Preveive Meine Repos 6 (2017) 27-32
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Metabolic syndrome's risk factors and its association with nutritional status
in schoolchildren
Fabiana Costa Teixeira **, Flavia Erika Felix Pereira, Avany Fernandes Pereira °, Beatriz Goncalves Ribeiro“
+ Prana Ps Crag Niro de Nu UFR Laborato rere de Pei mes do Ere, UY Camps Maco ra
° Prana PCr om Alimentoa,Npo eSals, Ueno sda oo dono UES akan tra de equa om iri opr UF Comps Mao
hf Cs de Nun Unveridde era oi dea, rat
* Po Cs de Nar Laburacioigads de Psu em Cnc opr UF Comps Maca, Sl
Recent fo 2 amy 2917
‘lable eine 8 eraty
The metabolic risk actors (RF) tothe agnosis of metabalic syndrome (MS) have been evidenced a ea 39,
Inclang cilren, The aim of he presen study was to deni the prevalence of RF tothe diagnosis of Mets and
itsasaciton with ntrtional status of schookhikren fom to VOyears old. Acros-sectonal tudy wasted
‘tin 505 students of municipal schools in Maca, Braz, conducted rom 2013 9 2014 The RF evaluated were
blood pressure (mim He), rlycerides (minal), HDL-choesteol (no) fasting glucose (ramol} and waist
‘Sraumferece (cm). A fastone RF was present in 1% (n= 208) ofthe sample. By nutitional tats here was
= fisher peas of Fn overeioesescnlchlren compared tose i oral eight exeptin
Stu éone the contrat of HDL The prevalence oon, oan thee RF (MeiS) wore 307% (n= 175) 21.08
WS seat {m= 0) and 52% (n= 27) respec. Two RF were oe presen overweight (2028952 196, 390)
rc Sn obese (tt 58 9541314521) compared fo nota! weight elien 13589520139, 173}. Tre a
nu itore RF wee mre quent among ces (25 254170, 35) maton ooverwegt (248 952102
8) and nal weet crn (038 9SNL0 17), The datas high revalnce oF an ationship
wh be mud of body weight ences Terfree enicaion a early eament of tes ough
tininic tere Me and reed ean:
12017 The thors ubished by Ese in Thisisan open acess article unde the CCBY-NC-NDcese
itp. fcatvecommonsorgfitensesiy- nd
1. Introduction Ther sno consensus forthe dlagnoss of Metin cilzen (Corte
Metabolic syndrome (MetS) can be defined asthe co-occurrence of
metabolic risk factors (RF) that contributes tothe development of car-
diovascular disease (CVD) and type 2 diabetes mellitus (DM2) (Albert
‘tal, 2009), The RF, a insulin resistance (IR), hypertension (HAS), y=
perelvcemis, hypertriglycerdemia, low high density lipoprotein choes-
terol concentration (HDI-<) and excess waist circumference (WC), have
been identified at earlier ages, including children (Agirbasi etal, 2018),
Iyperersion, HDL, high density poproteim cholesterol ceaceazation: To,
trainer BF, lo presse: dy mando: Ww ceferens SE
* Comesponding autor at: Laborato lnegrado de Pesquisa em Sade e Sociedade
Universidade Feea earl UF. Compas Mass, hi Ni, $9 cans ot
‘Palade tastier (EC Tee} perealetgacrn
(EE Perera} anvergmurcaouipbr (AE Peer) nbekegncaleseOgmalom
(He Ren)
naps on/10 S016) pede 301702802
and Nobili, 2015; D‘Adamo et al, 2011; Petgher et al, 2010). Some
criteria have been suggested and differentiated for RF as ther cutoffs
(Ford ana Li, 2008). However, regardless ofthe eritri, commonly itis
required at least three RF for the diagnosis of MetS in children
(O'Adamn et al, 2011), Whea RF is present during childhood, it tend
to persist through adolescence and adulthood (Magnussen etal.
2014); thus ithas been suggested thatthe focus of research in children
be in the RF of MetS regardless ofits diagnosis (D'Adamo ct al, 2011;
Faienza etal, 2016; Kassiet al, 2011; Sinaiko, 2015),
The RF in children are more common in the obese population
(Abrams and Levit kata, 2011; de et al. 2003), which increased signif.
