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*Corresponding author: E-mail: samiraalaani@hotmail.com; 
 
 
 

Asian Journal of Immunology 
 
3(1): 1-10, 2020; Article no.AJI.53605 
 

 
 
 

 

High Rates of Birth Defects in Fallujah, Iraq: 
Radiological and Chemical Pollution of the  

Affected Children and their Parents 
 

Samira Telfah Abdulghani Alaani1*, Mohammad Tafash2,  
Abdulkadir Abdulkareem Murie1 and Allawi Muhyee Al-Esawi1 

 
1
Fallujah General Hospital, Fallujah, 00964, Anbar Province, Iraq.  

2Medical College, Anbar University, 00964, Ramadi, Iraq. 
  

Authors’ contributions 
 

This work was carried out in collaboration among all authors. Authors STAA and MT designed the 
study, performed the statistical analysis, wrote the protocol and wrote the first draft of the manuscript. 

Author AAM managed the analyses of the study. Author AMAE managed the literature searches.  
All authors read and approved the final manuscript. 

 
Article Information 

 
Editor(s): 

(1) Dr. Jaffu Othniel Chilongola, Department of Biochemistry and Molecular Biology, Kilimanjaro Christian Medical University 
College, Tumaini University, Tanzania. 

Reviewers: 
(1) Trupti Pandit, Wayne Memorial Hospital, USA. 

(2) Einar Arnbjörnsson, Skane University Hospital, Lund University, Sweden. 
Complete Peer review History: http://www.sdiarticle4.com/review-history/53605 

 
 

  
 

Received 22 October 2019  
Accepted 27 December 2019 

Published 09 January 2020 

 
 

ABSTRACT 
 

Background: Lack of birth registers hindered knowledge of the frequency of birth defects (BD) in 
Fallujah, Iraq and comparison of changes in prevalence in time. One study found correlation 
between BD presentation and teratogenic metal load [1]. 
Methods: We obtained reproductive history, kin health, environmental exposure and historical 
residence of families. Hair was sampled from the nape of the neck from families and analyzed by 
ICP/MS for metal content. 
Findings: BD in newborn in 2010 were about 14.7% [2]. Data of reproductive history from 56 
couples with child, overcoming the lack of previous data, shows pattern of increase in BD 
presentation since 1991. Information on parent's immediate kin in more than 1000 people, supports 
that BD are sporadic events. High residential stability of families allows to rule out local clusters for 
BD. Focus on load for ten teratogenic and carcinogenic metals (V, Cr, Co, As, Mo, Cd, W, U, Hg, 

Original Research Article 



 
 
 
 

Alaani et al.; AJI, 3(1): 1-10, 2020; Article no.AJI.53605 
 
 

 
2 
 

Pb) in hair of 43 BD children and 103 their parents, and of 11 healthy newborns and 16 their 
parents, compared with that of 10 children and 8 adults controls outside the war area, shows that 
metal contamination is diffuse in the whole Fallujah population and is present already in newborn 
children hair. Absolute levels of major teratogenic and carcinogenic contaminants (V, Co, Mo, U 
and Pb) were significantly higher in Fallujah people than in controls from other areas, with Pb levels 
in BD children higher than other newborns in Fallujah. 
Interpretation: Unusual high prevalence progressive in time and increased load of teratogenic 
metals even in new born hair are reported in Fallujah population. The extensive metal 
contamination persistent in people's hair in post-war environment and the composite metal load 
might be a major factor in the increase in time of stochastic events that lead to BD presentation. 

 
 
Keywords: Fallujah; congenital anomalies. 
 
1. INTRODUCTION 
 

Understanding potential long term effects of 
recent wars on civilian's health requires 
monitoring rates of birth defects, cancers and 
chronic pathologies. Often, lack of pre-existing 
records constitutes hindrance. In Fallujah, alarm 
on severely declining reproductive and children 
health come from doctors, reports from human 
right groups and political figures [3]. 
 

Moreover, modalities of the presentation of BD, 
relative frequencies, and causes of their recent 
increase have not been investigated, nor 
teratogens have been searched for, and 
mechanistic aspects remain largely unknown till 
2011 when the 1

st
 study on limited number of 

babies with birth defects & their parents done & 
showed strong correlation between the 
development of birth defects & the presence of 
metal load in the investigated sample. 
 

