Mahmudetal. BMC Res Notes (2020) 13:1
parasitic infections, anaemia, anddiarrhoea
amongschool aged children, andtheimpact
ofhand-washing andnail clipping
Mahmud Abdulkader Mahmud1* , Mark Spigt2, Afework Mulugeta Bezabih3, Geert‑Jan Dinant2
and Roman Blanco Velasco4
Objective: In marginalized setting, under‑nutrition and illnesses due to infectious agents create a vicious circle. In
our previous study, we reported that easy‑to‑do hand hygiene interventions were eﬀective in preventing intestinal
parasite infections (IPIs) and reduce the rate of anaemia among school‑aged children. The aim of this study was to
assess the pattern of associations between IPIs, anaemia and diarrhoea among the school‑aged children and to
explore if the observed impact of hand‑washing and nail clipping interventions in our ﬁndings was similar across
children with diﬀerent baseline demographic and disease characteristics. The study was based on the analysis of
data that was collected during the randomized controlled trial and hence have used the same study participants and
Results: Children with IPIs had a much higher chance of also being anaemic (AOR 2.09, 95% CI 1.15–3.80), hav‑
ing diarrhoea (AOR 2.83, 95% CI 1.57–5.09), and vice versa. Anaemia and diarrhoea were very strongly related (AOR
9.62, 95% CI 5.18–17.85). Overall, hand‑washing with soap at key times and weekly nail clipping were eﬃcacious
in preventing intestinal parasite re‑infection among children despite the diﬀerences in baseline demographic
Trial registration: NCT01619254 (June 09/2012)
Keywords: Intestinal parasitic infections, Anaemia, Diarrhoea, Hand‑washing, School‑aged children
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In resource‐poor settings, under‐nutrition and illnesses
due to infectious diseases are highly prevalent and closely
interlinked. Nutritional deﬁciencies predispose people
to infection, and infections lead to nutritional deﬁcien-
cies which further reduce resistance to new infections
[1–3]. Children are especially susceptible to the delete-
rious eﬀects of under‐nutrition  and infections  in
In Ethiopia, similar to many developing countries, IPIs
[6, 7] and anaemia [6, 8] are common among school‐aged
children. is suggests that school‐aged children in Ethi-
opia may be vulnerable to the cyclical ill‐eﬀects of anae-
mia and illnesses due to parasitic infections. However,
there is insuﬃcient evidence regarding the associations
of IPIs, anaemia and diarrhoea among these population
groups in the country.
BMC Research Notes
1 Medical Microbiology and Immunology Department, Biomedical
Division, School of Medicine, Mekelle University, PO. Box: 1871, Mekelle,
Full list of author information is available at the end of the article
Page 2 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
Remarkable heterogeneity is documented in the dis-
tribution patterns of IPIs . Several demographic ,
socioeconomic , and environmental  factors
inﬂuence the distribution patterns of IPIs within a com-
munity. ese factors can create diﬀerent distributions of
susceptibility to re‐infection by IPIs among a population,
and hence, diﬀerent groups of children may be at diﬀer-
ent risks of parasitic re‐infection.
A randomised controlled trial revealed a signiﬁcant
impact of regular hand‐washing with soap on the preven-
tion of parasitic re‐infection and anaemia among children
. It is unknown if certain characteristics of the chil-
dren also determined the eﬀects of hand‐washing. One
could imagine, for example, that in areas where parasites
are distributed by polluted water, that hand‐washing
would not be eﬀective in preventing parasitic infections.
We set out to explore if the eﬀect of hand‐washing and
nail clipping interventions in our ﬁndings  was simi-
lar across the study population despite their diﬀerent
In our previous randomized controlled trial , we
reported that easy-to-do hand washing interventions
were eﬀective in preventing intestinal parasite infections
(IPIs) and reduce the rate of anaemia among school-
aged children. is study was carried out on the analysis
of data collected during the randomized controlled trial
with the objective of assessing whether the observed eﬃ-
cacy of the easy-to-do hand washing interventions was
universally eﬀective to prevent infection among the same
school‐aged children with diﬀerent socio-demographic
baseline characteristics. Moreover, we aimed to explore
whether infection and malnutrition were interlinked and
hence the infection prevention interventions used in the
previous study would break the vicious cycle of infection
and malnutrition in such marginalized areas for the long-
term health beneﬁts of this population group.
