Epidemiology and In ec ion
camb idge.o g/hyg
O iginal Pape
Ci e his a icle: Fan Y-M, Oika inen S, Leh o
K-M, Nu minen N, Juu i R, Mangani C, Male a
K, Hyö y H, Asho n P (2019). High p e alence
o selec ed i uses and pa asi es and hei
p edic o s in Malawian child en. Epidemiology
and In ec ion 147,e90,1–9. h ps://doi.o g/
10.1017/S0950268819000025
Recei ed: 6 No embe 2017
Re ised: 16 Decembe 2018
Accep ed: 1 Janua y 2019
Key wo ds:
In ec ion; pa asi e; p edic o ; p e alence; i us
Au ho o co espondence:
Y.-M. Fan, E-mail: [email p o ec ed]
© The Au ho (s) 2019. This is an Open Access
a icle, dis ibu ed unde he e ms o he
C ea i e Commons A ibu ion licence (h p://
c ea i ecommons.o g/licenses/by/4.0/), which
pe mi s un es ic ed e-use, dis ibu ion, and
ep oduc ion in any medium, p o ided he
o iginal wo k is p ope ly ci ed.
High p e alence o selec ed i uses and
pa asi es and hei p edic o s in
Malawian child en
Y.-M. Fan1, S. Oika inen2, K.-M. Leh o1, N. Nu minen2, R. Juu i3, C. Mangani1,4,
K. Male a4, H. Hyö y2and P. Asho n1,5
1
Cen e o Child Heal h Resea ch, Tampe e Uni e si y, Facul y o Medicine and Heal h Technology and Tampe e
Uni e si y Hospi al, Tampe e, Finland;
2
Depa men o Vi ology, Facul y o Medicine and Heal h Technology,
Tampe e Uni e si y, Tampe e, Finland;
3
EPID Resea ch Oy, Espoo, Finland;
4
College o Medicine, Uni e si y o
Malawi, Blan y e, Malawi and
5
Depa men o Paedia ics, Tampe e Uni e si y Hospi al, Tampe e, Finland
Abs ac
En e ic pa hogens ha e been ela ed o child unde nu i ion. Whe eas he e a e lo s o da a on
en e ic bac e ial mic obio a and in ec ions, much less is known abou he incidence o p e a-
lence o in es inal colonisa ion wi h i uses o impo an pa asi ic species. This s udy assessed
he p esence o selec ed i uses and pa asi es in s ools o 469, 354, 468 Malawian child en a 6,
12 and 18 mon hs. We also assessed en i onmen al p edic o s o he p esence o i uses and
pa asi es among 6-mon h in an s. Mic obial p esence was documen ed using eal- ime poly-
me ase chain eac ion (PCR). En e o i uses we e iden i ied in 68%, 80% and 81% o he s ool
samples a 6, 12 and 18 mon hs child en, hino i us in 28%, 18% and 31%, no o i us in 24%,
22% and 16%, pa echo i us in 23%, 17% and 17%, o a i us in 3%, 1% and 0.6%, Gia dia
lamblia in 9.6%, 23.5% and 26%, and C yp ospo idium (spp.) in 6%, 8% and 2% o he 6,
12 and 18 mon hs s ool samples. D y season (May–Oc obe ) was associa ed wi h a low in ec-
ion a e o en e o i us, no o i us and C yp ospo idium (spp.). Highe a he ’s educa ion le el,
less numbe o pe son in he household and highe sani a ion we e associa ed wi h a low
in ec ion a e o en e o i us, no o i us and o a i us, espec i ely. The esul s sugges ha
he p e alence o asymp oma ic i al and pa asi ic in ec ions is high among Malawian chil-
d en and ha he amily’s li ing condi ions and seasonali y in luence he a e o in ec ions.
In oduc ion
S un ing, de ined as child en’s leng h- o -age o heigh - o -age, is mo e han wo s anda d
de ia ions below he Wo ld Heal h O ganisa ion (WHO) Child G ow h S anda d median.
Globally, i is es ima ed ha 165 million child en younge han 5 yea s we e a ec ed by s un -
ing in 2011. The p e alence has been dec easing du ing he pas decades, bu is s ill high in
Sub-Saha an A ica and Sou h Asia (36% and 27%) [1]. In childhood, s un ing is associa ed
wi h an inc eased isk o mo bidi y and mo ali y as well as delayed men al and mo o de el-
opmen [1]. Impai ed ea ly childhood unde nu i ion in u n has been associa ed wi h lowe
educa ional achie emen , lowe adul p oduc i i y and ea ning po en ial [2].
The mos common cause o s un ing is belie ed o be esul s o inadequa e die a y in ake,
equen in ec ions o combina ion o bo h. In ecen yea s, en i onmen al en e opa hy, also
known as en i onmen al en e ic dys unc ion (EED), has been s udied as ano he possible
cause [3,4]. This condi ion is cha ac e ised by in es inal in lamma ion, di use illous a ophy
and impai ed nu ien abso p ion and g ow h. I is belie ed o ha e an in ec ious o igin [5],
bu nei he an ibio ic no p obio ic ea men seems o modi y i s cou se [6,7]. Vi al and pa a-
si ic in ec ions would no be a ec ed by an ibac e ial in e en ions bu hey do cause in es inal
in lamma ion esponse [8,9]. Fu he mo e, whole- ansc ip ome analysis om Malawian chil-
d en wi h a ying s a es o EED showed ha 57% ansc ip s wi h inc eased exp ession in EED
we e epo ed o espond o i al in ec ion [10]. Vi al o pa asi ic in ec ions o he gas oin es-
inal ac a e also o en common bu asymp oma ic [11–18]; o ins ance, in a pilo s udy o 44
6-mon h-old in an s in u al Malawi, we de ec ed en e o i al RNA in 50% o he es ed s ool
samples [19]. The s ool samples we e collec ed as pa o he same in e en ion ial as he
cu en s udy. Gi en all hese indings, i seems plausible ha asymp oma ic in es inal i al
o pa asi ic in ec ions would be con ibu ing o EED.