A first task is to collect recent data on 
prevalence of BD and to attempt a reconstruction 
of past events; recording reproductive history at 
registration, with specific questionnaire, is a 
valuable mean to achieve that aim [4]. Together 
with the information on health status (BD 
presentation) within members of the immediate 
family of the parents of BD children, this 
information allows to dismiss that monogenetic, 
high penetrance genetic factors pre-exist in the 
parents of BD children [5]. 
 

Candidate gene effectors are unknown for 
most structural BDs, and for all a relevant 
component, generically called, of environmental 
and/or maternal effect is acknowledged [6]. It is 
unknown the number of genes contributing to 
anencephaly in humans, and, in mice. 
 

Anencephaly is attributed to multifactorial 
combinations of hypomorphs and low-

penetrance heterozygotes [7]. CHD have various 
phenotypes, sometimes compounded with 
different cardiac-unrelated features and cohort 
studies detected with very low frequency single 
genetic mutations putatively involved, while 
approximately 30% of CHD and tetralogy of 
Fallot (TOF) are associated with wide genomic 
rearrangements (chromosome translocation, 
copy number variation and chromosome 
trisomies) [8]. Combinations of genetic and non-
genetic factors is associated to inheritance of 
CLP in mice [9]. Also in mice, synpolydactyly is 
linked to Hoxd13 mutations and its manifestation 
is dependent upon environmental factors [10]. 

 
The traditional paradigm of prevalence data 
surveillance has been that detection of a 
particularly high prevalence of BD in one 
particular population, or a sudden increase in 
prevalence over time, can help identify 
possible environmental causes. Presence of 
teratogenic metals in the war/post-war 
environment is expected because of the weapon 
systems used and proofs of fact of their 
presence in weaponry used in the Middle East 
wars were reported [11]. Metals persist in 
environment, are up taken via respiratory, skin 
contact and ingestion of contaminated water or 
food, and accumulate and persist in the hair of 
exposed people's [12]. Metal exposure, acute 
and/or chronic has the potentials to induce 
reproductive and neoplastic damages, via 
epigenetic changes [13-16] by regulating 
genome stability, X chromosome inactivation, 
gene imprinting, and reprogramming gene 
expression. Metals act as metalloestrogens [17], 
inhibit DNA repair and alter DNA methylation, 
change transcriptome and microRNAs 
production [13], histone acetylation [18]  and 
methylation [19,20] oxidative DNA damage [21] 

all of which can lead to birth defects, whether 
translated into mutations or not [21,22]. 



 
 
 
 

Alaani et al.; AJI, 3(1): 1-10, 2020; Article no.AJI.53605 
 
 

 
3 
 

Some metals can induce sporadic gene 
mutations because of internal radiation and is 
unclear the relative relevance of radiation versus 
chemical activities of DU as a mutagen, while it 
was shown to induces epigenetic changes via 
hypomethylation of DNA [20,21,22]. 
 

It was not previously attempted to conduct 
investigation of the association between 
presentation of BD families and metal load in 
post-war contexts, while studies of industrial or 
mine derived metals pollution have implied this 
correlation. The residential history of the parents, 
their exposure to major war events, the source of 
drinking water, all contribute to define the 
environmental context. 
 

Here we report an observational investigation at  
Fallujah General Hospital of 56 families with BD 
and 11 controls inclusive of all the information 
above, and results of ICP/MS analysis to 
determine load of ten teratogenic metals in hair 
of newborns and their parents, with or without 
BD and of children and adult controls from Italy 
and Jerusalem. 
 

2. METHODS 
 
Collection of data (Supplementary Fig. 1) was 
done by medical personnel. Information 
included reproductive history, information on 
health of parent's brothers and sisters, historical 
residence and environmental exposure. 
 

Classification of birth defects was according to 
definition of the primary phenotype. Patients and 
controls were taken in order of arrival, among 
those that accepted in writing to answer to 
questionnaire, and consenting to the scientific 
use of data. Pedigrees of families are as 
standard. Clinical diagnosis was assisted by the 
use of instrumental diagnosis (Xrays,  
Echocardiography, CT scans, MRI) as 
appropriate. Samples of hair of about 2 cm 
length from the nape of the neck were used for 
metal load determination by ICP/MS, as 
recommended by IAEA [12]. 
 