Data collection procedure
Baseline data brieﬂy, demographics (child age, gender,
latrine use, maternal age, family size, family drinking water
source, and living house ownership), socio economic
(maternal education) and pre‐existing disease character-
istics (IPIs, anaemia, and thinness) were included for this
analysis from data collected during the previous rand-
omized controlled trial .
Parasitological analysis Following 6months follow‐up,
fresh stool specimens were collected from the study sub-
jects. Stool specimens were analysed using direct saline
wet mount, formalin ethyl‐acetate concentration tech-
nique  and the Kato‐Katz technique . A child was
classiﬁed as re‐infected if an infection was detected by any
methods used. Sub‐samples of stool smears, comprising
10% of the total, were re‐examined for quality control pur-
Diarrhoea incidence Data on self‐reported diarrhoeal
episodes were collected using a separate questionnaire
on a weekly basis during the study period. Diarrhoea was
deﬁned as the passage of three or more loose or liquid
stools per day .
Anthropometry Anthropometric measurements were
taken at the start and the end of the follow‐up in duplicate
and the average of the two measurements was recorded.
Portable weight scales and locally made stadiometers with
a sliding headpiece were used to measure weight (to the
nearest 0.1kg) and height (to the nearest 0.1cm), respec-
tively. Each child was weighed with minimal clothing and
barefooted. e weighing scales were calibrated using
standard calibration weights of 5 kg iron bars. Height
measurements were taken with children faced forwards,
barefooted with feet ﬂat and together, and their heels and
back against the rod. Anthropometric measurements
were converted into BMI‐for‐age Z scores using WHO
AnthroPlus software, version 1.0.4 (WHO Anthro 2007,
WHO, Geneva, Switzerland). Children below − 2Z scores
for BMI‐for‐age were classiﬁed as thin.
Statistical analysis was computed using SPSS for Win-
dows version 16.0 (Chicago, USA). Associations between
post‐intervention IPIs, anaemia, and diarrhoea were ana-
lyzed using binary and multivariate logistic regression
models by odds ratios (OR) and 95% conﬁdence intervals
(CI). e impact of hand‐washing with soap and nail clip-
ping on intestinal parasite re‐infection across children
with diﬀerent demographic and disease characteristics
was analysed using logistic regression models. Stratiﬁca-
tions included baseline demographics (child age, gender,
latrine use, maternal education, maternal age, family size,
family drinking water source, and living house owner-
ship) and pre‐existing disease characteristics (IPIs, anae-
mia, and thinness). Possible moderating eﬀects of each
baseline variable on the eﬀect of intervention were iden-
tiﬁed by adding interaction terms to the regression model
. Statistical signiﬁcance was set at p < 0.05.
Baseline characteristics and the trial proﬁle of the
original project have been described previously .
Brieﬂy, 365 (99%) children were analysed for six‐month
Page 3 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
follow‐up. Boys comprised 41% (n = 150) of the study
participants and mean age was 10 (SD = 2.6) years. Fol-
lowing 6months follow‐up, 21% (95% CI 17–25%) of the
children were re‐infected with intestinal parasites, 18%
(95% CI 14–22%) of the children were anaemic and 17%
(95% CI 13–21%) had diarrhoea.
Table 1 describes the multivariate logistic regression
analysis results of the associations between intestinal
parasitosis, anaemia, and diarrhoea. Eﬀects were adjusted
for each intervention. Current intestinal parasitosis, a
history of diarrhoea in the previous week, and current
anaemia were independently associated. IPIs were sig-
niﬁcantly associated with anaemia (AOR 2.09, 95% CI
1.15–3.80) and diarrhoea (AOR 2.83, 95% CI 1.57–5.09),
and vice versa. Anaemia and diarrhoea were also strongly
related (AOR 9.62, 95% CI 5.18–17.85), meaning that
children with diarrhoea had a very high chance of also
having anaemia, and vice versa.