‘cantly in recent years, representing a serious public health problem in
Brazil and worldwide (IBGE, 2010; Cupra et al, 2013; Marie etal
2014). Although studies to evaluate the nutsitonal status, bload pres-
sure (BP), lipid profile and blood glucose levels in the juvenile group
are growing (Kuschnir etal, 2016; Onzuz and Demir, 2015; Strufaldi
etal, 2009; Wee etal, 2011), they are not so frequent in children espe-
cialy in developing countries (Gupta et al,2013), Early identifieation of
the presence of RF predictors of MetS enables the planning and imple-
‘mentation of programs for the prevention of CVD and DMD. in
221133557 2017 The Authors Published by Elsevier Ine This a open aces ate unde the CCBY-NCND lense (hp teavecomsnonsrgcenssy-ne-ndi40)8 Trea Prose Meer 6 (2017) 27-22
adulthood, Thus, the aim ofthis stady sto identify the prevalence of RF
to MetS and its association with nutritional stats in schoolchildren
from 6 to 10 yeats ol in the city of Macae, Bazi,
2. Methods
2.1, Study design and sample population
‘This investigation was 2 cross-sectional study conducted from
March 2013 to November 2014 in schoolchildren (6-19 years)
fom public schools in the city of Macae, located in the state of Rio
de Janeiro, Brazil, with 1219.8 kn of area and about 217,000 inhab-
itants thas the petroleum as main economic activity, being the low
social class prevalent among schoolchildren of municipal schools.
The city is divided into $ administrative sectors, with $2 schools
and 10,247 schoolchildren (6-10 years). For the reference popula-
tion, by logistical issues, it was selected one school of ezch sector, to-
taling 1553 schoolchildren, who were invited to participate. A simple
dora sample size was carried based on the national prevalence of
‘obesity in the study age group (142%) (IBGE, 2010), 95%CI, maxi-
mum error 2.5% and the population (1553). The final sample size
‘was 502 schoolehildren,
‘The exclusion criteria were: children whe had physical impair-
‘ment that prevented the evaluations, wth diabetes mellitus and/or
hypothyroidism and/or use of medications that could interfere in
‘the results, OF the 1553 schoolchildren, one was exclude due to
‘dwarfism, Were not authorized for biochemical examination 936
schoolchildren. The total of children evaluated in all parameters
‘was 505 (Fig. 1),
22, Data collection
Data were collected in schools under the supervision af responsi-
ble research including: body weight, height, WC, BP and biochemical
L oa
|
05221 males 26 en
ig 1. Fw chartof the study sample cre ag 6-10 years Naa, rl, 2013/14
‘examination, Te team that carried out the collection was properly
trained,
23, Anthropometry
Body weight and height were measured in duplicate according to
the technique proposed by Lohman etal. (1988), through electronic
and portable scale Tanita® platform (linois, USA) with capacity of up
to 150 kg and range of 50g and anthropometer Height Exataw® (Minas
Gerais, Brazil) with 20.1 cm, The children were evaluated with light
clothing without shoes and without headdress. The value ofthe average
‘ofthe two measurements was used to calculate body mass index (BMI)
in kg/m’. The schoolchildren were classified in four categories: under-
‘welght, normal weight, overweight and obese by 2-score as the criteria
proposed by WHO (2007).
