002

trum of parasites considered. While the previous studies

focused on helminths alone, this work, in addition, also

The proportion of infection was highest among pupils

identified other forms of intestinal parasites other than

from low socioeconomic family 90.9% while the least

helminths. This assertion is further supported by the

prevalence of 17.1% found in the private schools where

Nutritional status had no significant effect on the preva-

only helminths were isolated which is comparable to

lence of intestinal parasitic infection among the study

16.6% and 20.9% in the previous studies.

population. This is contrary to the findings in several

earlier studies,

23-25

This wide disparity in prevalence between the schools

where malnutrition has consistently

might be due to variation in the various factors associ-

been found to be associated with higher prevalence of

ated with the transmission of the parasites including

intestinal parasites. Intestinal parasitic infections have

factors like age, socioeconomic status, type of housing,

been said to exert a very heavy toll on the nutritional

source of water, mode of sewage disposal and nutri-

status of children through increased metabolic rate, ano-

tional status.

rexia and diarrhoea among other things hence contribut-

ing to undernutrition . The reason why we could not

Similar to the findings in previous studies

10,18,19

age had

no significant association with intestinal parasite infec-

demonstrate similar relationship between malnutrition

tion. Odinaka et al

found the highest prevalence

and intestinal parasitic infection in this work is not clear.

among children aged 8-10years and least among those

Deworming was significantly associated with lower

14 -16years but in the overall this variation by age was

prevalence of intestinal parasites among the study popu-

not statistically significant. Similarly, Obikwu et al

lation affirming the fact that intermittent use of

and Ukpai et al observed slightly higher prevalence

anthelminthic remains an important and effective control

measure. Palatty et al in 2015 also demonstrated a sig-

among children between the ages of 9-12years but again

were not significantly different from other age groups.

nificant reduction in prevalence of intestinal parasites

In this study, the highest prevalence of 53.4% was found

among Indian school children following Government

among those aged 9-10years. The reason for this consis-

sponsored 6 monthly deworming programme but how-

tent finding of higher prevalence among children be-

ever, noted that anthelminthic chemoprophylaxis alone

tween 8-12 years of age is not clear but may be due to

is unlikely to control the scourge due to its multifactorial

the adventurous nature of the early adolescent.

nature.

The high prevalence of 90.9% among pupils of low so-

cioeconomic class compared to 14.4% among those of

Ascaris lumbricoides was the most frequently isolated

high socioeconomic status highlights the cardinal role of

helminths in both the public (62.8%) and private

low socioeconomic status in the prevalence of intestinal

(66.7%) schools.

While several authors have docu-

mented similar parttern , others have found Hook-

8.9

parasite. The pupils from public school were signifi-

cantly of lower socioeconomic class compared to those

worms

the

most

frequently

isolated

10,18,19

of private school and hence the high prevalence re-

helminths

. This study similar to the earlier studi-

8,9

corded in the public schools. Several other studies have

were carried out in the urban centre as opposed to

the others

10,18,19

equally highlighted similar relationship between low

which were studies from rural commu-

socioeconomic status and prevalence of intestinal parasi-

nities. The reason for the variation in pattern of helmin-

tosis.

8-10,20

It is a known fact that low socioeconomic

thic isolates in studies from urban centres and those

status is an important determinant of slum dwelling in

from rural area is not clear but might be due to differ-

urban centres which provides conducive environment

ences in occupation and behaviour. While majority of

for parasite transmission. The search of the literature

inhabitants of rural communities in Nigeria are usually

yielded no contrary finding.

peasant farmers and are more likely to walk bare footed,

urban dwellers are predominantly civil servants and

In our study, mode of sewage disposal had no significant

traders. Some authors however, have not find any differ-

ence in pattern between rural and urban populations.

effect on the prevalence of intestinal parasites. Other

studies

9,10

have equally documented similar results. In

contrast, several other studies

8,18-12

have found mode of

sewage disposal to be an important factor in the preva-

lence of intestinal parasites. The finding in this study

Conclusion

and that of Salawu et al and Odinaka et al however is

not surprising as majority of the participants, 403(96%)

In conclusion, Intestinal parasitic infestation remains a

in our study, used similar mode of sewage disposal and

very common problem among children in urban centres

hence eliminating its supposed effect in the study popu-

in Nigeria with the highest burden among pupil in the

lation.

public schools. We recommend incorporation and provi-

Source of water supply had statistically significant asso-

sion of free anthelminthic to all pupil in public school at

ciation with the prevalence of intestinal parasite. The

the beginning of every term into the school health pro-

importance of source of water supply in the local epide-

gramme, while addressing the major risk factors in the

miology of intestinal parasites have been documented by

wider society.

several authors

6,21,22

. Of concern however, is the high

rate of infection 120 (57.4%) among children from fami-

lies using bore hole as source of water which is expected

Conflict of interest: None

to be contamination free. The reason for this observation

Funding: None

is not clear but might have to do with siting and depth of

the bore hole as well as surface storage facility.

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