Journal of Social Work in Disability & Rehabilitation

ISSN: 1536-710X (Print) 1536-7118 (Online) Journal homepage: http://www.tandfonline.com/loi/wswd20

Environmental Exposures to Metals in Native
Communities and Implications for Child
Development: Basis for the Navajo Birth Cohort
Study
Johnnye Lewis, Melissa Gonzales, Courtney Burnette, Malcolm Benally,
Paula Seanez, Christopher Shuey, Helen Nez, Christopher Nez & Seraphina
Nez
To cite this article: Johnnye Lewis, Melissa Gonzales, Courtney Burnette, Malcolm Benally,
Paula Seanez, Christopher Shuey, Helen Nez, Christopher Nez & Seraphina Nez (2015):
Environmental Exposures to Metals in Native Communities and Implications for Child
Development: Basis for the Navajo Birth Cohort Study, Journal of Social Work in Disability &
Rehabilitation, DOI: 10.1080/1536710X.2015.1068261
To link to this article: http://dx.doi.org/10.1080/1536710X.2015.1068261

Accepted online: 07 Jul 2015.Published
online: 07 Jul 2015.

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Date: 16 September 2015, At: 10:46

 Journal of Social Work in Disability & Rehabilitation, 0:1–25, 2015
Copyright # Taylor & Francis Group, LLC
ISSN: 1536-710X print=1536-7118 online
DOI: 10.1080/1536710X.2015.1068261

Environmental Exposures to Metals in Native
Communities and Implications for Child
Development: Basis for the Navajo Birth
Cohort Study

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JOHNNYE LEWIS, MELISSA GONZALES, COURTNEY BURNETTE,
and MALCOLM BENALLY
University of New Mexico Health Sciences Center, Albuquerque, New Mexico, USA

PAULA SEANEZ
Growing in Beauty, Window Rock Agency, Navajo Nation Office of Special Education and
Rehabilitation Services, Window Rock, Arizona, USA

CHRISTOPHER SHUEY
Uranium Impact Assessment Program, Southwest Research and Information Center,
Albuquerque, New Mexico, USA

HELEN NEZ, CHRISTOPHER NEZ, and SERAPHINA NEZ
Tachee Uranium Concerns Committee, Blue Gap, Arizona, USA

Two disparate statistics often cited for the Western United States
raise concern about risks for developmental disabilities in Native
American children. First, 13 of the states with the highest percentage of Native American population are located in the Western
United States (U.S. Census Bureau, 2012). Second, more than
161,000 abandoned hard-rock mines are located in 12 Western
states (General Accounting Office, 2014). Moreover, numerous
studies have linked low-level metals exposure with birth defects
and developmental delays. Concern has emerged among tribal
populations that metals exposure from abandoned mines might
threaten development of future generations.

Address correspondence to Melissa Gonzales, PhD, Associate Professor, University of
New Mexico Health Sciences Center, MSC09 5360, Albuquerque, NM 87131-0001, USA. E-mail:
mgonzales@salud.unm.edu
Color versions of one or more of the figures in the article can be found online at
www.tandfonline.com/wswd.
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J. Lewis et al.

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KEYWORDS birth defects, children, developmental delay, disabilities, exposure, health promotion, metals, Native American

More than 161,000 abandoned hard-rock mines are located in 12 Western states
(General Accounting Office [GAO], 2014). Thirteen Western states have the
highest percentage of Native American population in the country (U.S. Census
Bureau, 2012), creating concerns about the potential for Native American communities in the West to experience disproportionate exposures to mixtures of
heavy metals associated with developmental delays and disabilities. Abandoned
uranium mines account for more than 4,000 of the 161,000 abandoned
hard-rock mines (U.S. Environmental Protection Agency [U.S. EPA], 2008a). In
Navajo Nation specifically, more than 500 abandoned mines remain as the legacy of Cold War mining. These mine wastes represent mixtures of metals including not only uranium, but also arsenic, copper, and other heavy metals, as well
as remaining radionuclides. No systematic investigation has been undertaken to
understand how exposures in the numerous rural tribal communities in proximity to these wastes might affect health, especially in children. The mine sites are
most often unmarked, unfenced, and the historical memory of their location is
being lost in the communities. Our research team, working with many Navajo
communities, has observed children in direct contact with these mixed metal
wastes (see Figure 1). Many successive generations in the communities have
grown up in close proximity to these wastes, both during the active mining
era and now, when the unremediated legacy wastes remain in their communities (see Figure 2). In 2007, in response to numerous requests from Navajo
Nation and affected communities (McSwain, 2007), Congress implemented

FIGURE 1 Navajo children walking at the foot of unremediated uranium mine waste pile circa
2007.