Hair samples treatments, digestions and analysis 
were as reported [23]. XSERIES 2 ICP-MS 
(Thermo Fisher Scientific,  Germany)  was  used  
in  the  standard  configuration,  with  ASX-510  
auto-sampler  (Cetac,  USA). Additional details in 
supplementary file. For statistics, continuous 
variables were expressed as median and range, 
due to their non-normal distribution (assessed by 
Shapiro-Wilk test) and compared using Mann-
Whitney U test. Categorical variables are 

expressed as percent and compared with Chi-
square test for trend. Two-tail P values <0.05 are 
considered significant. 
 

3. RESULTS 
 
The frequency of birth defects was registered at 
the Fallujah General Hospital from November 
2009 to September 2010. Total number of 
deliveries were 5896 of which 869 birth defects, 
with a frequency of 14.7% [24]. In addition, as 
example, in the month of May 2010 with a total 
547 deliveries, there were also 75 premature 
births of which 60(10.9%) late miscarriages (after 
30 weeks) and 10 stillbirths (1.8%). 
 
We classified the BD according to the major 
primary defect. Many of the BD children show 
also additional defects in other body 
compartments, as often the case. The frequency 
of the different classes of BD in these ten months 
was:  CHD  -  Congenital  heart  defects,  include  
ADS,  VDS,  TOF,  33%;  NT-neural  tube  
defects,  include anencephaly (possibly 
underestimated, since it causes miscarriages 
which can be lost to hospitalization), spina bifida, 
hydrocephaly, cerebral palsy, 28%; CLP-cleft 
lip/palate, 14%; "others"-22%. Frequencies of 
relative prevalence are not significantly different 
from elsewhere [5,23]. 
 
Data collection from 56 families with BD, 31 of 
them registered in the Hospital for delivery or 
miscarriage between April and September 2010 
and 25 that returned for check up in these 
months, and from 11 families with a newborn 
normal child, included reproductive history, 
health of collateral kin (brothers and sisters) and 
its progeny, environmental and residential 
information and was done using the 
questionnaire in Fig. 1S. 
 

The population studied is highly stable in historic 
residence and converge to the hospital from 
different areas of town. The exposure to war 
chemicals in the environment is reported by 
subjective record: most of the parents in the 
study were present at the time of massive 
attacks to the town in 2004 and/or 2005, cleared 
rubble, assisted victims and families 116, 119, 
120, 132, 142 rebuilt their own house on the 
remains a bombed one. All mothers declared 
good to optimum quality of nutrition during 
pregnancy; most families studied are of large 
size. These data are shown by examples in 
Table 1 and in full in Table I 1S for reproductive 
history of families with BD, Table I 2S for kin and 



 
 
 
 

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4 
 

environmental information of families with BD, 
and Table I 3S, for pedigrees, kin and 
environmental information of Iraqi control 
families. Among the 56 families with BD, 41.36% 

were CHD, 25.4% NT, 4.7%, CLP, 14.3% 
Skeletal defects (SK), and 14.3% "others", in 
similar trend with the prevalence in wider 
population, above. 

 

 
 

Fig. 1. Prevalence of miscarriage and birth defects in different time periods in Fallujah. p< 
0.001 for changes of BD prevalence and p< 0.062 for changes of Miscarriage prevalence 

 

 

 
 

Fig. 2. Hair metal load in ppb, in children (panel A) and in adults (Panel B). Columns 
correspond to control from Italy (black bars), controls from Jerusalem (dark grey bars), 

controls from Fallujah (light grey bars) and BD from Fallujah (white bars). * p<0.05 vs controls 
from Italy; § p<0.05 vs controls from Jerusalem 

 



 
 
 
 

Alaani et al.; AJI, 3(1): 1-10, 2020; Article no.AJI.53605 
 
 

 
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Table 1A-  Birth defects- Family History 
 

 