Both hand‐washing with soap (AOR 0.32, 95% CI 0.20–
0.62, p = 0.001) and weekly ﬁnger nail clipping (AOR
0.51, 95% CI 0.27–0.95, p = 0.035) interventions were
reported to have a signiﬁcant impact in reducing intes-
tinal parasite re‐infection rates among the study partici-
In this study, we explored if these impacts were simi-
lar across children with diﬀerent demographic and dis-
ease backgrounds. Overall, interventions seem equally
eﬃcacious among children regardless of age, gender,
drinking water source, latrine use, mother’s age, mother’s
education, family size, house ownership, and history of
intestinal parasitosis, anaemia and thinness at baseline
(Table 2). e impact of hand‐washing was similar for
the whole group and for children who had IPIs at base-
line, but the eﬀect signiﬁcantly increased in children
who were parasite‐free at baseline (AOR 0.48 vs. AOR
0.31, p = 0.048). e eﬀects of hand‐washing and nail
clipping were higher for children whose drinking water
sources were wells and streams compared to those who
used pipeline and boreholes, but the eﬀects were not
statistically signiﬁcant (AOR 0.44 vs. AOR 0.08, p = 0.134
and AOR 0.68 vs. AOR 0.09, p = 0.053; respe ctively).
Findings of the present study demonstrate a clear rela-
tionship between IPIs, anaemia and diarrhoea among
children. Children with IPIs had a much higher chance
of also being anaemic and having diarrhoea. Anaemia
and diarrhoea were also very strongly related, as chil-
dren with diarrhoea had a very high chance of also hav-
ing anaemia, and vice versa. Hand-washing with soap and
nail clipping prevents the children from intestinal para-
site infections regardless their demographic diﬀerences
and hence breaks the vicious cycle of IPIs, anemia and
diarrhoea among the children.
Associations observed between anaemia and IPIs in
our data concord with other studies that showed IPIs to
be substantially linked with anaemia in children [18–21].
IPIs can decrease food and nutrient intake, cause intes-
tinal blood losses, induce red blood cell destruction by
the spleen, and induce autoimmune reactions leading to
chronic inﬂammation [20, 21]. ese eﬀects may have
accounted for the considerable proportion of anaemia
observed among the children infected with intestinal
Although in most instances IPIs are asymptomatic,
they may also cause diarrhea . IPIs can induce diar-
rhoea by increasing small intestine motility while reduc-
ing its digestive and absorptive capacities . Our
ﬁnding that diarrhoea may contribute substantially to
anaemia among children was also consistent with other
reports from developing settings . Diarrhoeal dis-
eases are reported to be associated with an increased
production of cytokines, interleukin 6 and tumour necro-
sis factor alpha . ese cytokines are indicated to play
a signiﬁcant role in causing anaemia . Repeated epi-
sodes of diarrhoea in children are also reported to lead
to decreased nutrient absorption, due to injury of the
small intestine mucosa . In our data, anaemia was
Table 1 Associations between intestinal parasitic infections, anaemia and diarrhoea among school-aged children,
Ethiopia (n = 365)
CI 95% condence interval, AOR adjusted odds ratio as computed by the logistic regression model, IPI intestinal parasitic infection
*Statistically signicant at 0.05
