A cross sectional study of the relationship between the exposure of pregnant women to military attacks in 2014 in Gaza and the load of heavy metal contaminants in the hair of mothers and newborns
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ManducaP, e al. BMJ Open 2017;7:e014035. doi:10.1136/bmjopen-2016-014035
Open Access
Abs Ac
Objec i e Me al con amina ion o humans in wa a eas
has a ely been in es iga ed. Weapon y’s hea y me als
become en i onmen ally s able wa emnan s and
accumula e in li ing hings. They also pose heal h isks
in e ms o p ena al in ake, wi h po en ial long e m isks
o ep oduc i e and child en’s heal h. We s udied he
con ibu ion o mili a y a acks o he load o 23 me als
in he hai o Pales inian women in he Gaza S ip, who
we e p egnan a he ime o he mili a y a acks in 2014,
and hei newbo ns. We compa ed he me al load in he
mo he s wi h alues o adul hai om ou side he wa
a ea (RHS) as he e e ence. We in es iga ed hea y me als
ans-passing in u e o, and assessed i he hea y me al
in ake could de i e om sou ces un ela ed o he wa .
Design C oss sec ional s udy.
Pa icipan s and se ing C oss sec ional con enience
sample o 502 mo he s deli e ing in he Gaza S ip and
hei newbo ns.
Main ou come measu ed Measu e o he load o hea y
me als in mo he and newbo n hai by induc i ely coupled
plasma-mass spec ome y (ICP-MS). Compa ison o
me al loads wi h he e e ence RHS, be ween g oups
wi h di e en exposu es o a acks and house/ag icul u e
chemicals, and be ween mo he s and newbo ns. Da a o
bi h egis y and o exposu es o wa and o he known
isk ac o s we e ob ained a in e iew wi h he mo he s.
Pho og aphic documen a ion o damage om mili a y
a acks was ob ained.
Resul s The whole c oss sec ional con enience sample
had a signi ican ly highe load o hea y me als han he
e e ence RHS. Women exposed o mili a y a acks had a
signi ican ly highe load o hea y me als han hose no
exposed; he load in newbo ns co ela ed posi i ely wi h
he mo he s’ load. No signi ican di e ence was ound
be ween use s/non-use s o house/ag icul u e chemicals.
No o he known con ounde was iden i ied.
Conclusions High hea y me al loads in mo he s, e lec ed
in hose o hei newbo ns, we e associa ed wi h exposu e
o mili a y a acks, posing a isk o immedia e and long
e m nega i e ou comes o p egnancy and child heal h.
Su eillance, biomoni o ing and u he esea ch a e
ecommended. Implica ions o gene al and public heal h
a e discussed.
A c oss sec ional s udy o he
ela ionship be ween he exposu e o
p egnan women o mili a y a acks in
2014 in Gaza and he load o hea y
me al con aminan s in he hai o
mo he s and newbo ns
Paola Manduca,1 Sa wa Y Diab,2 Sami R Qou a,3 Nabil MA Alba qouni,3
Raiija-Leena Punamaki4
To ci e: ManducaP, DiabSY,
Qou aSR, e al. A c oss
sec ional s udy o he
ela ionship be ween he
exposu e o p egnan women
o mili a y a acks in 2014
in Gaza and he load o
hea y me al con aminan s
in he hai o mo he s
and newbo ns. BMJ Open
2017;7:e014035. doi:10.1136/
bmjopen-2016-014035
►Addi ional ma e ial is
published online only. To iew
please isi he jou nal online
(h p:// dx. doi. o g/ 10. 1136/
bmjopen- 2016- 014035)
Recei ed 26 Augus 2016
Re ised 24 Ap il 2017
Accep ed 4 May 2017
1DISTAV, Uni e si y o Genoa,
Geno a, I aly
2Al-Quds Open Uni e si y-Gaza
B anch, Gaza, Gaza S ip,
Pales ine
3Islamic Uni e si y o Gaza,
Gaza, Pales ine
4Uni e si y o Tampe e, School o
Social Sciences and Humani ies/
Psychology, Tampe e, Finland
Co espondence o
P o . Paola Manduca;
paolamanduca@ gmail. com
Resea ch
S eng h and limi a ions o his s udy
►The lack o ‘ne e exposed o wa ’ con ols wi hin
Gaza is a limi a ion o he s udy which canno be
o e come.
►A gene al limi a ion o his ype o s udy is ha he
isks posed in he long e m by he in ake o mul iple
hea y me als a e s ill la gely unknown in humans,
and in pa icula du ing p egnancy.
►The size o he sample, while adequa e o iden i y
he co ela ion be ween le els o hea y me als
wi h en i onmen al exposu e, is no la ge enough
o accu a ely s udy he nega i e ou comes a
bi h (bi h de ec s and p e e m) due o hei low
equency.
►A s eng h o he s udy is he inclusion o a ela i ely
la ge c oss sec ional con enience sample o
pa icipan s, allowing o subg oups o exposu e,
sui able in size o s a is ical analysis.
►An impo an poin was he inclusion o analyis o
newbo n hai in o me al load. .
►Ve i ica ion by in loco isi s he ecall o exposu e
o women on an objec i e basis gi es addi ional
s eng h o he s udy.
►De elopmen o a ques ionnai e and o p ocedu es
ha allowed in o ma ion o be ob ained on a ious
habi s and di e en po en ially isky en i onmen al
exposu es, -allowing o exclude some mo e likely
po en ial con ounde s.
►The analysis o mic oelemen s and me als no
associa ed wi h weapon y p o ided an in e nal
con ol o he analy ic esul s.
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InT oducTIon
Women and child en a e highly ulne able du ing
pe iods o wa and mili a y a acks, as well as in he
a e ma h o wa , because o he possibili y o he long
e m e ec s o wa ela ed en i onmen al changes on
ep oduc i e and in an heal h. Accumula ion in human
bodies o oxican s and hea y me al e a ogens ound in
he emnan s o wa occu s, ha , coupled wi h hei long
pe sis ence in he en i onmen , sugges s a conside able
isk o heal h.1–6 The e ec s o oxican s, e a ogens and
ca cinogens ela ed o hea y me als ha e been ound in
emb yos a concen a ions lowe han in adul s.7 8 Du ing
he i s imes e o p egnancy, majo mo phogene ic
e en s occu , and is he pe iod o highes sensi i i y o he
emb yo o ex e nal e ec o s. Apa om he mu a ional
isks posed by some o he hea y me als, he e is compel-
ling e idence o hei p e alen epigene ic mechanisms
o ac ion.8–15 Hea y me als ac as endoc ine dis up o s,8
and hei in e e ence wi h gene exp ession causes dis u -
bances in a ious me abolic and ho monal pa hways.9
The epigene ic mechanisms a e an essen ial pa o he
cu en unde s anding o he de elopmen al o igin o
heal h and disease.11–15 Repo s show ha hea y me als
accumula e in speci ic body compa men s and can be
eleased du ing p egnancy.9 12–15 Howe e , ela i ely li le
is known abou he kine ics, modali ies and accumula ion
o hea y me als in compa men s o he human body. Also,
no much is known abou he ollowing phenomena: he
e ec s o human subjec s’ concu en in ake o mul iple
oxic me als, he kine ics o he passage o hea y me als
h ough he placen a and he c i ical concen a ions ha
a ec he emb yo and e us.
In addi ion o he isks posed by acu e exposu e,
pe sis ence o hea y me als in he en i onmen may cause
people o be con inually exposed which, combined wi h
he accumula ion o hea y me als in di e en compa -
men s o he body, adds o he conce ns abou he long
e m nega i e e ec s on heal h. The long e m e ec s o
me als ia epigene ic mechanisms can occu in mo he s,
e uses exposed in u e o and in b eas ed in an s and
child en; hese e ec s could e en be ansgene a-
ional.10–13 16 17
Mili a y a acks a e a sou ce o hea y me al inpu in wa
zone en i onmen s, and may in luence he heal h o he
popula ion and a ec he ou comes o p egnancies.4 16
The p e alence o bi h de ec s inc eased in a eas hea ily
exposed o mili a y a acks in I aq,18 and in Gaza a e
he Is aeli mili a y ope a ion o Cas Lead in 2008–200919
and since he implemen a ion o ai deli e ed weapons
in a acks.20 P e ious esea ch in Gaza also showed ha
women’s exposu e o mili a y a acks (cou esy o he
da abase o he Uni ed Na ions' mine ac ion eam)
co ela ed wi h a highe incidence o p ogeny wi h bi h
de ec s.20 21 Hai analysis o me al load o in an s bo n
p ema u ely o wi h bi h de ec s o mo he s who expe-
ienced mili a y a acks e ealed in u e o con amina ion
o he babies. The hea y me al load in hese newbo ns
was highe han ha o no mal newbo n babies o
e a ogens (me cu y and selenium) in babies wi h bi h
de ec s and o oxican s (ba ium and in) in p ema u e
babies.22 Toge he , he da a show an associa ion o he
damage o newbo n heal h wi h ma e nal exposu e o
a acks, and he ans-placen al passage o wa ime hea y
me al emnan s om exposed mo he s o hei p ogeny
in u e o.