To ge a mo e comp ehensi e pic u e o he equency o in es inal i al o pa asi ic in ec-
ions among child en in a low-income se ing, we de e mined he p e alence o i e i uses-
en e o i us, no o i us, hino i us, pa echo i us, o a i us and wo pa asi es –Gia dia lamblia
and C yp ospo idium species in s ools om 6, 12 and 18 mon hs Malawian child en. We
ocused on hese pa hogens because hey a e widely sp ead and e lec he hygienic condi ions
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whe e he child en a e li ing. As an a emp o iden i y po en ial
a ge s o p e en i e in e en ions, we also sough o iden i y
majo en i onmen al o socio-demog aphic p edic o s o being
in ec ed wi h selec ed i uses o pa asi es among 6-mon h in an s.
Me hods
S udy design, s udy subjec s and e hics
This s udy was a c oss-sec ional s udy using da a and s ool sam-
ples ha we e collec ed om u al Malawi. The 6-mon h in an s
we e ec ui ed o a clinical die a y supplemen a ion ial be ween
Janua y 2008 and May 2009, a ha poin we examined he
in an s, in e iewed hei gua dians and collec ed and s o ed a
s ool sample om hem. The in an s we e ollowed up o 12
mon hs and s ool samples we e also collec ed when hey we e
12- and 18-mon h-old.
De ails o his ial, designa ed Lungwena Child Nu i ion
In e en ion S udy (LCNI-5), ha e been desc ibed elsewhe e
[20]. In b ie , he s udy popula ion comp ised 840 6-mon h-old
in an s, who we e en olled o a clinical ial assessing he e ec
o die a y supplemen a ion wi h lipid-based nu ien supplemen s
o 12 mon hs on ea ly childhood g ow h ( egis a ion ID:
NCT00524446, a h ps://clinical ials.go /). This ial was con-
duc ed in Lungwena and Malindi, wo u al Malawian communi-
ies. Malindi is abou 17 km om Mangochi own and had on
a e age be e access o elec ici y, clean wa e , sani a ion and mis-
siona y hospi al and a mo e educa ed popula ion han Lungwena,
a mo e u al si e abou 32 km om he own. Bo h a eas a e along
he sho es o Lake Malawi, Malawi. (Fig. 1).
The ial adhe ed o he p inciples o he Decla a ion o
Helsinki and egula o y guidelines in Malawi. W i en in o med
consen was ob ained om he pa icipan s’gua dians and he
ial p o ocol was e iewed and app o ed by he College o
Medicine esea ch and e hics commi ee (Uni e si y o Malawi)
and he e hical commi ee o he Pi kanmaa Hospi al Dis ic ,
Finland.
Specimen collec ion, da a collec ion and s o age
All s ool samples we e collec ed wi hin 14 days a e he en ol-
men . The gua dians o he ial pa icipan s we e gi en a con-
aine o collec he s ool samples om he pa icipan s, and
hey b ough he sample o he heal h cen e a e wa ds. We col-
lec ed da a wi h pic u e calenda eco ded by ca e ake (gua d-
ian). Th oughou he s udy, he gua dians we e asked o eco d
on a daily basis he p esence o absence o illness symp oms in
pic u e calenda s ha we e p o ided e e y 2 weeks. The calenda
had sepa a e ows o di e en days up o 2 weeks and sepa a e
columns o he ollowing symp oms: (1) e e ; (2) cough; (3)
dia hoea (≥3 s ools/d); and (4) o he . The i s 3 symp om col-
umns had pic u es desc ibing hem o assis he gua dians in
iden i ying he co ec a ea o eco d he in o ma ion. The gua d-
ian epo s on he calenda s did no include he eco ding o em-
pe a u e o e e o he numbe o s ools o dia hoea. The
eco ded in o ma ion was e iewed and c oss-checked by ield-
wo ke s a each 2 weekly ood-deli e y isi o comple eness.
Those pa icipan s ca ying he pa hogens bu did no ha e illness
symp oms and looked ‘heal hy’ om hei ca e ake s’ iews com-
p ised ou s udy subjec s. F om he in o ma ion we collec ed a
en olmen , 31 child en had dia hoea in he las 14 days, 22 du -
ing he las 7 days and 11 in he las 2 days. The pa hogen
in ec ions we e iden i ied by PCR om s ool samples collec ed
a 6, 12 and 18 mon hs.
Time be ween de eca ion and s ool eezing was ypically 1–
3 h, maximally 6 h. Abou 1 g s ool sample was aliquo ed by a
labo a o y echnician o a sc ew cap collec ion ube. The samples
we e s o ed o a maximum o 1 week a −20 °C in he s udy si e,
2–4 yea s a −40 °C a a cen al labo a o y in Mangochi and 2–7
mon hs a −80 °C a he Uni e si y o Tampe e whe e he analysis
was done. The sample shipmen om Malawi o Tampe e ook
place in d y ice.
Sample p epa a ions, nucleic acid ex ac ion and
eal- ime PCR
F ozen s ool samples we e hawed and p ocessed in o 10% (w/ )
suspension in HANKS medium con aining 0.2% BSA. Nucleic
acids we e isola ed using QIAamp Vi al RNA Mini Ki (Qiagen,
Hilden, Ge many) om he 10% aecal suspension and eal- ime
PCR was used o de ec en e o i uses, hino i uses, no o i uses,
pa echo i uses and o a i uses [21,22] as well as Gia dia lamblia
and C yp ospo idium (spp.) pa asi es as p e iously epo ed [23].
The p ime s and p obes used o PCR we e shown in supplemen-
a y Table S1. Fo each pa hogen, we an h ee imes PCR and
posi i e was iden i ied i PCR we e posi i e a wo o h ee imes.
Collec ion o backg ound in o ma ion and labo a o y es s
The da a on pa icipan s’socioeconomic backg ound we e col-
lec ed h ough pe sonal in e iews du ing en olmen . A en ol-
men , he pa icipan s’blood haemoglobin concen a ion was
also measu ed om a enous sample using cu e es and a eade
(HemoCue AB, Angelholm, Sweden). Mala ia was diagnosed
mic oscopically om Giemsa s ained hick and hin blood
ilms. Each smea was ead by wo independen mic oscopis s
and disco dan esul s we e e- ead by a hi d mic oscopis .