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Environmental Metals and Child Development

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FIGURE 2 Navajo child watches as 18’’ of contaminated soil is removed from his community.
Note gray uranium mine waste pile in upper right. Additional mine waste is located to his left.

the first steps to address this problem through a Five-Year Plan to address
uranium contamination on the Navajo Nation (U.S. EPA, 2008b). In 2010 the first
health study was added to that plan to understand the relationship between
exposures to uranium mining wastes, birth outcomes, and developmental
delays in this population: the Navajo Birth Cohort Study (NBCS). Authors of this
paper are members of the NBCS study team, including Dr. Lewis, NBCS Principal Investigator. No systematic assessment of the prevalence of adverse birth
outcomes and developmental disabilities or delays has been done in this population, despite early suggestions of a potential link between these exposures and
congenital malformations (Shields, Wiese, Skipper, Charley, & Benally, 1992).
In this article, we discuss (a) the basis of community concerns for child
development in relation to exposures from both the community and the
literature perspectives; (b) how the problem is being investigated; and finally
(c) some preliminary findings that we will build on in the coming years to
answer these questions. Barriers to treatment and diagnosis that contribute
to our lack of information and limit care, and the efforts of our partners to
address those barriers, are also discussed.

CASE STUDY VIGNETTE: HELEN NEZ,
TACHEE-BLUE GAP, NAVAJO
The story of coauthor Helen Nez, a member of the Tachee-Blue Gap
community on Navajo Nation in northeastern Arizona, illustrates the concern

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J. Lewis et al.

and stress many Native Americans experience when faced with the uncertainties of what causes disabilities in their children, and their questions over
what they can do to ensure that their babies grow up and have long, healthy
lives: lives that allow them to Grow in Beauty. Her story, as told to NBCS
media specialist and coauthor Malcolm Benally, also illustrates the need for
these parents to have access to adequate and informed clinical and social
networks to support their children’s health struggles. Helen’s story, which
follows, highlights several questions that remain unanswered today regarding prevention, diagnosis, and care of Native children with disabilities.

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Helen’s Story
Helen has lived her whole life in the Blue Gap Chapter of the Navajo Nation
near Tachee, Arizona (see Figure 3). Her first child was born when she was a
25-year-old woman. She had 11 children. One of her children was stillborn.
She lost six additional children to Navajo neuropathy, a disability that was not
recognized at the time. Three of her children—Jerome Nez (1967–1970),
Claudia Nez (1970–1972), and Euphemia Nez (1975–1978)—all died before
their third birthdays. Their stomachs had become bloated and their eyes
became a cloudy gray color as they became sick. Her daughter, Dorenta
Nez, spent a month at the hospital in Albuquerque, New Mexico (131 miles
away) when she became ill. Her stomach had also become bloated and
she died coughing up blood when she was 3 years old in 1978. Two of
Helen’s children lived into early adulthood. Theresa Nez lived to be 25 years
old. She began dialysis treatments at the age of 19 and died of kidney failure.

FIGURE 3 Helen Nez in her home in Tachee-Blue Gap, Arizona.

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Cedar Nelson Nez lived to the age of 35 years. Helen’s four surviving children
are now adults and talk not only about their own milder disabilities and
recurring health problems, but about the impact of seeing so many of their
family members suffer and die in such a short time, one likening the impact
to posttraumatic stress disorder.
Through all of her ordeals with each child, their help and support came
from the local Catholic Church, Navajo and Hopi medicine men, and a social
worker named Alta Earl. An advocate, Cherie Daut-Neztsosie from Tuba City,
Arizona, had begun helping Helen document her children’s conditions, but
Cherie passed away 20 years ago before completing the task. At one point,
when Helen was determined to get medical help for her children, she was
escorted out of the Chinle, Arizona, hospital by security. Western medicine
could only say that the children’s conditions were genetic and nothing could
be done.
A physician who cared for Dorenta in Albuquerque, Dr. Snyder, was the
first to suggest to Helen that the area where she lived might be contaminated
with hazardous materials from prior uranium mining, and that exposure to
the waste might contribute to the neuropathy. It was Dr. Snyder and his
colleagues who finally identified the disabilities in Helen’s family as Navajo
neuropathy in 1976 (Appenzeller, Kornfeld, & Snyder, 1976).