Th ee majo wa s, wi h hei complex consequences o
he en i onmen , may ha e been he single mos in lu-
en ial de e minan o change in he li ing condi ions
and in he demog aphy o Gaza om 2008 o 2014. The
con ex o he cu en s udy is he a e ma h o he 2014
Is aeli mili a y ope a ion ‘P o ec i e edge’ in Gaza, which
las ed o 55 days and had massi e e ec s on ci ilian li e.
This ope a ion le widesp ead s uc u al des uc ion,23–28
wi h physical emnan s o wa , including componen s o
weapons, sh apnel and missiles, as well as en i onmen-
ally s able chemical elemen s and con amina ed uins,
h oughou he a ea.29 The weapons used in hese a acks
we e documen ed by he Uni ed Na ions and o he epu-
able sou ces, and included missiles, mo a s, explosi e
de ices and bombs o a ious sizes, wi h o wi hou pene-
a o heads. The con en o hea y me als in each weapon
di e ed, and each had a di e en ange o sp ead, om
me es o hund eds o me es o mo e.23–29 The Is aeli
go e nmen does no make a ailable a lis o weapons
used, and all da a a e di ec ly om Uni ed Na ions' agen-
cies and independen wi nesses on he g ound. Remo al
o explosi e wa emnan s and he deb is o demoli ion
began only 6–8 mon hs a e he end o hos ili ies and
in ol ed he c ea ion o open ai deposi s and he euse
o ma e ials om demolished s uc u es. No ans e s o
deb is could be conduc ed ou side he a ea o he Gaza
S ip.29 Thus any con amina ion due o he 2014 wa
emained in he local en i onmen om he ime o he
a acks h oughou he pe iod o ou s udy.
The aim o he s udy was o in es iga e whe he he e
we e changes in he me al load o a ep esen a i e
segmen o he emale popula ion a e mili a y a acks,
pa icula ly wi h espec o hea y me al con aminan s
wi h known e a ogen, oxican and ca cinogenic e ec s,
which could pose long e m isks o heal h because o
hei s abili y in he en i onmen and endency o accu-
mula e in he human body. We in es iga ed he ex en
o exposu e o a acks in a c oss sec ional con enience
sample o women who had been in hei i s imes e
o p egnancy du ing he a acks in he summe o 2014
and who en e ed one o ou majo ma e ni y hospi als
in Gaza o deli e y. The co ela ion be ween ma e nal
con amina ion and hei newbo ns’ was also in es iga ed.
MeThods
Pa icipan s
Pa icipan s we e 502 mo he s who we e in hei i s
imes e o p egnancy du ing he 2014 wa on Gaza and
who deli e ed be ween la e Janua y and Ma ch 2015 in
one o ou ma e ni y wa ds: Al-Shi a (n=202), Al-Awda
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Open Access
(n=100), Al-Nasse (n=100) and Al-Aqsa (n=100). All
pa icipan s we e esiden s in one o ou Gaza S ip go e -
no a es. The e we e no exclusion c i e ia a en ollmen ;
no pa icipan da a we e disca ded a e he in e iews,
and all dona ed hai samples we e analysed.
P ocedu es
One midwi e in each hospi al egis e ed all he deli -
e ies occu ing du ing he wo k shi and ob ained
he pa icipan s’ w i en in o med consen o pa ic-
ipa ion in he s udy. The midwi e collec ed he hai
samples om mo he s and newbo ns. The midwi e also
adminis e ed a ace o ace in e iew wi h he mo he s,
ollowing a p epa ed ques ionnai e.20–22 This included
he s anda ds o Eu opean and US bi h egis e s and
was in eg a ed p e iously o include he heal h his o y
o he ex ended amily ( o he second deg ee), and
ques ions abou en i onmen al exposu e, including
he mo he s’ ecollec ions o hei exposu es o mili-
a y a acks and a a ie y o po en ially isky habi s. This
ques ionnai e was hus an ap ool o he su eillance
o changes in ep oduc i e heal h, including o he
inhe i ed componen o newbo n congeni al diseases,
and i was use ul o es ablishing co ela ions wi h
majo en i onmen al changes in Gaza. The Pales inian
Heal h Resea ch Council and he Helsinki Commi ee
o E hical App o al app o ed he s udy. The Resea ch
Boa d in he Islamic Uni e si y o Gaza, Pales ine,
e iewed and app o ed he esea ch ools and p oce-
du es. Mo he s’ ecollec ions o hei exposu es o
a acks we e co obo a ed wi h objec i ely documen ed
damage o hei dwellings, i he women epo ed he
a acks occu ing while hey we e a home.
Measu es
In he p esen s udy, he me al load in he hai o mo he s
and newbo ns was de e mined by induc i ely coupled
plasma-mass spec ome y (ICP-MS) using he me h-
odology ecommended by he In e na ional A omic
Ene gy Agency (IAEA) o es ing human exposu e
o en i onmen al me als.30 We analysed women’s and
newbo ns’ hai o he me al componen s o weapon y
al eady iden i ied in 2009 a weapons’ wound si es in he
bodies o ic ims o a acks.6 We had also de ec ed hese
me al componen s con amina ing he hai samples o
65 o 95 child en es ed 1 yea a e he a acks o Cas
lead (Manduca, unpublished da a). We also ound some
o hese me als con amina ing he hai o newbo ns in
2011.21 22 Finally, we es ed 23 me als, including known
weapon componen s and wa emnan s, such as lead
(Pb), ba ium (Ba), me cu y (Hg), a senic (As), zinc (Zn),
cadmium (Cd), in (Sn), u anium (U), ungs en (W) and
aluminium (Al). As an in e nal con ol, we also measu ed
o he me als and mic oelemen s ha ha e biological ele-
ance bu a e no weapons ela ed.
We compa ed he me al load o hec oss sec ional
con enience sample o Gaza women wi h alues o adul
hai om ou side he wa a ea (RHS).31 We analysed
whe he he me al loads in mo he s we e co ela ed wi h
hose in newbo ns.
Hea y me al concen a ions a e exp essed as ppm (pa s
pe million). Ma e nal hai (4 cm) was aken nea es o
he scalp a he nape o he neck, which e lec ed en i-
onmen al exposu e du ing he las 4–5 mon hs o
p egnancy and he e en ual elease o me als p e iously
accumula ed in he body. Hai om newbo ns e lec ed
he accumula ion o me als h ough li e in u e o.
All hai was p ese ed in plas ic bags un il he momen
o analysis, acco ding o he ecommenda ions o he
IAEA, in he Paci ic Rim Labo a o y, ISO/Tec 17 250
acc edi ed (Canada). Analy ical p ocedu es we e
pe o med acco ding o p e ious p o ocols.19 In b ie , 0.2
g o washed hai was added o 2 mL o HNO3 and 2 mL
o H2O2, hea ed o 85°C o 2 hou s and added a oom
empe a u e o 6 mL o wa e . Samples we e un in Agilen
7700. The limi s o de ec ion (ppm) we e: aluminium (Al)
and i on (Fe) 0.4; magnesium (Mg), coppe (Cu), lead
(Pb), manganese (Mn) and i anium (Ti) 0.04; ba ium
(Ba), cobal (Co) and ch omium (C ) 0.02; a senic (As),
cesium (Cs) and molybdenum (Mo) 0.001; cadmium
(Cd) and u anium (U) 0.0001; me cu y (Hg) 0.0004;
nickel (Ni) 0.15; selenium (Se) 0.22; in (Sn) and ung-
s en (W) 0.03; s on ium (S ) 0.01; anadium (V) 0.002;
and zinc (Zn) 0.3. Expe imen al alues below he limi s o
de ec ion o each me al we e conside ed equal o 0 0 o
he pu poses o s a is ical analysis, which was conduc ed
using median alues. Comme cial analy ical s anda ds o
hai o calib a ion pu poses we e un in pa allel (NCS
ZC 81002b and NCS DC73347a; China Na ional Analysis
Cen e o I on and S eel).