An h opome ic measu emen s
An h opome ic measu emen s we e ca ied ou by h ee ained
esea ch assis an s du ing he en olmen isi . Unclo hed in an s
we e weighed using an elec onic in an weighing scale (SECA
735; Chasmo s L d, London, England) and weigh s we e eco ded
o he nea es 10 g. The leng h was measu ed o he nea es 1 mm
using a high-quali y leng h boa d (Kiddime e; Ra en Equipmen
L d, Essex, England). An h opome ic indices (weigh - o -age Z
sco e = WAZ, leng h- o -age Zsco e = LAZ and weigh - o -leng h
Zsco e = WLZ) we e calcula ed using WHO Child G ow h
S anda ds (2010 STATA ig owup package) [24]. Age o all pa i-
cipan s was e i ied be o e en olmen objec i ely by c osschecking
documen ed bi h da es in heal h passpo s and unde - i e ca ds.
S a is ical analysis
P opo ions, means and s anda d de ia ions (S.D.) we e compa ed
be ween g oups by using S uden ’s es o con inuous a iables
and Fishe ’s exac es o p opo ions. F equencies we e used o
de e mine he p e alence o i uses and pa asi es. Bi a ia e ana-
lysis was used o de e mine he associa ion be ween po en ial p e-
dic o s including age, sex, g ow h indexes, age o he main
gua dian, numbe o pe sons and child en <5 yea s o age in
household, pa en s’educa ion le el, socioeconomic s a us, num-
be o animals in he house, anaemia, mala ia, sou ce o d inking
2 Y.-M. FAN e al.
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wa e , household sani a ion (la ine), si e (Lungwena o Malindi),
seasonali y (d y o ainy season when s ool samples we e col-
lec ed) and p esence o i uses and pa asi es. Those p edic o s
ha we e ound o be a he P< 0.1 le el we e included in he
mul i a ia e logis ic eg ession model. Age, sex, socioeconomic
s a us and numbe o animals in household we e o ced in o
he model since hey ha e been ound o be signi ican in he li -
e a u e and a e po en ial con ounde s [25–27]. Odds a ios wi h
95% CI we e used o measu e he associa ion be ween p edic o s
and p esence o i uses and pa asi es a s a is ical signi icance o
P< 0.05. S a is ical analyses we e pe o med using S a a 13.1
(S a a Co p, College S a ion, TX, USA).
Resul s
Cha ac e is ics o s udy subjec s
O he 840 LCNI-5 ial pa icipan s, we had 506 s o ed s ool
samples om 6-mon h in an s. Among hem, 37 we e ound o
ha e dia hoea a sample collec ion day and we e excluded om
his s udy. The e we e 11 in an s who had dia hoeal du ing he
pas 2 days when he samples we e collec ed. Howe e , hese pa -
icipan s we e included in he s udy subjec s. S ool samples o 354
and 468 child en we e a ailable a age o 12 and 18 mon hs,
espec i ely (Fig. 2). A 6 mon hs o age, he mean LAZ, WAZ
and WLZ o hese pa icipan s we e −1.65, −0.79 and +0.45,
espec i ely. App oxima ely 13% o hem had mala ia pa asi -
aemia in hei blood. In an s who pa icipa ed in he main
in e en ion ial bu we e no included in his sub-s udy we e
on a e age simila o he included ones, excep ha hey we e
sligh ly olde and less o en en olled om Lungwena heal h cen e
(Table 1).
P e alence o i uses and pa asi es in s ool samples
A o al o 320 (68.2%), 284 (80.2%) and 380 (81.2%) o he s ool
samples con ained en e o i al RNA a 6, 12 and 18 mon hs, espec -
i ely. Rhino i us was de ec ed in 130 (27.7%), 65 (18.4%) and 146
(31.2%) samples; no o i us in 110 (23.5%), 79 (22.3%) and 74
(15.8%); pa echo i us in 106 (22.6%), 60 (17%) and 77 (16.5%);
and o a i us in 15 (3.2%), 4 (1.1%) and 3 (0.6%) samples om 6,
12 and 18 mon hs, espec i ely (Table 2). A o al o 45 (9.6%), 83
(23.5%) and 123 (26.3%) samples we e posi i e o Gia dia lamblia
and 30 (6.4%), 28 (7.9%) and 9 (1.9%) o C yp ospo idium (spp.)
om 6, 12 and 18 mon hs, espec i ely (Table 2). A leas one
i us o pa asi e was de ec ed in 414 (88.3%), 317 (89.5%) and
418 (89.3%) s ool samples a 6, 12 and 18 mon hs. Two o mo e
mic obes we e de ec ed in 234 (49.9%), 188 (53.1%) and 262
(56%) and h ee o mo e mic obes in 86 (18.3%), 72 (20.7%) and
105 (22.4%) o 6, 12 and 18 mon hs samples.
We also used C alues o classi y in ec ions as low (C ⩾36),
median (30 ⩽C ⩽36) and high (C < 30) le els. The p e alence
o mic obes is highes in high in ec ion le els in mos o he
i uses excep hino i us in which he low in ec ion le el is he
highes (da a no shown).
Fig. 1. Map o s udy si es (Lungwena and Malindi). Sou ce: Da a laye o A ica map downloaded om h p://www. hema icmapping.o g, 2015 a ailable unde a
C ea i e Commons A ibu ion-Sha e Alike License 3.0 (bo de s may no be comple ely accu a e). All o he da a laye s downloaded om Malawi Spa ial Da a Po al,
2015 (h p://www.masdap.mw).
Epidemiology and In ec ion 3
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P edic o s o i al and pa asi ic in ec ions a 6-mon in an s
In bi a ia e analyses, en e o i us posi i i y in he s ool samples was
signi ican ly associa ed wi h sani a ion (no household la ine use),
si e (li ing in Lungwena), lowe le el o mo he ’s and a he ’s educa-
ion and ainy season (Table 3). In mul i a ia e analysis, seasonali y
and a he ’s educa ion le el emained signi ican ly associa ed wi h
en e o i us posi i i y (Table 3). In an s whose a he had a highe
le el o educa ion we e less likely en e o i us posi i e han hose
whose a he had a lowe le el o educa ion (OR 0.94, 95% CI
0.89–0.99, P= 0.031). In an s whose sample was collec ed du ing
he d y season (May–Oc obe ) we e less likely o be en e o i us posi-
i e han hose whose sample was collec ed du ing he ainy season
(No embe –Ap il) (OR 0.65, 95% CI 0.43–0.99, P=0.045)
(Table 3). Agewas associa ed wi h hino i us in ec ions in mul i a i-
a e analysis. Olde in an s we e less likely hino i us posi i e han
hose young in an s (OR 0.43, 95% CI 0.19–0.99,P= 0.046) (Table 3).