Table 1B –Birth defects- kin and environmental exposure 
 

N/sex/age BD House/vicinity Rescue/ 
clearing 

Acute 
symptoms 

Sibling 
number 

Sibling+progen 
With BD 

Residence2003
/10 

  bombed WP      
145/M/32 CHD-

CA 
Y2004/N N Y    Fallujah,north 

145/F/30  Y2004/N N Y    Fallujah.north 
156/M/33 NT Y2004/N N Y N 7 11 Fallujah,Nazzal 
156/F/33  Y2004/N N Y N 8 4 Fallujah,Alaskari 
131/M/42 SK-O Y2004/N N Y N 3 26 Fallujah,Nazzal 
101/F/23 O-NT Y/Y2004 Y Y Y 7 2 Albaghdadi/ 

2007 Fallujah, 
Althubbadh 

9/M/35  Y/Y Y Y N 10 25 Fallujah, 
Alandulus 

9/F/32  Y/Y Y Y N 10 1 Fallujah, 
Alandulus 

A-Reproductive history of families;a,b)with birth defect children,born in 2010. C,d)with birth defect children born before 2010.e) 
heathy child. B-corresponding data on exposure to war events,kin number and health,residence since 

 
empty= healthy 
 

filled in black= birth date 
 
filled in grey= dead 

male                         ██ 
 

female                                           

unknown sex                              
twins 
still born 
 
miscarriage           
 
 



 
 
 
 

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Table 2. Progeny with BD of families with reproductive history starting before the year 2000 
 

 
Families were selected for one BD in their reproductive history after 2003, and because their reproduction 

spanned  from before 2000 up to at least 2006. normal-healthy child; BD-birth defect; MS miscarriage.  BD and 
MS are listed in order of presentation in time in each family: CHD congenital hearth disease, NT neural tube, CLP 

cleft Lip/Palate, SK skeletal malformation, kidney here stays for atrophic 
 

More than one case of same BD was present in 
some families: NT in 123 and 105, and CHD in 
131 and 145; families 101, 107, 106, 131,132 
had children with major defects of different 
phenotypes. In all of these there was no BD in 
the immediate kin. 
 

Given to incomplete responses, we have full 
information only of 50 families on kin, 
environmental exposure and residence. These 
include the health state with respect to BD of 552 
siblings and 665 progeny (total 1217). The health 
information is incomplete by defect, since some 
parents were not informed fully of the health 
status of all of their kin. Seven cases of birth 
defects were registered and two infant deaths. 
These involved 5 families, with families 136 and 
138, with CHD children, and a CHD presented in 
the progeny of the father's siblings, potentially 
due the presence of a genetic mutation on the 
father side. Different defects from those in the 
family of reference were reported in the progeny 
of the mother's  sibling in family 1, and in the 
progeny of the father's  sibling in family 114. For 
all, the whole extended family resided in the 
same neighbour, throughout the last 7 years. 
 
Among the 56 families, there are 17 whose 
reproductive life started since at least 2002 and 
back up to 1992. The presentation of BD in time 
increased significantly stepwise during the 
observation period, from 0.017 in 1991- 2000 to 

0.615 in 2007-2010 (Fig. 1 and Table 2). If all the 
families with one BD in the last 6 years are 
considered, regardless of the extension 
backward of their reproductive life, similar results 
of distribution and same significance (p<0.001) 
for the trend in BD are obtained (supplementary 
Table II S). The frequency of miscarriages versus 
births at term also is significantly different, in both 
cases, comparing these periods of time 
(p<0.0062 for the 17 and p<0.0003 for the 56 
families, respectively), but has a different pattern 
than that of BDs. Miscarriages were most 
frequent in all families in the time interval 2004-
2006. 
 
We measured the load of teratogenic/mutagenic 
metals in the hair of parents and their children 
with birth defects delivered in Fallujah Hospital 
between April and September 2010, and of 25 
families returning for control visits of children with 
birth defects born in the last 6 years. We also 
collected hair samples from 11 families with 
normal children in the same hospital, from 
families in Italy and from Arab children in 
Jerusalem, without familiar records of BD. All 
participants gave their informed consent to use 
and delivered the data in scientific study. 
 