Exposu e o mili a y a acks
The a iable exposu e o women o mili a y a acks was
indica ed by sel - epo ing and e i ied by pho og aphic
documen a ion. Women esponded ‘yes’ o ‘no’ o i e
ques ions: whe he hei own house was bombed du ing
he 2014 wa , whe he he house nex doo was bombed
du ing he 2014 wa , whe he hey we e inside hei home
a he ime o he a ack, whe he hey we e displaced
a e wa ds and whe he hey ound spen ammuni ion
inside hei dweling. Based on hese answe s, hey we e
g ouped acco ding o hei 'p oximi y o exposu e o
a acks'. The concep o p oximal exposu e was o mu-
la ed on he ealisa ion ha a acks e y o en in ol ed
he sp ead o weapons' pa s o adjacen houses. The e m
'p oximally exposed” was used o iden i y women whose
homes o neighbou ing homes we e a acked. The p ox-
imally exposed g oup was di ided in o wo subg oups
acco ding o hei con inuous habi a ion in he places
whe e he a acks occu ed: women who emained in o
nex o he house ha had been bomba ded o shelled,
and women who mo ed elsewhe e a some ime a e he
a ack. C ea ion o hese subg oups e lec s he conce n
ha women wi h ongoing esidence a he loca ions o
he a acks migh ha e had di e en exposu es o wa
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emnan s han hose who had mo ed. This conce n was,
ul ima ely, un ounded. A hi d g oup included women
who had no ecollec ion o any exposu e. In Oc obe
2015, we isi ed he women in subg oups 1 and 2 and
pho og aphically documen ed he damage ha had
occu ed du ing he mili a y a acks on hei dwellings.
Exposu e o po en ial ci ilian sou ces o me al con amina ion
We es ed whe he o he known po en ial sou ces o
con amina ion by hea y me als co ela ed wi h he
mo he s’ dis ibu ion o me al load. Women we e asked
abou hei own use o ag icul u al subs ances (pes icides,
he bicides, ungicides) and gene ic household chemicals
o unknown composi ion, hei consump ion o h ee
main ypes o medicines and o h ee p ena al p e en ion
supplemen s, hei use o h ee a ailable sou ces o wa e
o d inking and cooking, hei equency o ea ing ish
and hei his o y o smoking. Fo s a is ical analyses, a
dicho omy a iable was o med wi h 1=women epo ing
he use o ag icul u al and household chemicals and
2=non-use s.
s a is ical me hods
The me al loads (ppm) ound in he hai o mo he s,
epo ed as median alues and in e qua ile anges, we e
s a is ically compa ed. The i s analysis in ol ed he
95 h pe cen ile alues o he whole coho and o each
exposu e g oup compa ed wi h hose alues o he hai
om adul s o bo h sexes om a eas una ec ed by wa
(RHS, Ge many, by Mic o T ace Mine als, MTM; USA
by T ace Mine als In e na ional, TMI).31 No equi alen
e e ence was a ailable o he newbo ns’ me al load.
The second analysis compa ed he me al loads wi hin he
c oss sec ional con enience sample be ween g oups p ox-
imally exposed and unexposed o mili a y a acks. The
hi d analysis compa ed he me al loads be ween use s
and non-use s o ag icul u al and household chemicals.
In analysing he indings in his s udy, quan ile eg es-
sion analysis was used because i allowed o he modelling
o any pe cen ile o qua ile o he ou come, ep e-
sen ed in his s udy by me al dis ibu ion, including he
median. Fu he mo e, he Shapi o–Wilk and Pea son’s χ2
no mali y es s showed ha me al concen a ions we e no
no mally dis ibu ed, and log ans o ma ion did no lead
o sa is ac o y esul s. Quan ile eg ession analysis has he
ad an age o being mo e obus agains ou lie s in he
ou come a iables han leas squa es eg ession (linea )
and, as a semi-pa ame ic ool, i a oids assump ions
abou he pa ame ic dis ibu ion o he e o p ocess.
The ela ionships be ween 23 me al concen a-
ions and exposu es o mili a y a acks we e analysed
by mul iple quan ile eg ession models, leas absolu e
alue models (LAV o MAD) and minimum L1 no m
models.32 The quan ile eg ession models, i by QREG
STATA COMMAND, exp ess he quan iles and he
condi ional dis ibu ion as linea unc ions o he inde-
penden a iables which, in his case, a e exposu e and
any con ounde s. Spea man co ela ions we e used o
iden i y he associa ions be ween mo he s’ and newbo ns’
me al concen a ions. All analyses we e pe o med using
STATA .13.
esulTs
In his sample, median age o he women was 26.9±5.92
yea s ( ange 16–52), and 2.5% o pa icipan s we e
younge han 18 yea s. O he 502 women, 26.7% we e
ca ying hei i s p egnancy du ing he wa , and he
majo i y (88.8%) wo ked a home. P ena al ca e e o s,
including consump ion o i on, i amins and olic acid,
we e unde aken by 89% o women. A o al o 29%
epo ed a diagnosis o anaemia while 0.5% epo ed a
diagnosis o diabe es. The p e alence o p e e m deli e y
was 1.5%; he p e alence o low bi h weigh (<2.5 kg) was
2.3%. O he in an s in he s udy, 4.5% we e bo n wi h
bi h de ec s, and all we e bo n ali e, al hough one baby
died in he minu es a e bi h.
Figu e 1A shows he pe cen ages o pa icipan s
esiding in each o he ou go e no a es and whe he
hey we e displaced a e he mili a y a acks. In o ma-
ion abou he exac loca ions o displacemen was no
a ailable. Figu e 1B shows ha 32.4% o women epo ed
weapon hi s di ec ly on hei own house and 14.7% ound
wa emnan s inside he dwelling. Among women whose
houses we e di ec ly hi (n=163), 63% (n=103) we e
inside he house du ing he mili a y a ack (Figu e 1C).
Thus a i h (20.4%) o all women we e in hei own
home unde he a ack, and almos hal (46.6%) o
hese ound wa emnan s, gene ally sh apnel and shells,
inside hei houses. In addi ion, 11.9% o he women
whose houses we e no di ec ly hi epo ed ha weapons
emnan s eached he in e io o hei home om mili-
a y a acks o neighbou ing buildings, sugges ing a wide
adius o he sp ead o agmen s om he blas s.
In Oc obe 2015, 78 women o he 103 whose homes
we e hi while hey we e inside we e con ac ed, and he
damage o 49 homes was eco ded (in pho og aphs)
in o de o objec i ely documen he mili a y a acks.
Figu e 2A shows he numbe o he isi ed homes whose
damages we e pho og aphed ; o hese 63% s ill exhib-
i ed he damage om he a acks. Ten houses we e o ally
des oyed, 15 exhibi ed majo damage and 24 displayed
mino damage (Figu e 2B and Figu e 1 in he online
supplemen ).
Subg oups o pe sonal exposu e o mili a y a acks we e
gene a ed in o de o in es iga e associa ions be ween he
load o me als in women’s hai and hei p oximi y o he
mili a y a acks. Figu e 3 shows he dis ibu ion o he wo
p oximally exposed and he unexposed subg oups. O
he 502 women in his s udy, 55.9% (n=282) belonged o
he subg oup o women who we e exposed o an a ack
and who emained in he same house, whe e weapon
emnan s we e likely o be p esen , du ing he ollowing
mon hs o hei p egnancy. Subg oup 2, composed o
women who we e exposed o a acks and who had mo ed
away om he bombed o shelled home, included 12.3%
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Figu e 1 -CLocaliza ion o he mo he s du ing a acks. (A) The esidence o he 502 mo he s. In black hose esiding in la e
2015 in he same place as du ing he a acks in g ay hose displaced a e wa ds. (B) Le column, pe cen age o women in he
502 c oss sec ional con enience sample ha epo ed ha hei own housing was hi di ec ly and igh column, hose ha ound
pa s o ammuni ions in hei house. (C) Pe cen age o women ha we e inside hei house unde he a ack .