The esul s o no o i us, pa echo i us and o a i us a e shown in
Table 4. In bi a ia e analysis, he numbe o pe sons in he household,
mo he ’s educa ion le el, a he ’s educa ion le el, anaemia and ainy
season we e signi ican ly associa ed wi h no o i us p esence.
Anaemia was associa ed wi h pa echo i us in ec ions and lowe
le el o sani a ion (household la ine use) was associa ed wi h o a-
i usin ec ions (Table 4). In mul i a ia e analysis, numbe o pe sons
in he household and seasonali y emained signi ican ly associa ed
wi h no o i us p esence; and sani a ion wi h o a i us p esence.
The mo e pe son li ing in he house, he mo e likely in an s we e
o ha e no o i us in ec ion (OR 1.16, 95% CI 1.02–1.31, P=0.024).
In an s whose sample was collec ed du ing he d y season (May–
Oc obe ) we e less likely no o i us posi i e han hose whose sample
was collec ed du ing he ainy season (No embe –Ap il) (OR 0.53,
95% CI 0.32–0.86, P= 0.01). In an s whose home did no ha e la ine
had ou imes highe odds o o a i us being de ec ed in hei s ool
han hose whose home had la ine (OR 4.11,95% CI 1.13–14.88,P=
0.032) (Table 4).
Fo Gia dia lamblia in ec ion, he s udy si e and mo he ’s edu-
ca ion le el we e associa ed wi h i in bi a ia e analysis (P= 0.015
and P= 0.012). In mul i a ia e analysis, bo h associa ions we e
disappea ed (P= 0.097 and P= 0.082) (Table 5).
C yp ospo idium (spp.) in ec ions we e signi ican ly associa ed
wi h seasonali y and WLZ in bi a ia e analysis. In mul i a ia e ana-
lysis, hey emained independen ly associa ed wi h C yp ospo id-
ium in ec ions oge he wi h gende (Table 5). In an s who had
highe WLZ we e less likely in ec ed wi h C yp ospo idium han
hose wi h lowe WLZ (OR 0.58, 95% CI 0.39–0.87, P= 0.008).
In an s whose samples we e collec ed du ing he d y season
(May–Oc obe ) we e less likely o be in ec ed wi h
C yp ospo idium han hose whose samples we e collec ed
du ing he ainy season (No embe –Ap il) (OR 0.3, 95% CI
0.11–0.81, P= 0.018). Gi ls we e mo e likely in ec ed wi h
C yp ospo idium han boys (OR 2.86, 95% CI 1.19–6.88, P= 0.019).
Discussion
Ou s udy in es iga ed he p e alence o selec ed common i uses
and pa asi es in a popula ion o asymp oma ic 6, 12 and 18-
Fig. 2. Flow diag am o pa icipan p og ess h oughou he s udy. CSB, co n-soy blend; LAZ, leng h- o -age Z-sco es; milk-LNS, lipid-based nu ien supplemen
wi h milk p o ein base; soy-LNS, lipid-based nu ien supplemen wi h soy p o ein base; WFL, weigh - o -leng h.
4 Y.-M. FAN e al.
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mon h-old Malawian child en. The s udy also assessed he en i -
onmen al p edic o s o he p esence o i uses and pa asi es
among 6-mon h in an s. We ound a high p e alence o i al
and pa asi ic in ec ions in hese child en. Se e al p edic o s
we e ound o be associa ed wi h he in ec ions including season-
ali y o sample collec ion, sani a ion condi ions and a he ’s edu-
ca ion le el.
In his s udy, we used eal- ime PCR o de ec i uses and
pa asi es. Due o he sensi i i y o hese assays we could de ec
also low-g ade in ec ions which may be common in asymp om-
a ic in an s and child en. Compa ed wi h adi ional me hods
such as cell cul u e, an igen de ec ion o mic oscopic examina ion
o i uses o pa asi es, ou esul s gi e mo e ep esen a i e pic u e
o he epidemiology o hese in ec ions including asymp oma ic
ones.
The p e alence o i uses and pa asi es in ou s udy we e
much highe han hose s udies ca ied ou in high-income coun-
ies, and mo e compa able wi h s udies in low-income coun ies.
The en e o i us p e alence in ou s udy was much highe han
hose epo ed in No wegian [28] and Finnish in an s [13,29],
bu mo e compa able wi h Mongolia in an s [30]. The same
end was o he p e alence o hino i us in ou s udy s.
Finnish in an s [21,29]; pa echo i us s. Finnish in an s [13,
31] and No wegian in an s [32]; no o i us s. Ge man [33],
Ko ean [34], Came oonian [12] and Sou h A ican child en
[35]. The p e alence o Gia dia lamblia in ou s udy was also
highe han epo ed in Bangladeshi heal hy in an s [36], bu
qui e compa able wi h Ugandan asymp oma ic in an s [37].
C yp ospo idium (spp.) p e alence was also highe han p e i-
ously epo ed om Spanish [38] and F ench child en [14], and
Chinese [15] and Bangladeshi in an s [36]. Ou esul s we e
also compa able wi h hose in MAL-ED and GEMS non-
dia hoeal samples in no o i us [16,18] and Gia dia in ec ions
[17], bu wi h a lowe a e o o a i us and C yp ospo idium in ec-
ions in ou s udy [18].
The disc epancy be ween ou indings and hose o o he s ud-
ies can o some ex en be explained by he use o di e en me h-
ods o de ec ing he in ec ions. In addi ion, o he ac o s such as
di e ences in s udy popula ions, pe sonal and communi y
hygienic s anda ds, sani a ion, clima e, home c owding, wa e
and ood supplies, socioeconomic condi ion, seasonal a ia ions,
p oximi y o bo h domes ic and wild animals and a high p e a-
lence o o he diseases and condi ions such as HIV in ec ion
and malnu i ion may ha e in luenced he indings in di e en
s udies.