‘Waist circumference (cm) was measured atthe midpoint between
the last rib and the upper edge of the iliac fest as recommended by
‘WHO (2014) in duplicate and the average of the measurementswasca-
culated, It was considered excess abdominal fat WC value above the
‘0th percentile according to sex and age (Maffes et al, 2001), obtained
from the sample data that consists of all schoolchiléren who had WC
measured (Dias etal, 201
24. Blood pressure
The procedures for measuring BP of the schoolchildren were
based on the guidelines of the Brazilian Society of Cardiology
(SBC, 2005), without having done exercise for an hour before the
procedure and after § min of rest, sitting, reclining in chair and legs
‘unerossed, It used validated digital equipment OMRON HEM-705
(cP (G-Tech International- Republican of Korea) and the cuffs
‘were adequate to arm size. The measurements were performed in
éuplicate and with an interval of 2 min between them. To classify
the PA was considered the average value of the measures. The cuto
point used were the suggested by the Brazilian Society of Cardiology
(high BP 295 percentile for age, sex and height percentile for age)
($8, 2008),
2, Biochemical measurements
Avenous blood sample was collected overnight past 12h, To make
sure about fasting it was sent tothe children's parents a reminder the
day before the procedure, It was also requested a signed confirmation
of fasting state ofeach chi delivered atthe time of biochemical analy-
sis. Approximately 10 mL blood sample was collected and centrifuged
for 5 min. Then, the samples were placed in coolers and transported
‘within a maximum of 2h tothe laboratory where they were frozen
for later analysis. They were analyzed by enzymatic colorimetric meth-
(od, kit LABTESTB: Glucose (mmol), HDL-c (mmol) and triglveerides
(16) (mmol)
For classification, were use the cutoff points suggested by the Bra-
zillan Society of Cardiology (SBC, 2005): HDL-c (<1.16 mmol/l), TG
(21.13 mmol) and fasting glucose was use to reference the Brazilian
Society Diabetes (SBD, 2016) of >5.55 mmol/l. The diagnosis of Mets
‘was based on the concurrent presence of three or more of RF cited as
citeria proposed by the NCEP-ATPII (Grundy etal, 2004) with cutof
points adapted forthe child population
26, Ethical aspects
The study was approved by the Research Ethics Committe of the
University Veiga de Almeida (Number: 875333) and authorized by the
‘Municipal Department of Education ofthe cty of Macae Ro de Janeiro
and the direction ofeach participating school, Parents or guardians in-
terested in their children’s participation inthe study signed the freeTrea / Prose Miner 2017 27-22 2
and informed consent, At the end ofthe investigation, participants re-
‘ceived individual results oftheir assessments
27, Statistical analysis
The mean and standard deviation were calculated for continuous
variables and frequencies of categorical variables and their respective
195% confidence interval (95%C1) Quantitative variables were compared
by sex using a Student's t-test for independent samples. For the associ-
ation between RF and nutritional status and gender, Chi-square and
Fisher's Exat tests were used. p value <005 for statistical significance
‘was considered fr all analysis. Data analysis was performed using the
Statistical Program forthe Socal Sciences, version 21.0 (SPSS, Chicago,
i)
3. Results
The sample included 505 schoolchildren, 221 (43.8%) boys and 284
(56.2%) gies. Anthropometric, B and biochemical data are presented
in Table 1. There was no gender difference in any ofthe parameters
evaluated,
‘Amongihe schoolchildren, 14 (2.8%), 312 (61.8%), 85 (168%) and 94
(186%) had underweight, normal weight, overweight and obesity, re-
spectively, At least one RF included in the diagnosis of MetS was present
in 308 (61%) children. The prevalences of RFin the total sample accord
ingto sex and nutritional status are shown in Table 2. The underweigh
schoolchildren were excluded from the analysis for nutritional status
‘due tothe reduced number of RF in this group.
Hypertrglyceridemia was the most prevalent RF, observed in 283%
(= 148) ofthe sample. The low HDL-<, more prevalent in males than
in females, wasthe only RF that showed a significant difference between,
Sexes (p = 0.03), and was not associated with nutritional status (p =
(043). For other BF in schoolchildren, overweight andjar obesity had
higher prevalence rates compared to normal weight (p < 005) (Table
2}
‘There were 175 (34.7%), 105 (21,08) and 27 (53%) schoolchildren
‘ith one, two and three or mare RE (MetS), respectively, without dffer-
lence between the sexes, According to the nutritional satus, there was
no significative difference between the prevalence of one RF (p =
(0.085) and significative diference was observed between 2,3 orm
RE (p< 000%) (Table 2)
‘Toe concomitant presence of two RF was higher in overweight cil-
‘dren and obese children compared to those with normal weight Three
‘or mare RF (MetS) were moze prevalent among obese in relation to
‘overweight and normal weight (Fig.2)
aber
(sos) (eae (es 2
‘ge Gea) Teri 79210 7x10 040
Ce) tess asa eea3s Om0
wetem) bi9i91 Gigaea Gisa0s On
Cheemia (mmol) 4732079 475209 478082 O51
Tetmmolt) Oa i047 Gap 204s Osrzode O15
SePiemis) 107283 1057 281 én
Deo(mm ie) 673077 S227 on
4 (Body Nass den) WC ast creer) 6 (ulyeees) HDL HDL ces
‘er BP sy Blood presize).BP(@asolc bed pestze)
Inthe present study conducted in Brazian children, at least one RF
{or MetS was identified in more than half ofthe sample, Ie was shown
‘that obese children have the highest prevalence of WC, and high
[BP in relation to normal weight, as well 2s WC and high BP relative to
‘overweight. The concomitant presence of two RE was higher in over-
‘weight/obesty children, and three or more among obeses. Therefore,
this study demonstrates the association of nutritional status of children
withthe RFthat contributes to Met.