Figu e 2A-B Repo ed a acks on he housing o he women in he c oss sec ional con enience sample(n=502). (A) Se en y
eigh o he 103 women who expe ienced a di ec a ack on hei house while hey we e inside i we e isi ed in Oc obe 2015.
The damages ha we e s ill isible we e documen ed by pho og aphy. (B) Damages obse ed classi ied acco ding o hei
impac on he s uc u e.
(n=61) o pa icipan s. Subg oups 1 and 2 compose wha
we named he "p oximally exposed" women and we e he
68.2% o he c oss sec ional con enience sample. App ox-
ima ely one- hi d (31.7%, n=159) o he women belonged
o subg oup 3, who epo ed no ha ing been unde o
nex doo o mili a y s ikes and we e he e o e consid-
e ed unexposed. Pho og aphic e idence con i med he
damage o he houses o 25 women in subg oup 1 and o
24 women in subg oup 2.
Me al load in mo he s and newbo ns
Supplemen a y Table 1 (see online supplemen a y Table
1) shows he desc ip i e alues o he me al load, as de e -
mined by ICP-MS, o he 23 me als in es iga ed in he hai
o mo he s and newbo ns, bo h o he whole g oup and
o subg oups o exposu e o mili a y a acks. In gene al,
he mo he s’ me al loads we e highe han he newbo ns’.
Spea man co ela ions o he me al load be ween he
mo he s and newbo ns o he whole sample (Table 1)
showed signi ican (p<0.05) posi i e co ela ions o all
me al loads, excep o Cu and Sn, and a nega i e co ela-
ion o Ba. These da a indica e ans-placen al passage o
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Figu e 3A-D Dis ibu ion o he c oss sec ional con enience sampleacco ding o di e en en i onmen al exposu es. (A)
Di ision o he whole sample in o subg oups was based on hei epo ed p oximal exposu e o non-exposu e. All women who
epo ed ha hei home o he home nex doo was hi in an a ack a e in subg oup 1 (55.9% o he sample i hey emained a
esiden in he same house un il hey deli e ed hei baby, o in subg oup 2 (12.3% o he sample) i hey we e displaced a e
he a ack. Subg oup 3 (31.7% o he sample epo ed no exposu e o a acks. (B) Sou ce o wa e o d inking and cooking. (C)
Nea ness o manu ac u e s and wo kshops. (D) Use o household and ag icul u e chemicals (shown in de ail): use s, o use s o
any o hese chemicals o mo e han one.
oxican s C , Cs, Mo, Ni, S , Pb and V, and e a ogens Hg,
U and W.
The me al load compa ison o a e e ence s anda d
(RHS) om a eas una ec ed by wa (Table 2) shows he
compa ison o he 95 h pe cen ile o he me al load o
he mo he s wi h ha o RHS. In he whole sample and in
each subg oup, he load o oxican s (Al, Fe, Ba, Mn, Ni,
Pb, S and V), e a ogens (Hg, U and W), ca cinogens (As,
Cd and Co), and o Mg and Zn was signi ican ly highe in
he hai o women in all g oups o he Gazac oss sec ional
con enience sample han in he e e ence g oup RHS.
The load o Cs, Cu, Mo, SE, Sn and Ti did no signi ican ly
di e om wha was ound in he e e ence g oup, RHS.
P oximal exposu e o mili a y a acks and me al load
To examine whe he he e is an associa ion be ween
p oximal exposu e o mili a y a acks and me al load, he
median alues o he subg oups we e analysed by mul iple
quan ile eg ession models. Resul s showed ha bo h
subg oups o p oximally exposed women had signi i-
can ly highe loads o he majo i y o me als han he
unexposed subg oup. Fo he sake o cla i y, Table 3 does
no include he ollowing me als which we e de ec ed a
he same le el in all samples as in RHS, and hus un e-
la ed o di e ences in an h opogenic ac i i ies o any
kind in he samples and he e e ence: Cs, Cu, Mo, Se, Sn
and Ti. This analysis con i ms ha p oximal exposu e is
associa ed wi h a highe load o con amina ion o mos
me als, wi h an excep ion o U, wi h he highes load
in subg oup 3. Speci ically, subg oups 1 and 2 oge he
showed signi ican ly highe me al loads han subg oup
3 o Al, Mg, Mn, Ba, As, Zn and V. Subg oups 1 and 2
showed signi ican di e ences be ween hem: subg oup
1 was highes o Ba and V; subg oup 2 o C , S and
W. Measu ed loads o Fe, Hg and Pb we e highe in he
h ee subg oups han in RHS bu did no di e among
he subg oups.
Compa ison be ween he newbo ns g oups o me al
load showed ha he newbo ns in subg oup 2 had
a signi ican ly highe load o con aminan s o mos
me als, excep o Hg and Zn. Ye , child en in subg oup
3 had a signi ican ly highe load o Al han newbo ns in
subg oup 1.
Rega ding exposu es o en i onmen al chemicals om
ci ilian sou ces and po en ial con ounde s, he s udy
showed high homogenei y in he women’s sample o
exposu e o mos o he po en ial isk ac o s. Fo 84%
o he women, i was common o use mul iple sou ces o
d inking wa e , and 87% o he women esided a om
indus ial plan s ( igu e 3B and C). All o he women
used a combina ion o he i e ood sou ces (UNRWA,
Egyp ian, Is aeli and Tu kish impo s, and local). Less
han 5% o women engaged in po en ially isky habi s,
such as smoking, using hai dye o consuming medicines
(no shown), and mos o he women (90%) a e ish, a
po en ial sou ce o me cu y, less han o equal o once
pe mon h. These pu a i e isk ac o s do no seem ele-
an o he di e ences in he dis ibu ion o he me al
load ound be ween he women p oximally exposed o
mili a y a acks and unexposed women.
Figu e 3D shows ha 76.3% (n=352) o women
epo ed non-use o household and ag icul u al chemi-
cals, whe eas he 109 women classi ied as use s epo ed
using pes icides (n=82), he bicides (n=9) o o he house-
hold chemicals (n=18). The chemicals we e iden i ied
acco ding o hei unc ion a he han hei chemical
composi ion and we e s udied only om he poin o iew
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Table 1 Co ela ion be ween mo he s' and newbo ns' me al loads. Spea man analysis o he co ela ion be ween mo he s' and newbo ns' me al loads. Values o p<0.05
a e enhanced in yellow o he posi i e co ela ions o Mg, C , Cs, Hg Mo, Ni, S , U, V and W. The co ela ion is nega i e o Ba. Values a e epo ed in ppm
Me al* Whole sample Exposu e 1 Exposu e 2 Exposu e 3 Me al Whole sample Exposu e 1 Exposu e 2 Exposu e 3
Al n 495 278 59 158 Mo n 505 282 61 162
ho 0.0486 0.0554 0.0764 0.0899 ho 0.1182 0.1403 0.0883 0.08
p 0.2801 0.3576 0.5651 0261 p 0.0078 0.0184 0.4988 0.3113
Fe n 506 282 61 163 Ni n 469 270 51 148
ho 0.0308 −0.0321 0.1373 0.0664 ho 0.1405 0.0646 0.3296 0198
p 0.4894 0591 0.2913 0.4001 p 0.0023 0.2904 0.0182 0.0159
Mg n 501 279 61 161 Pb n 476 271 54 151
ho 0.1443 0.1512 0.1295 0106 ho 0.0513 −0.0114 0.0104 0.1881
p 0.0012 0.0115 0.3198 0.1807 p 0.2641 0.8519 0.9406 0.0207
Mn n 483 275 56 152 Se n 467 269 50 148
ho 0.0307 0.0798 −0.0272 −0.0775 ho 0.0381 0.0016 −0.1302 0.1343
p 0.5005 0187 0842 0.3429 p 0.4115 0.9794 0.3674 0.1036
Ba n 496 278 61 157 Sn n 472 271 52 149
ho −0.0486 0.0569 −0.1084 −0.1611 ho 0.0156 0017 −0.0064 0.0212
p 0.2796 0.3447 0.4057 0.0438 p 0.7352 0781 0964 0.7972
As n 499 281 61 157 S n 505 282 61 162
ho 0038 0.0408 0.06 0.0543 ho 0.2308 0.2857 0.0931 0.1289
p 0.3973 0.4953 0.6462 0.4991 p 0 0 0.4753 0.1021
Cd n 503 281 61 161 Ti n 496 278 58 160
ho −0.0351 −0.027 −0.2051 0.0297 ho 0.0527 0.0196 −0.0437 0.1522
p 0.4317 0.6517 0.1129 0.7083 p 0.2416 0.7444 0.7444 0.0547
Co n 468 269 50 149 U n 493 278 59 156
ho −0.0849 −0.0961 −0.0334 −0.0645 ho 0.1398 0.1608 0.2142 0055
p 0.0666 0.1158 0.8179 0.4347 p 0.0019 0.0072 0.1032 0.4952
C n 480 273 54 153 V n 482 275 51 156
ho 0.1105 0.0915 0.1661 0.0984 ho 0.0938 0.1043 0.0953 0.0806
p 0.0154 0.1316 0.2299 0.2261 p 0.0396 0.0843 0.5059 0.3174
Cs n 474 272 52 150 W n 491 277 59 155
ho 0.1789 0.1904 −0.1259 0.2293 ho 0.4594 0.4288 0.6026 0.3253
p 0.0001 0.0016 0.3738 0.0048 p 0 0 0 0
Cu n 505 282 61 162 Zn n 505 282 61 162
Con inued
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Me al* Whole sample Exposu e 1 Exposu e 2 Exposu e 3 Me al Whole sample Exposu e 1 Exposu e 2 Exposu e 3
ho 0.0031 0.0313 −0.0912 −0.0032 ho 0.0385 0.0768 −0.1213 0.0258
p 0.9451 0.6008 0.4847 0.9681 p 0.3883 0.1984 0.3517 0.7446
Hg n 505 282 61 162
ho 0.2135 0.2051 0.1798 0.2282
p 0 0.0005 0.1655 0.0035
*Al, aluminium; Fe, i on; Mg, magnesium; Mn, manganese; Ba, ba ium; As, a senic; Cd, cadmium; Co, cobal ; C , ch omium; Cs, cesium; Cu, coppe ; Hg, me cu y.