Only a ew s udies ha e in es iga ed he p edic o s o i al and
pa asi ic in ec ions in heal hy in an s li ing in u al low-income
se ings. Ou esul s a e, howe e , in ag eemen wi h p e ious
s udies showing seasonali y o en e o i us and C yp ospo idium
in ec ions [39–41]. The e is also some p e ious e idence om
Acc a ha he use o non- lush oile s is associa ed wi h a highe
en e o i al isola ion a e among heal hy in an s [39]. The absence
o la ines has been associa ed wi h dia hoea incidence also in
Vie nam, whe e o a i us was he mos common causa i e
agen [42]. These indings a e consis en wi h he ecal-o al ans-
mission ou e o hese mic obes and sugges ha imp o emen s
in sani a y condi ions migh dec ease he p e alence o en e ic
i al in ec ions in u al Malawi.
Ou s udy shows he high asymp oma ic in ec ions in
Malawian child en. These child en ca ying he pa hogens did
Table 1. Cha ac e is ics o pa icipan s
S udy pa icipan s
(N= 469)
Subjec s wi hou s ool samples
o wi h dia hoea (N= 371) P alue
P opo ion o boys 47.3% 53.1% 0.110
Mean (S.D.) in an age, mon hs 5.98 (0.25) 6.09 (0.22) <0.001
Mean (S.D.) weigh - o -age z-sco e (WAZ) −0.79 (1.10) −0.79 (1.13) 0.499
Mean (S.D.) leng h- o -age z-sco e (LAZ) −1.65 (1.00) −1.66 (1.03) 0.4403
Mean (S.D.) weigh - o -leng h z-sco e (WLZ) 0.45 (1.02) 0.45 (1.08) 0.473
Mean (S.D.) age o he main gua dian, yea s 28 (9) 28 (10) 0.342
Mean (S.D.) numbe o pe sons in household 4.8 (1.8) 4.9 (1.8) 0.196
Mean (S.D.) numbe o child en <5 yea s o age in household 1.6 (0.7) 1.6 (0.6) 0.145
Mean (S.D.) mo he s’educa ion, comple ed yea s 3.5 (3.4) 3.6 (3.2) 0.328
Mean (S.D.) a he s’educa ion, comple ed yea s 4.1 (3.8) 4.3 (4.0) 0.269
Mean (S.D.) numbe o economic suppo pe son in he amily 1.5 (1.1) 1.7 (1.3) 0.076
Mean (S.D.) numbe o animals in he house 5.9 (10.6) 5.2 (8.0) 0.166
P opo ion wi h mode a e anaemia (Hb <80 g/l) 15.0% 14.9% 1.00
P opo ion wi h posi i e mala ia mic oscopy 13.0% 14.6% 0.539
P opo ion wi h unsa e sou ce o d inking wa e
a
10.2% 6.2% 0.056
P opo ion wi h household la ine 92.8% 93.8% 0.673
P opo ion en olled om Lungwena si e 62.9% 48.5% <0.001
P opo ion o sample collec ion a ainy season, No embe –Ap il 58.4% 53.6% 0.183
S.D., s anda d de ia ion.
a
Sou ce o d inking wa e om unp o ec ed well, lake o pond.
P- alue ob ained om S uden ’s es (con inuous a iables) o Fishe ’s exac es (p opo ions).
Epidemiology and In ec ion 5
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no ha e clinical symp oms and looked ‘heal hy’ om hei
ca e ake s’ iews when he s ool samples we e collec ed. I is pos-
sible ha he high p e alence o he asymp oma ic in ec ions in
hese child en is due o he equen exposu e o he pa hogens
which a e common in low-income se ings. In ega ds o
C yp ospo idium and Gia dia lamblia, some species does no
in ec human and possibly play a ole in he high p e alence o
pa asi ic asymp oma ic in ec ions in ou s udy. To educe he
Table 3. Bi a ia e and mul i a ia e analysis o po en ial p edic o s o en e o i us and hino i us among he pa icipan s
En e o i us bi a ia e En e o i us mul i a ia e Rhino i us bi a ia e Rhino i us mul i a ia e
Va iable OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue
Age 0.50 (0.23–1.10) 0.084 0.64 (0.27–1.53) 0.32 0.46 (0.20–1.03) 0.06 0.43 (0.19–0.99) 0.046
Gende (gi ls) 1.15 (0.78–1.69) 0.491 1.19 (0.79–1.79) 0.418 1.11 (0.74–1.67) 0.6 1.16 (0.77–1.76) 0.485
Numbe o economic suppo
pe son in he amily
1.02 (0.84–1.23) 0.849 1.09 (0.90–1.33) 0.374 1.05 (0.87–1.27) 0.612 1.06 (0.87–1.28) 0.573
Sani a ion (no household la ine) 2.72 (1.03–7.20) 0.044 2.40 (0.87–6.59) 0.089 0.68 (0.29–1.62) 0.385
Si e (Lungwena) 1.56 (1.05–2.32) 0.028 1.18 (0.75–1.87) 0.467 1.16 (0.76–1.77) 0.49
Numbe o child en < 5 yea s o
age in household
1.28 (0.96–1.71) 0.096 1.19 (0.88–1.59) 0.258 1.12 (0.85–1.47) 0.435
High ma e nal educa ion le el 0.91 (0.86–0.97) 0.002 0.96 (0.89–1.02) 0.208 0.99 (0.93–1.05) 0.665
High pa en al educa ion le el 0.92 (0.87–0.97) 0.001 0.94 (0.89–0.99) 0.031 0.99 (0.94–1.04) 0.664
Season (May–Oc obe ) 0.64 (0.43–0.95) 0.027 0.65 (0.43–0.99) 0.045 1.04 (0.69–1.57) 0.843
Numbe o animals in house 0.89 (0.75–1.07) 0.209 1.00 (0.98–1.02) 0.791 0.99 (0.97–1.01) 0.404 0.99 (0.97–1.01) 0.403
CI, con idence in e al; OR, odds a io.
Bi a ia e analysis also included WAZ, LAZ, WLZ, numbe o pe sons in household, anaemia, mala ia, sou ce o d inking wa e and age o main gua dian (N= 455–469).