COMMUNITY CONCERNS ABOUT POTENTIAL
ENVIRONMENTAL LINKS
The frustration on the part of both those affected and of providers who can
offer no solutions is clear in Helen’s story. The neuropathy that Helen’s children struggled with results in multisystem degeneration involving the liver,
central and peripheral nervous systems, and the immune system, among
others. The disability is accompanied by a failure to thrive and often results
in premature mortality due to liver failure. In 40% of children affected, this
occurs in their teens. The average age of death is 10, and onset generally
is in the first year of life. The prevalence of this disability in the Navajo
population is now recognized to be as high as 1 in 1,600 live births in certain
geographic regions of the Navajo Nation (Karadimas et al., 2006). As illustrated by Helen’s story, this disability can affect multiple members of individual families, creating even more significant impact than suggested by
the prevalence.
Helen’s community is one of many affected by the mining of uranium to
meet Cold War weapons development demands in the United States. Helen’s
home during the active mining period of the mid-1950s to the late 1960s was
located about 1 to 2 miles south of a series of what are now abandoned mines
that were operational during her childbearing years, opening in 1957. For the
Nez family and others similarly affected, their questions as to the cause of

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their children’s disabilities have continued to focus on the uranium exposures (Pasternak, 2011; Rosen & Mushak, 2000), in spite of indications that
a genetic anomaly is involved (Karadimas et al., 2006). Two of the Nez
family’s main water sources during Helen’s childbearing years were a windmill at a now-abandoned school site and a natural spring located about a
mile from their family home. The windmill, which was closed in 1999, had
evidence of contamination by manganese in a sample collected by federal
scientists in 1998, long after Helen drank from the well. No historic water
quality data for this windmill exist in available records. The spring, which
was identified by Helen’s adult son Christopher and is now covered with
mine wastes, had a uranium concentrations more than five times the U.S.
EPA maximum contaminant level when tested in 2014 by the University of
New Mexico (UNM) METALS team (see UNM, 2014). Our research team
has found no historic water quality data for this spring in available records
to compare with the recent results. Even if samples had been collected from
both sources during Helen’s childbearing years in the 1960s and 1970s, uranium and other metals were not routinely tested for in water sources during
that era.
On the Navajo Nation, greater than 30% of the population lacks access
to clean, regulated drinking water, and therefore historically they have used a
variety of unregulated and therefore untested sources for their drinking
water. In Helen’s case, she, like many others, did not understand the potential hazards of uranium mines until concerns were expressed by her chapter
in the late 1980s. Helen’s story has been repeated by several other women
and has generated hypotheses linking prenatal uranium exposure to development of Navajo neuropathy in the book Yellow Dirt by Pasternak (2011),
as well as in evidence in a toxic tort case (Rosen & Mushak, 2000).
A mitochondrial genetic mutation (MPV17) has been identified in those
affected with Navajo neuropathy (Karadimas et al., 2006), but the prevalence
of this mutation in the overall Navajo population has not yet been investigated. Nor have gene–environment interactions been investigated whereby
exposures might influence expression of a genetic susceptibility for a disease
or condition. Rather, the link of Navajo neuropathy to a genetic mutation has
caused researchers to attribute the condition to a ‘‘founder effect’’ whereby it
is hypothesized that genetic diversity in the population was reduced following the Long Walk of the Navajo people to Fort Sumner, New Mexico, in 1864
(Karadimas et al., 2006).
This founder effect has over the years been ascribed as causation for the
increased prevalence of severe combined immunodeficiency (SCID), Navajo
neuropathy, Navajo poikiloderma, and Athapaskan brain stem dysgenesis, all
occurring at higher than expected prevalence in the Navajo population
(Erickson, 1999). Although such historical events, which result in major
population reduction, have commonly been associated with increased
frequencies of recessive alleles, other researchers have pointed out that

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pedigree analyses on Navajo have not supported that hypothesis in this case
(Jones, Ritenbaugh, Spence, & Hayward, 1991). These researchers note that
Navajo marriage rules, which prohibit marriage into either the mother’s or the
father’s clan or to members of related clans, have had the opposite effect in
this culture. Their pedigree analyses suggest that rather than increased homozygosity that would result from the inbreeding predicted from the founder
effect, there might be excess heterozygosity associated with the maximized
outbreeding maintained in the culture. Also, common ancestors could only
be identified in 3 of 13 families affected by Navajo neuropathy in a 1990
study (Singleton et al., 1990). The fact remains that there has never been
an investigation of potential gene–environment interactions, or a systematic
evaluation of the role of environmental exposures on Navajo or their link to
potential genetic susceptibilities for Navajo neuropathy or other disabilities at
higher than expected prevalence in this population.