Table 1 Con inued
o hei po en ial con ibu ion o he load o hea y me als
in hai . Table 4 compa es he median quan iles be ween
use and non-use g oups, showing no signi ican di e -
ences (p >0.3 o all analyses) among hese subg oups in
he load o all 23 me als. I is possible, hen, o ule ou
he possibili y ha he use o hese p oduc s con ibu ed
o he hea y me al con amina ion.
dIscussIon
P incipal indings
The s udy is he i s o documen he numbe o ci ilian
subjec s in he popula ion who we e exposed in 2014 o
mili a y a acks in Gaza. The women in his c oss sec ional
con enience sample expe ienced, in 32.4% o cases, a
di ec hi o hei p i a e dwellings and, in 63% o hese
cases, he a acks occu ed while he women we e inside
hei homes. The women’s ecollec ions we e suppo ed
by pho og aphic documen a ion o he epo ed damage
which e i ied i s ex en . Hi s including hose on neigh-
bou ing buildings (p oximal exposu e) we e epo ed by
almos 70% o he women.
The s udy examined he load o hea y me als in he hai
o his c oss sec ional con enience sample o women who
we e all p egnan du ing he wa in Gaza in 2014. Hai
samples we e collec ed when he women deli e ed du ing
he win e o 2014 and he sp ing o 2015. We ound a
posi i e co ela ion be ween a high load o oxican s (Ba,
Al, V, S and C ), a e a ogen (W) and a ca cinogen (As)
in women’s hai and hei p oximi y o mili a y a acks in
2014.
We also ound ha he e was a highe load in he en i e
c oss sec ional con enience sample o Gaza women in
compa ison wi h he hai samples om indi iduals in
a eas una ec ed by wa (RHS), ega dless o hei ecen
exposu e o a acks. The high load was o hea y me als
al eady de ec ed as wa emnan s om p e ious a acks in
2009 ( oxican s such as Al, Fe, Ba, Mn, C , Ni, Pb, S and
V; e a ogens such as U and W; and ca cinogens such as
As, Cd and Co).
The e was, ins ead, no di e ence in he c oss sec ional
con enience sample o Gaza women, ega dless o hei
epo ed exposu e o he a acks in 2014, in compa ison
wi h he me al load in he hai o adul s o bo h sexes
om he a eas una ec ed by wa (RHS) o he concen-
a ion o mic oelemen s (Cu, Se and Mo) and a ew
o he me als (Cs, Sn and Ti). Mo eo e , an h opogenic
sou ces no a ising om mili a y a acks we e excluded
as con ounde s. These da a con i m ha he sou ce o
oxican , e a ogen and ca cinogen con aminan s was
an h opogenic and associa ed wi h mili a y a acks. We
also showed ha he e was ans-placen al passage o
hea y me als om mo he s o hei newbo ns.
limi a ions o he s udy
The lack o ‘ne e exposed o wa ’ con ols wi hin Gaza
is a limi a ion o he s udy which canno be o e come
because he e is no ecen ‘ ime ze o’ o an h opogenic,
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Table 2 Compa ison o he me al load o he mo he s in he c oss sec ional con enience sampleand in subg oups 1, 2 and 3 wi h ha o e e ence anges o s anda ds
om a eas no in ol ed in he wa . Compa ison o he 95 h pe cen ile o me al load in he wholesample and in subg oups 1–3 wi h ha o s anda ds om a eas no
in ol ed in wa s. Con idence in e als a e shown. Resul s wi h 95 h pe cen iles signi ican ly highe han he e e ence alue a e enhanced in ligh blue and in bold. Values
a e epo ed in ppm. Subg oups 1 and 2 a e mo he s ‘p oximally exposed’ o a acks and subg oup 3 hose ha epo ed no exposu e
All mo he sI (n=502) Exposu e g oup 1 (n=282) Exposu e g oup 2 (n=61) Exposu e g oup 3 (n=159)
Re e ence
alue
Me al*
95 h
pe cen ile 95% CI
95 h
pe cen ile 95% CI
95 h
pe cen ile 95% CI
95 h
pe cen ile 95% CI 95°pe cen ile
Al 16.91 13.88 21.68 15.37 13.06 21.63 15.60 12.60 47.60 18.87 13.57 25.11 <8
Fe 40.16 35.25 52.28 41.07 34.50 55.07 35.52 26.49 418.33 40.26 34.52 68.23 1.6–17
Mg 1260.00 1260 1123 1198 1108 1381 1265.00 1012.27 11 30 1510 1057. 1745 20–130
Mn 2.90 2.38 3.44 2.87 2.28 3.40 4.52 1.89 13.20 2.99 2.18 4.76 0.05–0.92
Ba 29.69 24.04 49.18 42.52 26.98 137.13 22.07 15.13 33.90 20.10 15.46 53.45 <4.64
As 0.24 0.21 0.28 0.23 0.20 0.28 0.28 0.14 0.38 0.25 0.21 0.50 <0.2
Cd 0.24 0.20 0.30 0.20 0.18 0.30 0.25 0.19 0.47 0.28 0.20 0.37 <0.2
Co 0.57 0.37 0.76 0.75 0.50 1.04 0.57 0.24 0.72 0.32 0.22 0.69 0.01–0.30
C 2.93 2.43 3.29 2.28 2.10 2.97 3.95 2.79 7.52 3.20 2.64 3.74 0.02–0.21
Cs 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 <0.01
Cu 40.73 33.60 52.24 48.53 37.72 71.78 35.67 23.63 145.00 31.10 27.51 62.63 Oc -41
Hg 1.62 1.16 4.84 1.50 0.97 3.14 20.61 0.95 2480.00 1.41 1.08 24.20 <0.60
Mo 0.26 0.21 0.32 0.23 0.18 0.30 0.40 0.25 0.78 0.28 0.20 0.38 0.03–1.00
Ni 2.76 2.23 3.56 2.76 2.23 3.90 2.05 1.69 3.31 3.10 2.05 4.51 <1.00
Pb 6.50 6.00 7.35 6.65 6.17 7.98 6.47 3.77 7.25 6.17 5.25 9.67 <3.0
Se 0.88 0.86 0.95 0.87 0.83 0.95 0.99 0.84 8.47 0.89 0.87 0.97 0.40–1.70
Sn 0.75 0.61 0.98 0.75 0.57 1.04 0.86 0.49 1.94 0.71 0.55 1.09 <0.70
S 136.00 122.39 160.26 134.85 118.00 162.53 161.50 113.66 1480.00 142.00 108.46 197.21 0.65–6.90
Ti 0.82 0.73 1.00 0.76 0.70 1.01 0.72 0.51 1.45 0.89 0.69 1.15 <1.50
U0.53 0.46 0.68 0.46 0.40 0.62 0.71 0.48 2.49 0.65 0.48 1.01 <0.10
V1.40 1.26 1.56 1.27 1.16 1.40 1.88 1.39 3.92 1.56 1.25 1.80 0.01–0.20
W1.37 1.07 2.28 1.76 1.06 2.74 2.48 1.20 7.27 0.99 0.48 1.52 <0.02
Zn 990.5 902.2 1202,8 1029.6 889.7 1269 990.1 767.3 1657.1 926.53 671.20 1569.16 150–272
*Al, aluminium; Fe, i on; Mg, magnesium; Mn, manganese; Ba, ba ium; As, a senic; Cd, cadmium; Co, cobal ; C , ch omium; Cs, cesium; Cu, coppe ; Hg, me cu y; Mo, molybdenum; Ni,
nickel; Pb, lead; Se, selenium; Sn, in; S , s on ium; Ti, i anium; U, u anium; V, anadium; W, ungs en; Zn, zinc.