Table 2. P e alence o i uses and pa asi es in 6, 12 and 18-mon h-old Malawian child en
Vi us/Pa asi e Age NNo posi i e % o posi i e 95% CI
En e o i us 6-mon h 469 320 68.2 64.0–72.5
12-mon h 354 284 80.2 76.1–84.4
18-mon h 468 380 81.2 77.6–84.7
Rhino i us 6-mon h 469 130 27.7 23.7–31.8
12-mon h 354 65 18.4 14.3–22.4
18-mon h 468 146 31.2 27.0–35.4
No o i us 6-mon h 469 110 23.5 19.6–27.3
12-mon h 354 79 22.3 18.0–26.7
18-mon h 468 74 15.8 12.5–19.1
Pa echo i us 6-mon h 469 106 22.6 18.8–26.4
12-mon h 354 60 17.0 13.0–20.9
18-mon h 468 77 16.5 13.1–19.8
Ro a i us 6-mon h 469 15 3.2 1.6–4.8
12-mon h 354 4 1.1 0.02–2.2
18-mon h 468 3 0.6 −0.08 o 1.4
Gia dia lamblia 6-mon h 469 45 9.6 6.9–12.3
12-mon h 354 83 23.5 19.0–27.9
18-mon h 468 123 26.3 22.3–30.3
C yp ospo idium 6-mon h 469 30 6.4 4.2–8.6
12-mon h 354 28 7.9 5.1–10.7
18-mon h 468 9 1.9 0.7–3.2
CI, con idence in e al.
6 Y.-M. FAN e al.
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Table 4. Bi a ia e and mul i a ia e analysis o po en ial p edic o s o no o i us, pa echo i us and o a i us among he pa icipan s
No o i us bi a ia e No o i us mul i a ia e Pa echo i us bi a ia e Pa echo i us mul i a ia e Ro a i us bi a ia e Ro a i us mul i a ia e
Va iable OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue
Age 1.29 (0.55–3.02) 0.56 1.40 (0.58–3.34) 0.455 1.38 (0.58–3.28) 0.463 1.44 (0.61–3.44) 0.407 0.57 (0.07–4.38) 0.588 0.82 (0.10–6.97) 0.859
Gende (gi ls) 1.16 (0.75–1.78) 0.503 1.08 (0.68–1.71) 0.753 1.06 (0.69–1.63) 0.795 1.03 (0.65–1.62) 0.902 1.03 (0.37–2.88) 0.958 1.28 (0.43–3.79) 0.652
Numbe o economic
suppo pe son in he
amily
0.98 (0.80–1.21) 0.87 1.07 (0.86–1.34) 0.552 1.05 (0.85–1.28) 0.669 1.10 (0.89–1.35) 0.384 0.93 (0.55–1.57) 0.79 1.00 (0.59–1.71) 0.992
Sani a ion (no
household la ine)
0.88 (0.37–2.10) 0.778 1.31 (0.59–2.92) 0.503 5.23 (1.57–17.44) 0.007 4.11 (1.13–14.88) 0.032
High ma e nal educa ion
le el
0.92 (0.86–0.99) 0.017 0.95 (0.87–1.03) 0.183 1.02 (0.95–1.09) 0.579 0.88 (0.73–1.05) 0.16
High pa en al educa ion
le el
0.93 (0.88–0.99) 0.022 0.94 (0.88–1.01) 0.094 1.01 (0.96–1.07) 0.611 0.85 (0.72–1.01) 0.059 0.88 (0.74–1.04) 0.128
Season (May-Oc obe ) 0.55 (0.35–0.87) 0.01 0.53 (0.32–0.86) 0.01 0.66 (0.42–1.04) 0.072 0.71 (0.44–1.13) 0.149 1.63 (0.58–4.58) 0.352
Numbe o animals in
house
0.98 (0.96–1.01) 0.199 0.98 (0.95–1.01) 0.169 0.99 (0.97–1.02) 0.512 0.99 (0.97–1.02) 0.461 0.95 (0.86–1.05) 0.307 0.96 (0.87–1.06) 0.44
Numbe o pe sons in
household
1.13 (1.01–1.27) 0.032 1.16 (1.02–1.31) 0.024 1.06 (0.94–1.19) 0.322 0.92 (0.68–1.25) 0.6
Anaemia 0.45 (0.22–0.95) 0.035 0.45 (0.20–1.01) 0.052 0.47 (0.23–0.99) 0.046 0.52 (0.24–1.10) 0.086 1.57 (0.43–5.76) 0.5
CI, con idence in e al; OR, odds a io.
Bi a ia e analysis also included WAZ, LAZ, WLZ, si e, numbe o child en <5 yea s o age in household, age o main gua dian and sou ce o d inking wa e (N= 455–469).
Epidemiology and In ec ion 7
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in ec ion a e based on ou indings, hygiene, be e sani a ion
especially in he ainy season a e impo an .
Taken oge he , ou indings e eal a high p e alence o
i uses and pa asi es in asymp oma ic Malawian child en. The
high p e alence o in ec ion could a ec immune esponse and
p oduc ion o p o-in lamma o y cy okines, nu i ional s a us
and he de elopmen o EED. Ch onic in ec ions may be asymp-
oma ic in hese child en. Howe e , he cumula i e e ec o hese
in ec ions could be subs an ial. Fu u e s udies a e needed o in es-
iga e i such in ec ions and speci ic species o pa hogens a e asso-
cia ed wi h he de elopmen o EED and e en ually lead o g ow h
ailu e among in an s and child en in low-income se ings.
Supplemen a y ma e ial. The supplemen a y ma e ial o his a icle can
be ound a h ps://doi.o g/10.1017/S0950268819000025.
Au ho ORCIDs. Y.-M. Fan, 0000-0002-3241-6225
Acknowledgemen s. We hank he s udy pa icipan s and he s a membe s
o Lungwena Heal h Cen e in Mangochi Dis ic o hei suppo and help in
he s udy and Emily McKinney, Ma ie Hélou, Ma ia O askainen, E eliina
Jalonen and Basho Poelman o hei skil ul echnical assis ance. The
LCNI-5 clinical ial was unded by he Academy o Finland (g an s 109796
and 127025), wi h addi ional unding om he Founda ion o Paedia ic
Resea ch in Finland, he compe i i e esea ch Funding o he Tampe e
Uni e si y Hospi al (g an s 9H003, 9J006 and 9R005), he US Agency o
In e na ional De elopmen unde e ms o coope a i e ag eemen CHN-A-
00-08-00001-00, h ough he Food and Nu i ion Technical Assis ance-2
P ojec managed by he Academy o Educa ional De elopmen (AED) and
he Nu ise Inc.
Con lic o in e es . None.
Re e ences
1. Black RE e al.(2013) Ma e nal and child unde nu i ion and o e weigh
in low-income and middle-income coun ies. Lance 382, 427–451.