Studies in difleent countries also demonstrate the occurrence of BF
for CVD and DMB2 in children, especially among the overwreight/obese
‘ones (Adair etal, 2014; Freedman etal, 2007; Folst-Schumacher et
al, 2009; "Allemand etal, 2008; Kuschnir etal, 2016; Rosin et al.
2015; Seki et al, 200%; Van Vliet etal, 2009). In children born after
‘the 2000s, obesity was abserved tobe three times prevalent as com-
pared to those ofthe same age born inthe 80's (Gupta, 2015; Marie et
al, 2014), Despite being stabilize in some countries, the prevalence
of obesity remains high (Dietz and Economos, 2015; Ogden et al
2016). In Brazil, the ast national survey data showed overweightobes
{y in 33.5% of children aged 5 to 9 years of age. Obesity was present in
16% ofthe girls and 11.8% ofthe boys (IBGE, 2010), igh BMI in child
hood is related to metabolic changes, including changes inthe lpi pro-
file, BP elevation and insulin resistance (Abrams etal, 2011; Han eta.
2010; Freedman etal, 1999). In this sense, the high prevalence of over~
‘weight/abesity observed inthis study may explain, in part the frequen-
cy of Fin the sample,
Associated with the occurrence of obesity or overweight diagnosed
by BMI itwas shown the prevalence about 60% of excess WC among
‘obese, which was compatible with other national studies such as
‘those conducted by Ricco etal. (2010) and Preto et al. (2015) who ob-
setved, respectively, 50% and 84,7&excess WC among obese ehilden, ln
study conducted in Turkey in about 4000 schoolchildren, excess WC
‘was also observed in those with high BMI (inane, 2014). Although its
nota consensus in children, it has been shown that excess abdominal
fat, estimated by WC, is beter predictor of metabolic alterations com-
pared with BMI (MeCarthy, 2006), that can indicate the impact of the
istribution of body fat in the cardiovascular risk (Goran and Gower,
1999; Spolidoro etal, 2013) There is no universal cutoff point for WC
associated to cardiometabolic RF, butit has been suggested that children
‘with a WC > 80th percentile are at higher risk of having multiple cardio-
‘metabolic RF than those with lower WC percentiles (Maffels et al
2001). Considering the lack of such reference curves in Brazile cassi-
Sication of risk in this study was WC > 90th percentile according to
values ofits sample, Despite the difficulty in comparing with other stud-
Jes, the results showed excess of cental adiposity, with posible reper-
cussions onthe heath of these children.
-Hypertriglyceridemia and low HDL-< were the most common abnor-
‘mal biochemical parameters a5 observed by Tavares etal (2010) in a
systematic review of MetS in Brazilian children and adolescents
Rosiniet al, (2015) also identified a high prevalence ofthese RFbetween
Brazilian schoolchildren 6-14 years old. The process of atherosclerosis
‘may begin in childhood (Amaiz et al. 2013; Magnussen etal, 2014)
and is associated with changes in lipid profile, including the rise of
low-density cholesterol and T (Berenson etal, 1998), andthe low con-
centration of HDL-c, wich is also included in Met's diagnosis (Ford and
1K, 2008). In 2 26-year cohort study with 770 schoolchildren from
5 yeats old, Morrison etal. (2012b) observed that children with perss-
{ent hypertriglyeeridemia from childhood to adulthood had a higher
prevalence of CVD compared to those without this RE
‘According tothe nutitonal status, there was no difference in prev=
lence in low HDL concentration, corroborating to Perera el, (2009)
in a Brazilian study. Moreover, hypertriglyceridemia was higher in
‘obese than normal weight children, as reported by Seki etal (2001)
and Inanc (2014) in Brazilian and Turkish schoolchildren respectively
Data from large longitudinal studies such asthe Bogalusa Heart Studyx0 Pe Tate Preven Mi Report 6 2017) 27-32
able?