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Table 3d Compa ison be ween newbo ns o me al load be ween subg oups acco ding o he mo he s ‘p oximal exposu e’. The me al load in newbo ns o di e en
subg oups we e compa ed wi h each o he . Analysis was by mul iple quan ile eg ession on median alues as linea unc ion o he independen a iable, ‘p oximal
exposu e’. Fo ease in eading he da a, he colou yellow indica es ha he g oup in he column on he le in each panel has signi ican ly highe load (p<0.05) han he
one in he column on he igh in he same panel. I ice e sa, he line is enhanced in g een colou . Panel C compa es exposu e subg oups 1+2 wi h 3; panel D compa es
exposu e subg oups 1 wi h 2
Newbo n
C
Me al
Median exposu es
1+2 95% CI Median exposu e3 95% CI Di e ence p>| | 95% CI - INF 95% CI -SUP
Al 4.98 4.3 o 5.66 5.71 4.72 o6.7 −0.73 0.233 −1.929914 0.4699142
Fe 28.53 25.41 o 31.65 31.82 27.29 o-36.35 −3.289999 0.241 −8.794128 2.21413
Mg 160 152.59 o 167.41 157 146.23 o 167.77 3 0.652 −10.07445 16.07445
Mn 0.33 0.28 o 0.38 0.3 0.23 o0.37 0.03 0.478 −0.0530647 0.1130647
Ba 0.43 0.38 o0.48 0.36 0.29 o0.43 0.07 0.108 −0.0153842 0.1553842
As 0.012 0.011 o0.013 0.011 0.009 o0.013 0.001 0.344 −0.0010762 0.0030762
Cd 0.0061 0.005 o 0.007 0.0053 0.004 o 0.007 0.0008 0.398 −0.0010599 0.0026599
Co 0.02 0.02 0
C 0.12 0.1 o 0.14 0.13 0.1 o 0.16 −0.01 0.601 −0.0475405 0.0275405
Cu 7.64 7.37 o 7.91 7.87 7.48 o 8.26 −0.23 0.339 −0.7023612 0.2423612
Hg 0.0592 0.05 o 0.07 0.0544 0.04 o 0.06 0.0048 0.46 −0.0079632 0.0175632
Ni 0.2 0.17 o 0.23 0.18 0.13 o 0.23 0.02 0.492 −0.0371107 0.0771107
Pb 0.23 0.2 o 0.26 0.22 0.17 o0.27 0.01 0.736 −0.0481337 0.0681337
S 2.96 2.76 o 3.16 3.05 2.75 o 3.35 −0.0899999 0.623 −0.4492506 0.2692508
Ti 0.26 0.22 o 0.3 0.25 0.19 o 0.31 0.01 0.784 −0.061673 0.081673
U 0.0017 0.001 o 0.002 0.0014 0.001 o 0.002 0.0003 0.277 −0.0002415 0.0008415
V 0.011 0.009 o 0.013 0.012 0.01 o 0.014 −0.001 0.486 −0.0038153 0.0018153
W 0.05 0.04 o 0.06 0.04 0.03 o0.05 0.01 0.169 −0.0042687 0.0242687
Zn 203.48 196.77 o 210.19 205.68 195.92 o215.44 −2.199997 0.715 −14.04812 9.648124
D
Me al Median exposu e 1 95% CI Median exposu e 2 95% CI Di e ence p>| | 95% CI - INF 95% CI -SUP
Al 4.55 3.892 o 5.208 6.99 5.561 o8.419 −2.44 0.002 −4.012933 −0.867066
Fe 26.83 23.489 o30.171 36.64 29.457 o 43.824 −9.809999 0.015 −17.73244 −1.887563
Mg 153 145.207 o 160.793 188 171.334 o 204.666 −35 0 −53.39833 −16.60167
Mn 0.3 0.229 o 0.371 0.86 0.703 o 1.017 −0.56 0 −0.7319964 −0.3880036
Ba 0.4 0.342 o 0.458 0.73 0.606 o 0.854 −0.33 0 −0.4673186 −0.1926814
Con inued
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As 0.011 0.009 o 0.013 0.02 0.016 o 0.024 −0.009 0 −0.0128915 −0.0051085
Cd 0.0056 0.004 o 0.007 0.0104 0.008 o 0.013 −0.0048 0 −0.0074228 −0.0021772
Co 0.02 0.02 0
C 0.12 0.096 o 0.144 0.19 0.135 o 0.245 −0.07 0.022 −0.1296617 −0.0103383
Cu 7.31 7.005 o 7.615 8.8 8.144 o9.456 −1.49 0 −2.213651 −0.7663499
Hg 0.0618 0.054 o 0.069 0.0468 0.03 o0.063 0.015 0.103 −0.003037 0.033037
Ni 0.19 0.157 o0.223 0.29 0.214 o0.366 −0.1 0.018 −0.1830964 −0.0169035
Pb 0.2 0.167 o 0.233 0.3 0.226 o0.374 −0.1 0.016 −0.1812501 −0.01875
S 2.82 2.631 o 3.009 3.78 3.374 o4.186 −0.96 0 −1.407472 −0.5125281
Ti 0.24 0.195 o 0.285 0.45 0.352 o0.548 −0.21 0 −0.3172189 −0.1027811
U 0.0014 0.001 o 0.002 0.0029 0.002 o0.004 −0.0015 0 −0.0022334 −0.0007666
V 0.01 0.008– o 0.012 0.014 0.01 o0.018 −0.004 0.044 −0.0078844 −0.0001156
W 0.04 0.007 o 0.073 0.15 0.079 o 0.221 −0.11 0.006 −0.1880415 −0.0319585
Zn 201.73 195.873 o 207.587 213.65 201.058 o 226.242 −11.92 0.092 −25.80754 1.967541
*Al, aluminium; Fe, i on; Mg, magnesium; Mn, manganese; Ba, ba ium; As, a senic; Cd, cadmium; Co, cobal ; C , ch omium; Cs, cesium; Cu, coppe ; Hg, me cu y; Ni, nickel; Pb, lead; S ,
s on ium; Ti, i anium; U, u anium; V, anadium; W, ungs en; Zn, zinc.
Table 3d Con inued
His o ical con amina ion by o he wa emnan hea y me als and
hei pe sis ence in he en i onmen
Besides he iden i ica ion o a high load o hea y me als,
which we speci ically aced o exposu e o he mili a y
a acks in 2014, we ound ha all he pa icipan s had
le els signi ican ly highe han con ols om ou side
a eas a ec ed by wa (RHS) o o he wa emnan hea y
me als, such as U, Hg, Cd, Co, Fe, Ni, Pb, V, Mn, Cd and
Co. P e ious epo s had shown hei deli e y in Gaza by
weapon y; e a ogens Hg and Cd and oxican s Pb and
Fe we e deli e ed by weapons in he 2008–2009 wa .6 A
high load o Hg was epo ed in newbo ns o mo he s
exposed a ha ime o bombing and o a acks wi h
whi e phospho us ammuni ions.17–20 High loads o Al,
Fe, Cd, Hg and U we e de ec ed in he hai o child en
es ed 1 yea a e he 2008–2009 a acks (unpublished,
Manduca).