2. Vic o a CG e al.(2008) Ma e nal and child unde nu i ion: conse-
quences o adul heal h and human capi al. Lance 371, 340–357.
3. Keusch GT e al.(2014) En i onmen al en e ic dys unc ion: pa hogenesis,
diagnosis, and clinical consequences. Clinical In ec ious Diseases :i an
O icial Publica ion o he In ec ious Diseases Socie y o Ame ica 59,
S207–S212.
4. P ende gas AJ and Humph ey JH (2014) The s un ing synd ome in
de eloping coun ies. Paedia ics and In e na ional Child Heal h 34,
250–265.
5. C ane RJ, Jones KD and Be kley JA (2015) En i onmen al en e ic dys-
unc ion: an o e iew. Food and Nu i ion Bulle in 36(suppl. 1), S76–S87.
6. T ehan I e al.(2009) A andomized, double-blind, placebo-con olled ial o
i aximin, a nonabso bable an ibio ic, in he ea men o opical en e opa hy.
The Ame ican Jou nal o Gas oen e ology 104,2326–2333.
7. Galpin L e al.(2005) E ec o Lac obacillus GG on in es inal in eg i y in
Malawian child en a isk o opical en e opa hy. The Ame ican Jou nal o
Clinical Nu i ion 82, 1040–1045.
8. Go o R, Mascie-Taylo CG and Lunn PG (2009) Impac o in es inal pe -
meabili y, in lamma ion s a us and pa asi ic in ec ions on in an g ow h
al e ing in u al Bangladesh. The B i ish Jou nal o Nu i ion 101,
1509–1516.
9. P ende gas A and Kelly P (2012) En e opa hies in he de eloping wo ld:
neglec ed e ec s on global heal h. The Ame ican Jou nal o T opical
Medicine and Hygiene 86, 756–763.
10. Yu J e al.(2015) En i onmen al en e ic dys unc ion includes a b oad
spec um o in lamma o y esponses and epi helial epai p ocesses.
Cellula and Molecula Gas oen e ology and Hepa ology 2, 158–174.
11. Ama CF e al.(2007) De ec ion by PCR o eigh g oups o en e ic pa ho-
gens in 4,627 aecal samples: e-examina ion o he English case-con ol
In ec ious In es inal Disease S udy (1993–1996). Eu opean Jou nal o
Clinical Mic obiology & In ec ious Diseases : O icial Publica ion o he
Eu opean Socie y o Clinical Mic obiology 26, 311–323.
12. Ayukekbong J e al.(2011) En e ic i uses in heal hy child en in
Came oon: i al load and geno yping o no o i us s ains. Jou nal o
Medical Vi ology 83, 2135–2142.
13. Simonen-Tikka ML e al.(2013) Vi us in ec ions among young child en –
he i s yea o he INDIS s udy. Jou nal o Medical Vi ology 85, 1678–
1684.
Table 5. Bi a ia e and mul i a ia e analysis o po en ial p edic o s o Gia dia lamblia and C yp ospo idium among he pa icipan s
Gia dia bi a ia e Gia dia mul i a ia e C yp ospo idium bi a ia e
C yp ospo idium
mul i a ia e
Va iable OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue OR (95% CI)
P
alue
Age 0.91 (0.27–3.10) 0.882 1.19 (0.35–4.03) 0.781 0.82 (0.19–3.59) 0.795 1.78 (0.43–7.37) 0.424
Gende (gi ls) 0.93 (0.50–1.73) 0.826 1.01 (0.53–1.89) 0.987 2.20 (0.99–4.91) 0.054 2.86 (1.19–6.88) 0.019
Numbe o economic suppo
pe son in he amily
0.78 (0.55–1.11) 0.172 0.87 (0.60–1.25) 0.439 1.03 (0.73–1.45) 0.877 1.16 (0.80–1.69) 0.433
Sani a ion (no household la ine) 1.30 (0.44–3.89) 0.636 0.43 (0.06–3.26) 0.414
Si e (Lungwena) 2.55 (1.20–5.43) 0.015 1.97 (0.88–4.39) 0.097 2.48 (0.99–6.19) 0.052 2.59 (0.97–6.89) 0.057
Numbe o child en <5 yea s o
age in household
1.22 (0.83–1.80) 0.301 0.88 (0.52–1.51) 0.645
High ma e nal educa ion le el 0.87 (0.78–0.97) 0.012 0.90 (0.81–1.01) 0.082 0.95 (0.84–1.07) 0.359
High pa en al educa ion le el 0.94 (0.87–1.03) 0.185 0.97 (0.88–1.08) 0.619
Season (May–Oc obe ) 0.61 (0.31–1.17) 0.137 0.33 (0.13–0.83) 0.018 0.30 (0.11–0.81) 0.018
Numbe o animals in house 0.99 (0.95–1.02) 0.489 0.99 (0.95–1.03) 0.644 0.99 (0.94–1.03) 0.537 0.97 (0.91–1.04) 0.393
WLZ 0.96 (0.71–1.30) 0.801 0.68 (0.47–0.99) 0.043 0.58 (0.39–0.87) 0.008
Age o main gua dian 1.01 (0.97–1.04) 0.665 1.03 (1.00–1.07) 0.08 1.04 (0.99–1.09) 0.051
CI, con idence in e al; OR, odds a io.
Bi a ia e analysis also included WAZ, LAZ, numbe o pe sons in household, anaemia, mala ia, and sou ce o d inking wa e (N= 455–469).
8 Y.-M. FAN e al.
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14. Lac oix C e al.(1987) C yp ospo idium oocys s in immunocompe en
child en: epidemiologic in es iga ions in he day-ca e cen e s o Poi ie s,
F ance. Eu opean Jou nal o Epidemiology 3, 381–385.
15. Chen YG e al.(1992) C yp ospo idium in ec ion and dia hea in u al
and u ban a eas o Jiangsu, People’s Republic o China. Jou nal o
Clinical Mic obiology 30, 492–494.
16. Rouhani S e al.(2016) No o i us in ec ion and acqui ed immuni y in 8
coun ies: esul s om he MAL-ED S udy. Clinical In ec ious Diseases : an
O icial Publica ion o he In ec ious Diseases Socie y o Ame ica 62, 1210–1217.
