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Associations between intestinal parasitic infections, anaemia, and diarrhoea among school aged children, and the impact of hand-washing and nail clipping

Authors:

Abstract

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 study area. Results: Children with IPIs had a much higher chance of also being anaemic (AOR 2.09, 95% CI 1.15-3.80), having 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 characteristics. Trial registration: NCT01619254 (June 09/2012).
Mahmudetal. BMC Res Notes (2020) 13:1
https://doi.org/10.1186/s13104-019-4871-2
RESEARCH NOTE
Associations betweenintestinal
parasitic infections, anaemia, anddiarrhoea
amongschool aged children, andtheimpact
ofhand-washing andnail clipping
Mahmud Abdulkader Mahmud1* , Mark Spigt2, Afework Mulugeta Bezabih3, Geert‑Jan Dinant2
and Roman Blanco Velasco4
Abstract
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
study area.
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
characteristics.
Trial registration: NCT01619254 (June 09/2012)
Keywords: Intestinal parasitic infections, Anaemia, Diarrhoea, Hand‑washing, School‑aged children
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Introduction
In resourcepoor settings, undernutrition 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
[13]. Children are especially susceptible to the delete-
rious effects of undernutrition [4] and infections [5] in
developing settings.
In Ethiopia, similar to many developing countries, IPIs
[6, 7] and anaemia [6, 8] are common among schoolaged
children. is suggests that schoolaged children in Ethi-
opia may be vulnerable to the cyclical illeffects 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.
Open Access
BMC Research Notes
*Correspondence: muheab2008@yahoo.com
1 Medical Microbiology and Immunology Department, Biomedical
Division, School of Medicine, Mekelle University, PO. Box: 1871, Mekelle,
Ethiopia
Full list of author information is available at the end of the article
Page 2 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
Remarkable heterogeneity is documented in the dis-
tribution patterns of IPIs [9]. Several demographic [10],
socioeconomic [11], and environmental [12] factors
influence the distribution patterns of IPIs within a com-
munity. ese factors can create different distributions of
susceptibility to reinfection by IPIs among a population,
and hence, different groups of children may be at differ-
ent risks of parasitic reinfection.
A randomised controlled trial revealed a significant
impact of regular handwashing with soap on the preven-
tion of parasitic reinfection and anaemia among children
[13]. It is unknown if certain characteristics of the chil-
dren also determined the effects of handwashing. One
could imagine, for example, that in areas where parasites
are distributed by polluted water, that handwashing
would not be effective in preventing parasitic infections.
We set out to explore if the effect of handwashing and
nail clipping interventions in our findings [13] was simi-
lar across the study population despite their different
characteristics.
Main text
Methods
Description ofthetrial
In our previous randomized controlled trial [13], 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
schoolaged 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 preexisting disease character-
istics (IPIs, anaemia, and thinness) were included for this
analysis from data collected during the previous rand-
omized controlled trial [13].
Parasitological analysis Following 6months followup,
fresh stool specimens were collected from the study sub-
jects. Stool specimens were analysed using direct saline
wet mount, formalin ethylacetate concentration tech-
nique [14] and the KatoKatz technique [15]. A child was
classified as reinfected if an infection was detected by any
methods used. Subsamples of stool smears, comprising
10% of the total, were reexamined for quality control pur-
poses.
Diarrhoea incidence Data on selfreported 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 [16].
Anthropometry Anthropometric measurements were
taken at the start and the end of the followup 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 0.1kg) and height (to the nearest 0.1cm), 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 BMIforage Z scores using WHO
AnthroPlus software, version 1.0.4 (WHO Anthro 2007,
WHO, Geneva, Switzerland). Children below 2Z scores
for BMIforage were classified as thin.
Statistical analysis
Statistical analysis was computed using SPSS for Win-
dows version 16.0 (Chicago, USA). Associations between
postintervention 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 handwashing with soap and nail clip-
ping on intestinal parasite reinfection 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 preexisting 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
[17]. Statistical significance was set at p < 0.05.
Results
Baseline characteristics and the trial profile of the
original project have been described previously [13].
Briefly, 365 (99%) children were analysed for sixmonth
Page 3 of 6
Mahmudetal. BMC Res Notes (2020) 13:1
followup. Boys comprised 41% (n = 150) of the study
participants and mean age was 10 (SD = 2.6) years. Fol-
lowing 6months followup, 21% (95% CI 17–25%) of the
children were reinfected 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 handwashing 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 reinfection rates among the study partici-
pants [13].
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 handwashing was similar for
the whole group and for children who had IPIs at base-
line, but the effect significantly increased in children
who were parasitefree at baseline (AOR 0.48 vs. AOR
0.31, p = 0.048). e effects of handwashing 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).
Discussion
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 [1821].
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
parasites.
Although in most instances IPIs are asymptomatic,
they may also cause diarrhea [22]. IPIs can induce diar-
rhoea by increasing small intestine motility while reduc-
ing its digestive and absorptive capacities [23]. Our
finding that diarrhoea may contribute substantially to
anaemia among children was also consistent with other
reports from developing settings [24]. Diarrhoeal dis-
eases are reported to be associated with an increased
production of cytokines, interleukin 6 and tumour necro-
sis factor alpha [25]. ese cytokines are indicated to play
a significant role in causing anaemia [24]. Repeated epi-
sodes of diarrhoea in children are also reported to lead
to decreased nutrient absorption, due to injury of the
small intestine mucosa [26]. In our data, anaemia was
Table 1 Associations between intestinal parasitic infections, anaemia and diarrhoea among school-aged children,
Ethiopia (n = 365)
CI 95% condence interval, AOR adjusted odds ratio as computed by the logistic regression model, IPI intestinal parasitic infection
*Statistically signicant 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
Mahmudetal. BMC Res Notes (2020) 13:1
Table 2 Impact of hand-washing on parasite re-infection rates across children withdierent base-line demographic
anddisease characteristics (n = 365)