Metal concentrations in hair was measured by 
ICP/MS for ten toxic and carcinogenic metals (V, 
Cr, Co, As, Mo, Cd, W, U, Hg, Pb) also 
components of weapons, and are expressed in 



 
 
 
 

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7 
 

ppb, in graphical form in Fig. 2 and in full 
(supplementary Table III 1S for children and 
2S for adults). BD children analyzed were 32 
newborn and 13 between 6 months and 7 years 
of age, for a total of 45. The group of 11 Iraqi 
children without BD was registered without any 
selective criteria among the newborns in the 
period of the study. The group of Italian (from 
Genoa and Naples, both industrial and traffic 
polluted large towns) and Jerusalem Arab 
children, all between 6 months and 7 year  of  
age,  were  taken  randomly  among                    
families  with  no  BD. The adults group  
analyzed include the corresponding parents for 
BD and all controls (with few exceptions where 
one of the parent refused to donate or was  
bold). 
 
While for As and Hg there are no differences in 
all groups, and W is lower in all Iraqi than 
outside Iraq controls, the hair metal load in 
children is significantly higher in control subject 
from Fallujah than in controls from Ital y for Co, 
Mo, U, Cr, V and Pb. The same holds true for 
children with BD from Fallujah relatively to Co, 
Mo and Pb (Fig. 2, A). Differences in hair metal 
load is reported for adults in Fig. 2, B. Co, Mo, U, 
V, and Cr were significantly higher in parents of 
BD children than in controls from Italy. In 
addition, Cd and U were also greater in controls 
from Falluhja with respect to Italian controls. In 
Fig 1, A, BD children were grouped regardless of 
their age (newborns and 6 months to 7 years), as 
there was no significant differences between the 
two groups in load for any of the ten metals 
considered (supplementary Table III 1S). 
Subgroups comparison between CHD and NT 
children for the load of each of the ten metals, 
showed no significant differences, suggesting 
that there is not specific metal association with 
one kind of these BD (not shown). We left out 
from the statistical analysis family 119 (Table III, 
S2), whit a much higher level of all the toxicants 
that all the other families. This family is one of 
four in this report living in an house rebuilt on 
the previous one bombed. Outliners were also 
observed in other families, being more frequent 
for Hg and Pb. 

 
In terms of absolute amounts for all elements 
significantively higher in all the population in 
Iraq, these are between 2-5 and more in median 
values than experimental controls, amounts 
available in the literature, and those previously 
obtained by our group for another group of ten 
Italian healthy people of age from 2 to 60 years 
(not shown). 

4. DISCUSSION 
 
In cases where a rapid increase in prevalence 
of birth defects is suspected/observed, there 
might be clustering of referrals to the structure 
where the investigation is undertaken. We have 
no reason to think that in this case since Fallujah 
General hospital is the main and the largest 
public structure in the area, and people convey 
to it from different areas of town, as shown by 
the residence of parents. Prenatal diagnosis and 
therapeutic abortions are not implemented in 
Fallujah, determining a slight overestimation in 
comparison with data from countries where these 
are practiced. Even taking this in consideration, 
the frequency of BD detected in Fallujah is 
unusually high compared with those reported in 
the literature [4,23] usually not exceeding 6%. 
The data of prevalence are also susceptible of 
underestimation, due to limited  availability of 
instrumental  tools  for  diagnosis, with  possible 
oversight of minor BD. Nonetheless, the 
distribution for kinds of different major BD is 
similar to what reported in the world [4,23]. 

 
Modality of the presentation in the families with 
a BD child is in the majority of cases sporadic 
and occasional, consistent with the possibility 
that BD are novel events due to dominant 
mutation and/or to epigenetic changes during 
gametogenesis or early embryogenesis. Among 
the cases where more than one child with BD 
was born to the same parents, in three cases 
they differed in phenotypes and there was no 
BD in the immediate kin. This is most 
adequately interpreted on the ground of 
environmental/mother genetic background or 
epigenetic origin for the multiple events of BD 
[25,26]. In the few families with recurrence of 
the same BD in children, two NT and one with 
two CDH, a supplement of study may be 
required as to possibility of genetic changes. 
Similar criteria apply in the cases of occasional 
recurrence of different or same BD in children in 
the kin of the family of reference. A persistent  
environmental  effect  in  the  siblings,  
associated  to  a  generic  "predisposition"  and  
same  historical residence can explain the 
recurrences as well as the occurrence of BD with 
different phenotypes. 
 