Prove of metabo isk ator or table syndrome scaking apne nd ins as ia len aged 6-10 es, Macs ea 2013/14
a Se ro
we 2m nce
tel ss sxc
Wate Female Nomalweait —Ovewaat Obs
(wn zy tm 284) pale n= 312) (ees) Gent) pale
Raktactr
acess WC fm) secs) e027) s0cins) as 103) 102) 5695) <0001
yperiicerdemia 48283) 0271) 8308) ass 75 (240) wa = ear) <0
waesss aS Bete? iaueon2 dots? aes
Lon OL t3@e3) G2) aa) 751240) aaGns) 26075) a
ign 068) 39075) aanss) ast 23193) w6cs8) 3793) «oom
wis eas sen02 ba-n30 sieae7 254400
yperaeemia an is) Aas) 08 70) Busy iat) or
Nmber ok fctore
‘ik aor mea G7) aaa a 11588) sagsss) 254245) ass
2 rk tacoe osieis) 3025) 5197) 2033) pasa) 394415) 45,000 children of different ethnic groups and
identified increased risk of high BP as increased BMI, regardless of sex,
ace or age. In a systematic review of HAS in Brazllan schoolchildren
aged 6 fo 10 years, Pereira et al. (2015) showed higher prevalence in
‘overweightéobese children and highlighted the association between mu-
‘wtional status and che BP values. However, o consolidate the diagnosis
‘ofHAS in children itis necessary thatthe BP average i above the cuto
established in at least three days (SBC, 2005). In this sense, the results
shouldbe interpreted only asa risk. Nevertheless, the high prevalence
ofthis RF in the study group is relevant, cansidering that BP values
can be elevated since their childhood and it can also be related to arte-
‘al stiffness and HAS in adults (i etal, 2004; SBC, 2005)
The insulin resistance (IR), other RF associated with Mets results in
hyperglycemia, what is a Fisk for the development of DM2 (junior
RF ORF
Sor #RF
Number of risk factors
‘snormalweght overweight obesity
Eu tn)
pelos ecm nema wee
Wp oy manatee
e001 ey nee
ig 2 Prevalence (of numbe fiat or dane of metalic some by nuttional status ince ar 6-10 years Maza, rz 200314eT etal/Peeve Men Report 6 2017) 27-32 n
Montenegro etal, 2013).The IR during cilchood and adolescence cor-
responds toa cardiovascular RF independent of the DM2 development
and is associated with the increased rate of cardiovascular events in
adults (Steinberger et al, 2009). Hyperglycemia, parameter used
in the study to evaluate the glucose metabolism, was preseat in 8.7%
‘ofthe sample, and it has been also the less frequent RF in other invest-
gations (Seki etal, 2001; Weiss et al, 2004). However, the prevalence of
hyperglycemia among overweight/obese children was twice higher
‘compated to normal weight, showing the association between excess
‘weight and changes in glucose metabolism (Dias et al, 2014; Han et
al, 2010; Morrison eta, 20128}.
Except forthe reduced HDL-« concentration, more in boys than in
irl, there was no difference inthe presence of RF to sex. Seki eta
(2001) ina study of Brazilian schoolchléren and Paula et al (2015) in
Pediatric patients in clinical nutrition have not identified differences in
RF to sex. However, ina systematic review conducted by Friend et al.