UNANSWERED QUESTIONS
The questions that remain unanswered for Helen Nez, her community, and
thousands of other Native Americans affected by the legacy of uranium
and other metal mining today include the following:
1. Has anything been done to improve diagnosis and treatment of childhood
disabilities since Helen’s experience?
2. Are community concerns about exposures to environmental metal contaminants and the health of their children and future generations well
founded?
3. Could environmental contaminants interact with genetic factors to trigger
disabilities?
4. How can we further our understanding of relationships between exposure
and disease to answer the questions in our Native communities?
As noted in articles throughout this issue, our knowledge of disabilities
in tribal communities remains limited. The lack of understanding of severity,
type, and causes of disabilities, combined with the limits in infrastructure and
resources for clinical and social service support within many Native communities can hamper the provision of optimal care and support to affected
families. Further complications arise from cultural differences in the perception of disability, and the lack of discussion of the problems associated with
disability in Native American communities, within the scientific literature and
in the academic realm in which medical and social services professionals are
trained. Differences across states in how disabilities are identified and
tracked further complicates our understanding, as does the small number
of tribal members represented in state databases and inability to access

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J. Lewis et al.

tribal-specific data within compiled data sets in many states. Data compiled
from birth records will not be consistent with those compiled over the first
few years of life to pick up anomalies not clearly presented at birth. Data
sharing agreements in some states have not been established with tribes,
limiting ability to access tribal-specific data within the state-compiled data
sets. Lack of tribal resources often limits the ability for tribes to track cases
internally, and failure to report data from tribal populations further limits
the accuracy of state data.
In the remainder of this article, we summarize what is known to answer
Helen’s questions. Helen’s community is representative not only of many
isolated Native American communities in the West, but also of other rural
communities impacted by tens of thousands of abandoned hard-rock mines,
a subset of which are abandoned uranium mines from the Cold War era.
Therefore, answering Helen’s questions will have relevance for all of these
communities living in proximity to these abandoned sites.

Has Anything Been Done to Improve Diagnosis and Treatment of
Childhood Disabilities since Helen’s Experience?
As highlighted in a 2009 review, 7.9 million people are born each year with a
birth defect; 3.3 million a year die before the age of 5 from the defect; and 3.2
million of those surviving face mental or physical disability for life
(Weinhold, 2009). In the words of Ted Schettler, Science Director for the
nonprofit Science and Environmental Health Network, classification and data
challenges in surveillance of birth defects almost makes cancer tracking look
easy (Weinhold, 2009). Systematic assessment of developmental delays and
disabilities resulting from congenital malformations in tribal communities is
difficult. Several factors likely contribute to the underestimation of actual
prevalence in Native populations. These include the relatively small numbers
of affected individuals, which limits the ability to extract reliable estimates
from larger state or national data sets; differences in perceptions of disabilities in tribal cultures, which might lead to a lack of recognition within affected families; and the lack of infrastructure and resources for diagnosis and
service, or the willingness to access those available.
Even in states such as New Mexico where Native Americans represent
approximately 10% of the population (U.S. Census Bureau, 2012), or Arizona
with 4.6% of the population, tracking methodology for birth defects differs
substantially, as do agreements on data sharing, making it difficult to compare or integrate results. For example, differences in birth defect tracking
include whether or not congenital defects are tracked at birth only or over
a number of years often required for diagnosis; whether only live births
are included, or also stillbirths and elective terminations; whether the
frequency of occurrence and the population size are sufficient to establish
prevalence within states; and whether adjusted or raw data are available.

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These differences hamper the ability to make comparisons and to pool data
across states to establish representative Native American prevalence estimates
for most congenital anomalies.
A recent study has attempted to overcome these barriers, working with
birth defect surveillance data from 12 states with consistent methodology
over an 8-year period ending in 2008. This work documented a substantially
higher prevalence in Native Americans and Alaska Natives for 8 of 27 tracked
birth defects. The adjusted prevalence of seven of the eight birth defects
(anotia or microtia, trisomy 18, cleft lip with or without cleft palate, lower
limb deficiency, encephalocele, upper limb deficiency, and any limb
deficiency) was 50% higher or more among Native children than among
non-Hispanic White children (Canfield et al., 2014). Adjusted prevalence of
anotia or microtia was sixfold higher than in the lowest racial or ethnic group
(non-Hispanic Blacks), with the next four of the listed defects nearly double
in adjusted prevalence compared to non-Hispanic Whites. Only two conditions were found at lower prevalence in American Indians and Alaska
Natives: hypospadias in males, and pyloric stenosis. The Canfield et al.
(2014) study was the first multistate estimate for American Indians and Alaska
Natives. However, of the 12 states included in the study, only 2 have greater
than 1% Native population, and none of the six states with the highest percentage of Native populations in the 2010 Census were included. For
example, when looking at defects such as Down syndrome that had relatively similar prevalence across groups, the prevalence was based on 110
cases for Native Americans and 17,006 cases for non-Hispanic Whites. Therefore, although this is the most comprehensive assessment of rates of
birth defects to include Native Americans to date and represents 37% of all
U.S. live births from 1999 to 2007, the relatively small numbers of Native
Americans within the data set makes it difficult to know how representative
it is of the actual rates for Native Americans. Moreover, the study did not look
at environmental risk factors.
Severe disabilities with genetic components such as those discussed
previously are somewhat more frequently documented in the literature. On
the Navajo Nation, for example, the prevalence of SCID is approximately
52 per 100,000 compared with 1 per 100,000 in the general U.S. population
(Lipstein et al., 2010). Again, this severe disability is known to have a substantial genetic linkage along with other immunologic disorders found at higher
prevalence among members of the Navajo Nation, but is not geographically
homogeneous in distribution throughout the tribe (Jones et al., 1991), and
questions as to gene–environment interactions, epigenetic factors, and the
overall prevalence of specific genetic markers in the population remain.
For Navajo, current policy on human research has placed a moratorium on
genetic research, maintained through review by the Navajo Nation Human
Research Review Board, making it likely these uncertainties will remain for
some time.