The p esence o concen a ions highe han hose
ound in he e e ence g oup (RHS) o hea y me als
in oduced p e iously by weapon y in Gaza in he en i e
c oss sec ional con enience sample o women ha we
ha e es ed in 2015 con i ms ha hese elemen s ha e
pe sis ed in he en i onmen o yea s and sugges s ha
he whole popula ion may ha e been ch onically in aking
hese me als.
Implica ions o ch onic exposu e o hea y me als and hei in-body
accumula ion
Ch onic exposu e o hea y me als be o e he a acks in
2014 complica es he con ibu ion o he a acks in 2014,
and in ol es also di e se ypes o hea y me als. Ye , he
hea y me als de ec ed p e iously, as well hose ecen ly
de ec ed as de i ing om he 2014 a acks, a e known o
hei e a ogenic, oxican and ca cinogenic p ope ies.
They a e isk ac o s o non-communicable diseases and
o ep oduc i e heal h. On he one hand, he en i on-
men al s abili y o hea y me als makes i possible o hei
ch onic in ake om he en i onmen by indi iduals. On
he o he hand, hese me als, a e in ake in o he body,
a e no exc e ed apidly and accumula e in o gans whe e
hey can con inue o induce soma ic epigene ic changes.
I he e is a h eshold o hei ac ion , hey can each
he c i ical concen a ions capable o causing nega i e
biological e ec s o e ime and can he e o e a ec
heal h e en a a ime dis an om ha o in ake, and
pa hological and pheno ypic endpoin s o hei e ec s
could be delayed.
A a ie y o nega i e e ec s in ime a ec ing he
physiology o indi iduals, as well as an inc ease in
non-communicable diseases, we e epo ed in associa-
ion wi h hea y me al exposu e. Un o una ely, e y li le
knowledge is a ailable o da e on he kine ics o he depo-
si ion o each hea y me al in he body and o i s elease
om each speci ic o gan o deposi ion, and hese unan-
swe ed ques ions equi e u he in es iga ion. Among
he a ious po en ial long e m nega i e e ec s associa ed
wi h hea y me al in ake, we he e only discuss some o he
conce ns ega ding ep oduc i e heal h, o which some
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Table 4 Compa ison o me al load be ween mo he s acco ding o hei use o house–ag icul u al chemicals. Subg oups
a e no use s-subg oup1 (n=352) o use s subg oup 2 (109), o any o he chemicals lis ed in igu e3D . Analysis was by
mul iple quan ile eg ession on median alues as linea unc ion o he independen a iable, ‘use o chemicals’. The e was no
signi ican di e ence o he load o all me al es ed (p > 0,3) be ween he wo g oups
Me al Subg oups Median es p In 95% CI Sup 95% CI
Al 1–0 0.4099998 0.4472674 0.92 0.36 −0.4687552 1.288755
Fe 1–0 0.3400002 0.8071532 0.42 0.674 −1.24583 1.92583
Mg 1–0 −32 36.53437 −0.88 0.382 −103.7798 39.77981
Mn 1–0 0.07 0.0755919 0.93 0.355 −0.078517 0.2185169
Ba 1–0 0.0299997 0.6327794 0.05 0.962 −1.213234 1.273234
As 1–0 0.003 0.0067409 0.45 0.656 −0.010244 0.016244
Cd 1–0 −0.0029 0.0053168 −0.55 0.586 −0.013346 0.007546
Co 1–0 0 0.006578 0 1 −0.012924 0.012924
C 1–0 −0.02 0.0771729 −0.26 0.796 −0.1716231 0.131623
Cs 1–0 0
Cu 1–0 0.1999998 0.6981627 0.29 0.775 −1.171694 1.571694
Hg 1–0 0.001 0.0219324 0.05 0.964 −0.042091 0.044091
Mo 1–0 −0.003 0.0057415 −0.52 0.602 −0.0142804 0.0082804
Ni 1–0 −0.06 0.0769901 −0.78 0.436 −0.2112641 0.0912641
Pb 1–0 −0.0599999 0.2266566 −0.26 0.791 −0.5053166 0.3853167
Se 1–0 −0.0100001 0.0171442 −0.58 0.56 −0.0436837 0.0236836
Sn 1–0 −0.01 0.0159526 −0.63 0.531 −0.0413423 0.0213423
S 1–0 2.5 3.742336 0.67 0.504 −4.852641 9.852641
Ti 1–0 −0.01 0.0215455 −0.46 0.643 −0.0523308 0.0323308
U 1–0 0.009 0.0156546 0.57 0.566 −0.021757 0.039757
V 1–0 −0.019 0.0510704 −0.37 0.71 −0.1193391 0.0813391
W 1–0 0 0.004584 0 1 −0.0090062 0.0090062
Zn 1–0 −14.70999 23.91878 −0.61 0.539 −61.70368 32.2837
*Al, aluminium; Fe, i on; Mg, magnesium; Mn, manganese; Ba, ba ium; As, a senic; Cd, cadmium; Co, cobal ; C , ch omium; Cs, cesium; Cu,
coppe ; Hg, me cu y; Mo, molybdenum; Ni, nickel; Pb, lead; Se, selenium; Sn, in; S , s on ium; Ti, i anium; U, u anium; V, anadium; W,
ungs en; Zn, zinc.
in o ma ion in humans is a ailable, as well as he ole o
e a ogens o some o he hea y me al con aminan s.
Exposu e o a acks, hea y me al load and long e m implica ions
o ep oduc i e heal h
We ha e men ioned he limi s o his s udy in in es i-
ga ing he associa ion o he me al load wi h pheno ypes
a bi h. The p esen s udy is a i s s ep in his di ec ion.
None heless, he inding o an inc ease in bi h de ec s
and p e e m bi hs, compa ed wi h he incidence egis-
e ed in 2011, is a conce n.21 We can an icipa e ha ou
da a on a wide c oss sec ional con enience sample would
egis e signi ican inc eases in bi h de ec s and p e e m
bi hs by he yea 2016 (Manduca e al, submi ed 2016).
In o he pos -wa se ings, he associa ion be ween expo-
su e o a acks and nega i e ep oduc i e ou comes was
epo ed.18 In Gaza, by e ospec i e pedig ee analysis,20
an inc ease in bi h de ec s was epo ed s a ing in 2005,
a e he newes ai deli e ed weapons we e i s used.
Be ween 2006 and 2010, i.e. be o e and a e he Cas
lead ope a ion in 2009, he e was a signi ican inc ease
in bi h de ec in in an s,19 a ise which was con inuing
in 2011 (Manduca, unpublished). In Gaza was epo ed
in 2011 associa ion be ween he exposu e o a acks
and he con aminan load in newbo n hai o speci ic
e a ogens, i he in an was bo n wi h a bi h de ec ,
o oxican s, i he in an was bo n p e e m.22 The e is
hus some e idence o he po en ial nega i e impac on
he ou comes o p egnancies due o he in ake o hea y
me als du ing wa s.
The e was also limi ed p e ious e idence ha mos o
he hea y me als pass h ough he placen al ba ie , as we
he e documen e, and accumula e in he hai du ing e al
li e. Howe e , he c i ical le els o hea y me als capable
o nega i ely impac ing on he human emb yo and e us
a e unknown, and li le is known abou he kine ics and
modali ies o ans-placen al ans e o each indi idual
hea y me al o e ime.
We ha e epo ed ha newbo n babies in his c oss
sec ional con enience sample ha e lowe hea y me al
loads han mo he s, bu ou p esen knowledge does
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no allow o a conclusion o whe he his is eassu ing
o hei u u e heal h as in an s. Delayed e ec s we e
epo ed o in u e o exposu e o a acks among child en
as inc eased a es o ch onic illnesses, de elopmen al
p oblems and g ow h impai men s.7–10 12–16 Ou da a on
newbo n con amina ion a e only an ini ial con ibu ion
o he needed esea ch o in es iga e whe he a high
ma e nal load o weapons ela ed me als and in u e o
exposu e o he baby can p edic physical, cogni i e,
emo ional and psychological de elopmen in he in an .
We a e p esen ly add essing his issue wi h a longi udinal
assessmen .
O he long e m exposu es o hea y me als ha could
ha m he in an ’s de elopmen may occu because o he
ansmission o hea y me als om he mo he h ough
b eas eeding.