Post-intervention out-come variables (n) Post-intervention out-come variables
IPI Anaemia Diarrhoea
AOR (CI) AOR (CI) AOR (CI)
IPI (79) – 2.09 (1.15 to 3.80)* 2.83 (1.57 to 5.09)*
Anaemia (81) 2.09 (1.15 to 3.80)* – 9.62 (5.18 to 17.85)*
Diarrhoea (68) 2.83 (1.57 to 5.09)* 9.62 (5.18 to 17.85)* –
Page 4 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
Table 2 Impact of hand-washing on parasite re-infection rates across children withdierent base-line demographic
anddisease characteristics (n = 365)
CI 95% condence interval, AOR adjusted odds ratio
*Statistically signicant at 0.05
a Adjusted for intervention
Hand-washing vs. control Nail clipping vs. control
0.43 (0.24, 0.68) 0.59 (0.36, 0.98)
AOR (CI)aAOR (CI)aAOR (CI)aAOR (CI)a
0.41 (0.17, 0.97) 0.39 (0.20, 0.75) 0.34 (0.14, 0.82) 0.79 (0.41, 1.51)
p = 0.923 p = 0.131
Age 6–9 years 10–15 years 6–9 years 10–15 years
208 (57%) 157 (43%) 208 (57%) 157 (43%)
0.30 (0.13, 0.66) 0.50 (0.25, 1.01) 0.50 (0.23, 1.09) 0.66 (0.33, 1.31)
p = 0.338 p = 0.604
Water source Pipeline and borehole Wells and streams Pipeline and borehole Wells and streams
321 (88%) 44 (12%) 321 (88%) 44 (12%)
0.44 (0.25, 0.76) 0.08 (0.01, 0.68) 0.68 (0.39, 1.17) 0.09 (0.13, 0.64)
p = 0.134 p = 0.053
Latrine use Yes No Yes No
139 (38%) 226 (62%) 139 (38%) 226 (62%)
0.33 (0.13, 0.81) 0.44 (0.23, 0.84) 0.48 (0.20, 1.19) 0.61 (0.32, 1.16)
p = 0.744 p = 0.791
Mother education Literate Illiterate Literate Illiterate
161 (44%) 204 (56%) 161 (44%) 204 (56%)
0.58 (0.26, 1.30) 0.28 (0.14, 0.58) 0.83 (0.37, 1.85) 0.42 (0.21, 0.84)
p = 0.198 p = 0.207
Maternal age ≤ 35 > 35 ≤ 35 > 35
193 (53%) 172 (47%) 193 (53%) 172 (47%)
0.22 (0.09, 0.51) 0.58 (0.28, 1.22) 0.58 (0.21, 1.58) 0.71 (0.25, 2.02)
p = 0.085 p = 0.787
Family size ≤ 6 members > 6 members ≤ 6 members > 6 members
208 (57%) 157 (43%) 208 (57%) 157 (43%)
0.27 (0.13, 0.54) 0.69 (0.31, 1.55) 0.60 (0.30, 1.17) 0.53 (0.23, 1.20)
p = 0.082 p = 0.814
House ownership Yes No Yes No
307 (84%) 58 (16%) 307 (84%) 58 (16%)
0.45 (0.26, 0.79) 0.17 (0.03, 0.88) 0.71 (0.40, 1.24) 0.19 (0.05, 0.77)
p = 0.661 p = 0.386
Baseline parasite infection status Yes No Yes No
146 (40%) 219 (60%) 146 (40%) 219 (60%)
0.48 (0.23, 1.01) 0.31 (0.14, 0.67) 0.44 (0.20, 0.97) 0.69 (0.34, 1.43)
p = 0.048* p = 0.696
Baseline anemia status Yes No Yes No
106 (29%) 259 (71%) 106 (29%) 259 (71%)
0.59 (0.25, 1.39) 0.32 (0.16, 0.64) 0.54 (0.23, 1.26) 0.60 (0.31, 1.15)
p = 0.577 p = 366
Baseline BMI‑for‑age Thin Normal Thin Normal
150 (41%) 215 (59%) 150 (41%) 215 (59%)
0.33 0.15, 0.75) 0.45 (0.23, 0.91) 0.44 (0.20, 0.97) 0.71 (0.36, 1.42)
p = 0.577 p = 0.366
Page 5 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
also an independent risk factor for both IPIs and diar-
rhoea. In agreement with our ﬁndings, Levy et al. 
have reported that anaemia increases rates of infection
in children. Furthermore, reports from several studies
have indicated that anaemia can predispose people to
infections by lowering host immunity [28, 29]. In general,
our ﬁndings strengthen the well‐established notion that
infection and malnutrition are intricately linked [1, 30,
e observed signiﬁcant preventive impact of hand‐
washing and nail clipping on intestinal parasite re‐
infection rates made us curious to explore whether
the intervention eﬀect noted in the whole cohort was
homogenous across children with diﬀerent backgrounds.