17. Rogawski ET e al.(2017) De e minan s and impac o Gia dia in ec ion
in he i s 2 yea s o li e in he MAL-ED Bi h Coho . Jou nal o he
Pedia ic In ec ious Diseases Socie y 6, 153–160.
18. Liu J e al.(2014) De elopmen and assessmen o molecula diagnos ic
es s o 15 en e opa hogens causing childhood dia hoea: a mul icen e
s udy. The Lance In ec ious Diseases 14, 716–724.
19. Rod iguez-Diaz J e al.(2014) P esence o human en e ic i uses in he
s ools o heal hy Malawian 6-mon h-old in an s. Jou nal o Pedia ic
Gas oen e ology and Nu i ion 58, 502–504.
20. Mangani C e al.(2015) E ec o complemen a y eeding wi h lipid-based
nu ien supplemen s and co n-soy blend on he incidence o s un ing and
linea g ow h among 6- o 18-mon h-old in an s and child en in u al
Malawi. Ma e nal & Child Nu i ion 11(suppl. 4), 132–143.
21. Honkanen H e al.(2013) Human hino i uses including g oup C a e
common in s ool samples o young Finnish child en. Jou nal o Clinical
Vi ology 56, 334–338.
22. K og old L e al.(2015) De ec ion o a low-g ade en e o i al in ec ion in
he isle s o lange hans o li ing pa ien s newly diagnosed wi h ype 1 dia-
be es. Diabe es 64, 1682–1687.
23. Nu minen N e al.(2015) High- h oughpu mul iplex quan i a i e poly-
me ase chain eac ion me hod o Gia dia lamblia and C yp ospo idium
Species de ec ion in s ool samples. The Ame ican Jou nal o T opical
Medicine and Hygiene 92, 1222–1226.
24. Wo ld Heal h O ganiza ion (WHO) (2010) An h o o pe sonal compu-
e s, e sion 3.2.2, 2011: So wa e o assessing g ow h and de elopmen o
he wo ld’s child en. A ailable a h p://www.who.in /childg ow h/
so wa e/en/ (Accessed 20 Feb ua y 2011).
25. Jenis a JA, Powell KR and Menegus MA (1984) Epidemiology o neo-
na al en e o i us in ec ion. The Jou nal o Pedia ics 104, 685–690.
26. G een MS (1992) The male p edominance in he incidence o in ec ious
diseases in child en: a pos ula ed explana ion o dispa i ies in he li e a-
u e. In e na ional Jou nal o Epidemiology 21, 381–386.
27. T aub RJ e al.(2004) Epidemiological and molecula e idence suppo s
he zoono ic ansmission o Gia dia among humans and dogs li ing in
he same communi y. Pa asi ology 128, 253–262.
28. Cinek O e al.(2006) Longi udinal obse a ion o en e o i us and adeno-
i us in s ool samples om No wegian in an s wi h he highes gene ic
isk o ype 1 diabe es. Jou nal o Clinical Vi ology 35,33–40.
29. Salminen KK e al.(2004) Isola ion o en e o i us s ains om child en
wi h p eclinical Type 1 diabe es. Diabe ic Medicine : a Jou nal o he
B i ish Diabe ic Associa ion 21, 156–164.
30. Ku ami su M e al.(2005) Non-polio en e o i us isola ion among am-
ilies in Ulaanbaa a and To p o ince, Mongolia: p e alence, in a amilial
sp ead, and isk ac o s o in ec ion. Epidemiology and In ec ion 133,
1131–1142.
31. Kolehmainen P e al.(2012) Human pa echo i uses a e equen ly
de ec ed in s ool o heal hy Finnish child en. Jou nal o Clinical
Vi ology 54, 156–161.
32. Tapia G e al.(2008) Longi udinal obse a ion o pa echo i us in s ool
samples om No wegian in an s. Jou nal o Medical Vi ology 80, 1835–
1842.
33. Ka s en C e al.(2009) Incidence and isk ac o s o communi y-acqui ed
acu e gas oen e i is in no h-wes Ge many in 2004. Eu opean Jou nal o
Clinical Mic obiology & In ec ious Diseases : O icial Publica ion o he
Eu opean Socie y o Clinical Mic obiology 28, 935–943.
34. Cheon DS e al.(2010) Seasonal p e alence o asymp oma ic no o i us
in ec ion in Ko ean child en. Foodbo ne Pa hogens and Disease 7,
1427–1430.
35. Ma ison K e al.(2010) Molecula de ec ion and cha ac e iza ion o
no o i uses om child en in Bo swana. Jou nal o Medical Vi ology 82,
321–324.
36. Haque R e al.(2009) P ospec i e case-con ol s udy o he associa ion
be ween common en e ic p o ozoal pa asi es and dia hea in
Bangladesh. Clinical In ec ious Diseases: an O icial Publica ion o he
In ec ious Diseases Socie y o Ame ica 48, 1191–1197.
37. Anka kle J e al.(2012) Common coin ec ions o Gia dia in es inalis and
Helicobac e pylo i in non-symp oma ic Ugandan child en. PLoS
Neglec ed T opical Diseases 6, e1780.
38. Ga cia-Rod iguez JA e al.(1990) The p e alence o C yp ospo idium
species in child en in day ca e cen es and p ima y schools in
Salamanca (Spain): an epidemiological s udy. Eu opean Jou nal o
Epidemiology 6, 432–435.
39. O a ume S and Addy P (1975) Ecology o en e o i uses in
opics. I. Ci cula ion o en e o i uses in heal hy in an s in opical
u ban a ea. Japanese Jou nal o Mic obiology 19, 201–209.
40. Molbak K e al.(1993) C yp ospo idiosis in in ancy and childhood
mo ali y in Guinea Bissau, Wes A ica. BMJ (Clinical Resea ch ed.)
307, 417–420.
41. Newman RD e al.(1999) Longi udinal s udy o C yp ospo idium in ec-
ion in child en in no heas e n B azil. The Jou nal o In ec ious Diseases
180, 167–175.
42. Vu Nguyen T e al.(2006) E iology and epidemiology o dia hea in chil-
d en in Hanoi, Vie nam. In e na ional Jou nal o In ec ious Diseases: IJID :
O icial Publica ion o he In e na ional Socie y o In ec ious Diseases 10,
298–308.
Epidemiology and In ec ion 9
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