A high load o some hea y me als can in e e e wi h he
mo he ’s u u e capabili y o b ing a p egnancy o e m,
esul ing in p ema u e deli e ies o nega i e e ec s on
hei nex babies’ heal h.11 29 Mobilisa ion du ing p eg-
nancy o me al p e iously accumula ed in he mo he ’s
body is likely o occu in p egnancies emo e in ime om
hei in ake, and he e u n o s o ed hea y me als in o
he lympha ic and ascula ci cula ion may ha e delayed
e ec s on ep oduc i e heal h.21 22 The e is e idence
ha di e en hea y me als accumula e p e e en ially in
di e en compa men s o he body (eg, bone o lead,
s on ium and u anium; b ain o me cu y, cadmium and
aluminium; kidney o cadmium, me cu y, ch ome, lead
and plu onium), and ha om hese o gans, he me als
can be mobilised du ing subsequen p egnancies, ia
o gan and issue emodelling, and he de elopmen o
he placen a, bu he ex en and de ails o hese mobilisa-
ions a e la gely unknown.
Gene alising he meaning o he s udy
The esul s o his s udy illus a e ha in Gaza, a speci ic
high load o hea y me als is associa ed o all he women
in he c oss sec ional con enience sample wi h he
exposu e o mili a y a acks in 2014, and widesp ead
con amina ion o many hea y me als was associa ed wi h
he use o weapon y in p e ious a acks. These e idences
suppo he possibili y o immedia e and long e m isks
o heal h posed by weapons associa ed hea y me als and
wa emnan s. They sugges ha he isks posed by he wa
emnan s a e di use, may no be limi ed o ep oduc i e
heal h and may also a ec he equency o pa hologies
such as cance s, male s e ili y, immuni y and endoc ine
diso de s, hus in e es ing all sexes and ages, as he insu -
gence o hese pa hologies can be in luenced by hea y
me al exposu e and is no iceable ha hey a e epo ed
by medical sou ces, on he ise in Gaza.8–11
The con amina ion documen ed in he c oss sec ional
con enience sample by po en ial e ec o s o non-com-
municable diseases sugges s new in es iga i e lines in
s udying hei e hology.
The ele ance o he local con ex needs o be unde -
lined as he i was he i s de e minan ha made ou
esea ch possible. The e a e ac o s in he Gaza S ip ha
aided conduc ing human s udies which would ha dly be
possible elsewhe e: good medical s uc u es, collabo a i e
communi ies wi h s able composi ion and esidences, and
s agna ing o es ic ed indus ial p oduc ion (al hough
imposed by he siege and nega i e o he well-being o he
people), independen documen a ion om in e na ional
obse e s o iming o a acks and o kind o weapons
used , and consul ing help o en i onmen al issues. The
collabo a i e con ex also allowed he de elopmen o a
ques ionnai e sui able o u he su eillance o heal h.
To ully unde s and he implica ions o heal h o
hese indings we need u u e s udies in ol ing a a ie y
o p o essional ap i udes. Resea ch is needed on he a e
o hea y me als in he human o ganism, pa icula ly in
ela ion o he elease om he mo he ’s o gan du ing
emodelling in p egnancies. Addi ionally, esea che s
should explo e he mechanis ic aspec s o he molecula
ac ion o each hea y me al, and longi udinal s udies can
iden i y and e i y he endpoin s o diseases o e ime.
Cu en ly, knowledge o all o hese ma e s is limi ed.
Gi en ha he weapon y used in many o he cu en
mili a y ope a ions in o he coun ies is o en manu ac-
u ed by he same i ms as he weapon y used in Gaza,
ou obse a ions may be ele an in designing s udies in
o he se ings.
conclusIons
The long e m e ec s on heal h due o con amina ion by
emnan s o wa con aining hea y me als needs conside -
a ion in associa ion wi h o he long e m e ec s o wa on
popula ions, including he auma o wa and wa ela ed
economic and s uc u al damage.
Su eillance a bi h, bio-moni o ing and he s udy
o ou comes o ma e nal and newbo n heal h mus be
main ained as s able p og ammes, as hey p o ide he
mos sensi i e i s sen inels o s udies o he sequelae
o an h opogenic con amina ion and can p o ide ale s
abou inc eases in damaging heal h condi ions. They also
p o ide solid in o ma ion in insic o p ospec i e da a
collec ion. Su eillance a bi h is ela i ely easy o imple-
men , and i s ou come in o ms he gene al isks o he
popula ion and helps ailo public heal h in e en ions
and p e en i e p ocedu es.
Re ospec i e and longi udinal in es iga ions should
be unde aken o in es iga e he e ec s o hea y me al
con amina ion on non-communicable diseases
Fu he esea ch on he long e m heal h damage
caused by exposu e o hea y me als is needed. Addi ionally,
plans o amily counselling, p e en ion and emedia ion
should be de eloped. These e o s equi e he suppo o
he scien i ic communi y and he in ol emen o an a ay
o p o essionals om di e en disciplines. Ou s udies
p o ide a backg ound o o he s o be implemen ed in
o he se ings whe e, in simila ashion as in Gaza, gene al
heal h may be h ea ened by hidden emnan s o wa in
he p esen and o he nex gene a ions.
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In summa y, in Gaza, con amina ion by hea y me als
ha pe sis in he en i onmen and hei con inuing
accumula ion in indi iduals a e ongoing isk ac o s o a
a ie y o heal h ou comes in he a e ma h o wa .
Acknowledgemen s Fab izio Minichilli, esea che , and Fab izio Bianchi, Resea ch
Di ec o Uni o En i onmen al Epidemiology, Ins i u e o Clinical Physiology, Pisa,
I aly, p o ided signi ican suppo in hes a is ical analysis.
Con ibu o s Con ibu o ship s a emen . PM de eloped he ques ionnai e used
o collec he da a, di ec ed he analy ical wo k and elabo a ion o he da a wi h
s a is icians, w o e he manusc ip , and p epa ed he igu es and e e ence
lis . SYD di ec ed he o ganised ield wo k in h ee hospi als, and he ollow-up
objec i e assessmen o damages, and con ibu ed o he de ini ion o he wo k
and e iew o he manusc ip . NMAA di ec ed he o ganised ield wo k in one
hospi al and con ibu ed o he de ini ion o he wo k and e iew o he manusc ip .
SRQ pa ecipa ed in he planning o he s udy and e iew o he manusc ip . R-LP
launched he idea o he s udy and pa icipa ed in he planning o he wo k and
i s d a and e iew o he manusc ip . All con ibu ed au ho s had access o and
e ised he da a.
Compe ing in e es s None decla ed.
Pa ien consen Yes.
E hics app o al The Pales inian Heal h Resea ch Council and he Helsinki
C’ommi ee o E hical App o al app o ed he s udy, and he Resea ch Boa d o he
Islamic Uni e si y o Gaza, Pales inine, e iewed and accep ed he esea ch ools and
p ocedu es. The women p o ided w i en in o med consen o hei own and hei
newbo ns’ pa icipa ion.
P o enance and pee e iew No commissioned; ex e nally pee e iewed.
Da a sha ing s a emen Ex a da a can be accessed ia he D yad da a eposi o y
a h p:// da ad yad. o g/ wi h he doi:10.5061/d yad.k 846.
Open Access This is an Open Access a icle dis ibu ed in acco dance wi h he
C ea i e Commons A ibu ion Non Comme cial (CC BY-NC 4.0) license, which
pe mi s o he s o dis ibu e, emix, adap , build upon his wo k non-comme cially,
and license hei de i a i e wo ks on di e en e ms, p o ided he o iginal wo k is
p ope ly ci ed and he use is non-comme cial. See: h p:// c ea i ecommons. o g/
licenses/ by- nc/ 4. 0/
© A icle au ho (s) (o hei employe (s) unless o he wise s a ed in he ex o he
a icle) 2017. All igh s ese ed. No comme cial use is pe mi ed unless o he wise
exp essly g an ed.
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g oup.bmj.com on Sep embe 28, 2017 - Published by h p://bmjopen.bmj.com/Downloaded om
mo he s and newbo ns
o hea y me al con aminan s in he hai o
mili a y a acks in 2014 in Gaza and he load
be ween he exposu e o p egnan women o
A c oss sec ional s udy o he ela ionship
Raiija-Leena Punamaki
Paola Manduca, Sa wa Y Diab, Sami R Qou a, Nabil MA Alba qouni and
doi: 10.1136/bmjopen-2016-014035
2017 7: BMJ Open
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