The historical reconstruction shows that 
frequency of BD in the last ten years of the last 
century was less that 2%, and that of 
miscarriages about at 5%, similar to that 
reported for other not heavily industrialized 
countries. The differences with the past in the 



 
 
 
 

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8 
 

following time windows are highly significant. 
These also show the different pattern of increase 
of BD and MS. Miscarriages increase, but with a 
different pattern than BD and the maximum is 
coincident with the years of major attacks to the 
city and decline from 2007, which may suggest 
that MS are an acute and shorter term response 
to the environmental changes. For BD, our data 
do not allow to know if and when the increase 
will stop and suggest that these are caused by 
accumulation of the environmental effectors. The 
fact that the presentation rate of birth defect is 
not declined in the last years suggest 
permanence in the environment of teratogenic 
substances. 
 
Metal load in teratogens (V, Co, Mo, U and Pb) 
is high in the whole population in Fallujah. If we 
adopt, as suggested from the sporadic and 
random presentation of BD the epigenetic 
paradigm, then this observation, assumes major 
relevance. 
 
It is known that toxicant metals compared to 
other known war-contaminants have longer 
persistence in the environment, accumulate in 
the organs, act on multiple functions and are 
capable to induce sporadic epigenetic changes 
of great impact during gametogenesis and 
embryo development; interactive effects of 
multiple metal toxicant were suggested and are 
still largely undocumented, while is described 
their capability to unbalance the amounts of 
essential metals in the organism [25-28]. The  
toxicants  which have increased load in the 
whole Fallujah population  are known for their  
capability to  interfere  with  embryo  
development and  may  be relevant in  the 
induction of  MS as acute response,  and of BD, 
as long time effect.  
 
Here we show association of high load of Co, Mo 
and Pb with all children, Pb being specifically 
highest in BD children, and of U and V in control 
Fallujah children. The load of these elements 
differs from that in adults who all have an U load 
higher in all controls outside Iraq, and parents of 
BD children showing Co, Mo, V, and Cr higher 
than that in all the adults groups. Although the 
metal load in newborn children hair must 
derive  from mother's exposure, these results 
show it does not reflects it immediately, 
suggesting the need of further study on the 
repartition of  the load of different metals during 
embryo and foetal life, which may be relevant in 
understanding the mechanisms of metal's 
teratogenic action. Notwithstanding the low 

mutagenic performance of teratogenic and 
carcinogenic metals, their effects are 
nonetheless important and transmittable to 
daughter cells within a lineage and 
transgenerationally in mammals [25-28]. via a 
mechanistic framework which suggests 
transmission of epigenetic modifications as a 
mechanism alternative to germ-line mutagenesis. 
By their multiple mechanisms of action metals 
can determine the alteration of functionality of 
cell lineages, organogenesis and homeostasis in 
the adult, and the type of cells in the body 
affected by metals range from somatic cells, also 
within the developing embryo, to germ cells, both 
of male and female [29]. The relevance of 
increase even of moderate amount in 
teratogenic metal load, and the possible 
combinatorial effects of their co presence is 
alluded to in many reports but need further 
studies to be fully understood. 
 

5. CONCLUSION 
 
We here reported mainly on two aspects related 
to the birth defects presentation, its frequency, 
much higher than in the world and of that 
retrospectively assessed in the place before the 
2003 war, and the observational study that 
indicates that the metal load of Fallujies, in 
general is unusually high for metals associated 
with weaponry. That is not enough to establish a 
cause-effect relationship, but is indicative of 
muted environmental that can condition 
differently MS and BD presentation and indicates 
a path to follow for future studies. 
 
The application of the historical method of 
recording births gave us a convenient tool for 
obtaining needed retrospective information and 
could be implemented for all registrations in 
countries where registration data have not been 
recorded in the past. 
 

We hope this knowledge will also help to 
propose studies directed to the management of 
the issue along lines of prevention and therapy. 
 

CONSENT AND ETHICAL APPROVAL 
 
As per international standard guideline 
participant consent and ethical approval has 
been collected and preserved by the authors. 
 

COMPETING INTERESTS 
 
Authors have declared that no competing 
interests exist. 



 
 
 
 

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