Hand‐washing with soap and nail clipping interven-
tions consistently favoured reduction of intestinal para-
site re‐infection rates across each sub‐group analysed.
A signiﬁcant diﬀerence in the eﬀect of hand‐washing
was observed only for baseline parasitic infection sta-
tus. Based on our data, it is possible to suggest that ben-
eﬁt from the interventions is likely to be more universal
among the study groups. e observed increased beneﬁt
of hand‐washing among children who were parasite‐free
at baseline should be interpreted with caution, although
analyses were based on formal tests of interaction. Chil-
dren were made parasite‐free at recruitment and this
might have aﬀected our analysis at follow‐up. e diﬀer-
ence in eﬀect for hand‐washing and nail clipping between
children who use pipeline and borehole water sources
and those using wells and streams is quite large, but not
signiﬁcant because of the small number of children who
use wells and streams.
In conclusion, our ﬁndings emphasise that intestinal
parasitosis, anaemia and diarrhoea were independently
associated. Furthermore, hand‐washing with soap and
nail clipping were eﬃcacious in preventing intestinal par-
asite re‐infection despite baseline diﬀerences and hence
can be universally used as infection prevention interven-
tions among school‐aged children to break the vicious
cycle of infection and malnutrition for the long‐term
health beneﬁts of this population.
e following limitation should be considered when
interpreting the results of the present study: the study
was powered to determine the overall eﬀect of the inter-
ventions in the original randomized controlled trial. Our
subgroup analyses might hence be underpowered to
detect subgroup eﬀects, unless the diﬀerences in treat-
ment eﬀects between subgroups would have been very
AOR: adjusted odds ratio; BMI: body‑mass‑index; CI: conﬁdence interval; IPIs:
intestinal parasitic infections; OR: odds ratio; SD: standard deviation; WHO:
World Health Organization.
The authors are grateful for all the children and their parents and/or guard‑
ians for the participation. We thank the ﬁeldworkers who implemented the
interventions and carried out the follow‑up. We express our sincere gratitude
to the laboratory personnel involved in the ﬁeld work. Our sincere acknowl‑
edgement also goes to the Tigray Regional Health Bureau, Mekelle University,
Ethiopia and Alcala University, Spain for their support and cooperation.
MAM participated in all phases of the study including writing the proposal,
data collection and writing the manuscript. MAM, MS, AMB, G‑JD, RBV con‑
ceived and designed the experiments. MAM, MS, and G‑JD analysed the data.
MAM and MS wrote the ﬁrst manuscript. MAM, MS, AMB, G‑JD and RBV con‑
tributed to the writing of the manuscript. MS and G‑JD revised and approved
the manuscript. All authors have read, and conﬁrm that they meet, ICMJE
criteria of authorship. All authors read and approved the ﬁnal manuscript.
Availability of data and materials
The datasets used and/or analysed during the current study are available from
the corresponding author on reasonable request.
Ethics approval and consent to participate
The study protocol and informed consent procedure for the initial randomized
controlled trial was approved by the Institutional Review Board of the College
of Health Sciences, Mekelle University, Ethiopia. Written informed consent
was obtained from each child’s parents and/or guardians. Children diagnosed
positive for IPIs at follow‐up were treated with standard medication , and
children with anaemia and/or diarrhoea were sent to the health facilities for
further medical attention.
Consent for publications
The authors declare that they have no competing interests.
1 Medical Microbiology and Immunology Department, Biomedical Division,
School of Medicine, Mekelle University, PO. Box: 1871, Mekelle, Ethiopia.
2 Department of Family Medicine, CAPHRI School for Public Health and Pri‑
mary Care, Maastricht University, Maastricht, The Netherlands. 3 School of Pub‑
lic Health, College of Health Sciences, Mekelle University, Mekelle, Ethiopia.
4 Department of Surgery, School of Medicine, Alcala University, Madrid, Spain.
Received: 29 October 2019 Accepted: 20 December 2019
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