(2013) the RF of MetS were more present among boys compared to
airls. The early age range of the schoolchildren in this study suggests
that most have not entered puberty, a period in which the differences
between the sexes are more evident, possibly with greater impact on
the evaluated parameters (SBC, 2005},
Three or more RF were seen in 5.2% of the sample, higher than that
‘observed by Seki et al, (2001) in Brazilian schoolchildren aged 6 to
‘years of age (3:28). However, the prevalence was lose to the average
‘of te most recent systematic review of MetS in children alsa identified
by NCEP-ATPII adaprations (4.2%) (Friend etal, 2013). It must be em-
phasized that, regardless ofthe Ms, the concomitant presence of RF
‘was present in approximately 26% of the schoolchildren. Loureiro eta
(2015) identified in Chilean children and adolescents progressive in-
‘crease in caiovascular risk including inflammation of the endotheli-
um, asthe presence of each RE. Barja et al. (2008) and Amnaiz etal
(2013) complemented these findings by identifying the individual ca-
rotid intima thickening in the co-occurrence of RF in children. The re-
sults ofthis study indicated the presence of associated RF, which may
promote physiological changes, independent of MetS'diagnosis
(Berenson et al, 1998)
‘The presence of two RF was higher among overweight/obese chil-
«dren compared to normal weight and three or more RF among obese
‘compared with others. The daca corroborate the literature and suggest
that overweight/obesity and its magnitude may increase the risk of
the association of RF, hence the presence of metabolic disorders
(Griend etal, 2013; [Allemand et al, 2008; Rosni eal 2015),
‘There was no difference in having one RF by nutritional status. It
shows that even those with adequate weight have already one RF. Be
sides the excess weight, REsuch as high BP, hyperglycemia ow HDL-<
may be associated with genetics, physical activity level, die, birth
‘weight, among others (Loureiro et al, 2015, Weiss et al, 2004). In this
Sense, studies have also demonstrated RF in normal weight children
(Seki et al, 2001; Dias et al, 2014),
Noteworthy, the early treatment of metabolic RF and averweight/
‘obesity does not imply a worse prognosis for CVD in adulthood when
‘compated to those who never had such complications (Magnussen et
al, 2014), Moreover, the persistence ofthese RF into adultinood relates
to the substantial increase cardiovascular risk (Magnussen et al,
2014). In this sense, once overweight/abesity o the presence of any of
the RF of MeS is identified. immediate intervention strategies as nutri-
tion education, regular physical exercise in addition to more active be-
havior in daly activities are suggested, regardless of the diagnosis of
MetS (Paienza et al, 2016; Magnussen et al, 2013; Owens and
Gallowey, 2014)
‘Although previous studies have demonstrated the presence of RFin
the pediatric population, the present study demonstrates in early ages
not only the RF, but also the concomitant presence of two or more RF
for MetS' and is association with nutritional satus, investigations that
are scarce in Brail (Seki eta, 2001; Rsini etal, 2015). In this sense,
itmay contribute tothe gap in the literature in developing countries,
especially in Brazil However our findings should be interpreted consi¢-
ering its limitations. Athough using cutoffs of different RF previously
advocated for child population, they donot always represent consensus
resulting in the lack of standardization between different studies.
‘Whereas the result of prevalence of RF depend, among others, on the
values established by diferent researchers, the interpretation and com-
parison ofthe occurrence of the different parameters become difficult
(an Vliet etal, 2011). In alton, the parameters evaluated as RF are
influenced by the behavior, genetics, ethnicity and may have more sig-
nificance than others depending onthe population studied (Loureiro et
Al, 2015). inthis sense, the data in ths specific group of children may
nat represent other groups even if they are the same age and nationality
and should not be extrapolated
5. Conclusions
The data indicated high prevalence of RF of MetS among
schoolchildten, mainly influenced by nutritional status. The potential
‘impact of excessive body weigh in the concomitant presence of RF and
its magnitude in the presence of three or more RF observed in the
study reinforce the importance of prevention and treatment of over-
‘Wielghtobesity in order to reduce the ikelnood of MetS and related is-
cases in adults
Financial support
This work was supported by the Foundation of Research Suppor of
the State of Rio de Janeiro (FAPER) number E-26/110,487/2010), Na-
tional Counsel of Technological and Scientific Development (CNPQ
number 19011),
Conflict of interest
None declare.
‘Authors’ contributions.
Study concept and design: BGR Acquisition of data: FC, EPP. Anal-
ysis and interpretation of data: BGR, AFP, FCT, FDP. Drafting ofthe
‘manuscript: CT, FPP, Critical revision ofthe manuscript: BGR, AFP.
Funding acquisition: BGR. Study supervision: BC.R. All authors read
and approved the fina version ofthis manuscript.
Acknowledgments
Te authors thank Professor Dr Roni Ragio (Postgraduate program
in public health at the Federal University of Rio de Janeiro) for his
assistance with statistical analysis, Dr. jackson de Souza Menezes and
Dr. Anderson Morales for biochemical analysis. We also thank the
‘Municipality of Macae (Municipal Department of Education and the
‘Municipal Health Department) for permission to access the schools
and technical support, respectively
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