CI 95% condence interval, AOR adjusted odds ratio
*Statistically signicant 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)
Gender Male
150 (41%)
Female
215 (49%)
Male
150 (41%)
Female
215 (49%)
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
Mahmudetal. 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. [27]
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 wellestablished notion that
infection and malnutrition are intricately linked [1, 30,
31].
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.
Handwashing with soap and nail clipping interven-
tions consistently favoured reduction of intestinal para-
site reinfection rates across each subgroup analysed.
A significant difference in the effect of handwashing
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 handwashing among children who were parasitefree
at baseline should be interpreted with caution, although
analyses were based on formal tests of interaction. Chil-
dren were made parasitefree at recruitment and this
might have affected our analysis at followup. e differ-
ence in effect for handwashing 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, handwashing with soap and
nail clipping were efficacious in preventing intestinal par-
asite reinfection despite baseline differences and hence
can be universally used as infection prevention interven-
tions among schoolaged children to break the vicious
cycle of infection and malnutrition for the longterm
health benefits of this population.
Limitations
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
large.
Abbreviations
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.
Acknowledgements
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.
Authors’ contribution
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.
Funding
None.
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 followup were treated with standard medication [16], and
children with anaemia and/or diarrhoea were sent to the health facilities for
further medical attention.
Consent for publications
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
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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... Our final assessment of access to hygiene indicators of WASH demonstrates (1) the consequences of poor parental involvement (23% do not know if their child uses soap in schools) in monitoring WASH services and (2) the necessity to establish or improve the previously mentioned parent-teacher collaboration. The postulate of a causal link of non-compliance with the rules of personal hygiene and an increase in the incidence of diseases is constantly brought to the attention of children [18,44,45]. At the same time, the insufficient level of access to hygiene items at school creates a paradoxical situation (discrepancy between desire and opportunity) among students, which in the future could potentially become one of the triggers for the development of unwillingness to observe hygiene rules, due to accumulated negative experiences. ...
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Data on intensity of infection (e.g. faecal egg count) were reported in a variety of ways across studies, precluding the pooling of results for this outcome. We did not find any studies reporting adverse events resulting from the WASH interventions under study or from mass drug administration (MDA). Authors' conclusions: Whilst the available evidence suggests that the WASH interventions under study may slightly protect against STH infection, WASH also serves as a broad preventive measure for many other diseases that have a faecal oral transmission route of transmission. As many of the studies were done in addition to MDA/deworming (i.e. MDA was ongoing in both the intervention and control arm), our data support WHO recommendations for implementation of improvements to basic sanitation and adequate access to safe water alongside MDA. The biological plausibility for improved access to WASH to interrupt transmission of STHs is clear, but WASH interventions as currently delivered have shown impacts that were lower than expected. There is a need for more rigorous and targeted implementation research and process evaluations in order that future WASH interventions can better provide benefit to users. Inconsistent reporting of the intensity of infection underscores the need to define the minimal, standard data that should be collected globally on STHs to enable pooled analyses and comparisons.
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Health inequities are a common problem for all countries and are the result of not only adverse social conditions but also poor public policies. Today chronic diseases represent the most relevant threats and are a current challenge. Parasitic infections, a leading cause of child morbidity affecting low-income populations, can be transmitted because of an unhealthy environment. Notwithstanding, scarce data have been published on the epidemiological profile of intestinal parasitoses in asymptomatic children living in shantytowns. Vulnerable populations settled in slums are growing in Argentina, particularly in Buenos Aires city. Consequently, this work intended to screen healthy carriers of enteric parasites and determine the epidemiologic profile in asymptomatic children residing in one of those communities, to explore risk factors associated with the transmission of parasites, and to initiate a basic health education campaign to promote healthy behavior in the community. Fecal samples (n = 138) were analyzed by conventional parasitological methods and a survey gathered data on symptoms, family composition, and environmental and hygiene-related variables. High prevalence of feco-orally-transmitted parasitoses (83·3%) and polyparasitism were remarkable findings. The main environmental health determinants were those related to excreta disposal and water provision. Health promotion actions were performed through the diffusion of a set of posters with iconic images and brief messages for health education. Results suggest the need for an environmental sanitation policy to complement health promotion actions. It is essential to spread the results of investigations that address inequities and social determinants of health in order to integrate data with local political processes and alert on acceptable actions for developing appropriate interventions.
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Intestinal parasite infections have been known to compromise the quality of human life since prehistoric times. Throughout the ages, human civilizations have fought against parasitism, including intestinal parasites. During the second half of the last century, the focus of disease-combating efforts moved to other imminent public health issues, under the notion that the fight against infectious diseases had been won. However, the disease incidence data indicate that these diseases continue to wreak havoc on human productivity across the globe. Lately, chemotherapeutic intervention has been stressed for the control of intestinal parasitic infections. In this paper we evaluate the need for a holistic approach to address this issue and make recommendations for this cause.
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