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New Mexico is home to almost 220,000 Native American citizens.
Nineteen Pueblo tribes, two Apache tribes (Jicarilla and Mescalero), and
the Navajo Nation comprise 10.5% of the state’s population (New Mexico
Indian Affairs Department, http://www.iad.state.nm.us/history.html). Many
families live in rural communities, with limited access to resources, including
health care and educational programs. Families who have children with
medical or developmental needs are affected by the rural nature of communities, as they have limited availability of providers with expertise in diagnosis and intervention. As a result, many families with children requiring
early intervention are referred to larger, metropolitan areas where specialized
service providers are available, but where logistical or cultural barriers either
prevent or significantly interfere with families receiving services. The University Centers of Excellence on Developmental Disabilities (UCEDD) and
Native American Research and Training Center at the University of Arizona
have found a range of barriers to receiving care in metropolitan areas ranging
from transportation barriers to a lack of support and resources outside of
their home communities. Further, Native individuals with developmental disabilities and their families want service systems to respect their culture and
customs and provide information, training, and services that are relevant
and appropriate.
The Indian Children’s Program (ICP) was a collaborative project formed
by UCEDD programs at Utah State University, Northern Arizona University,
and the University of New Mexico. Started in 1991, the ICP provided familycentered and community-based services to Native American children with
disabilities living in the Four Corners area of Utah, New Mexico, Arizona,
and Colorado. ICP addressed critical service needs for children with disabilities in Native American communities. In addition to diagnostic services, ICP
provided case coordination, therapeutic services, training, and technical
assistance. In November 2014, after 23 years of service, the ICP was disbanded, leaving a large gap in service coordination and delivery to this
already underserved community.
Navajo Nation is meeting this gap in services through its own early intervention referral program: Growing in Beauty (GIB). GIB is a component of
the Office of Special Education and Rehabilitation Services of the Diné
Department of Education and supports and promotes opportunities for
young Navajo children and their families to receive appropriate developmental services and early intervention. GIB respects and recognizes traditional
beliefs of child development. Whereas Western developmental milestones
help predict the next phase of a child’s growth, traditional Navajo recognition
of the baby’s and child’s life steps helps guide his or her health, safety, and
personality into adulthood.
GIB implements a team-based or transdisciplinary mode, assuring that
families have access to a full team of individuals representing diverse
disciplines including a service coordinator, physical therapist, occupational

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therapist, speech therapist, and developmental specialists with expertise in
autism, regulatory disorders, sensory impairments, and other developmental
disabilities. The GIB staff serve as a ‘‘guide’’ through the initial stress and confusion of having a child diagnosed with a disability by coordinating services
and helping anticipate family priorities and concerns, recognizing strengths
and advocating for the Navajo family. This can include access to traditional
healing ceremonies for families.
In 2014, GIB served 1,102 infants and toddlers (birth to 3 years), 735 from
New Mexico. Eligibility criteria for early intervention in New Mexico are
broader and include environmental risks, accounting for the increased percentage of New Mexico children. GIB works closely with the University of
New Mexico Center for Development and Disability (CDD) in provision of services. In 2012, CDD experienced the barriers to services previously discussed
when Navajo families missed 12% of appointments in the first 6 months of the
year. CDD also found that as a result of differences in Navajo versus Western
beliefs about child development, families often did not recognize the need for
or importance of a developmental evaluation. To overcome the physical and
cultural barriers to services, CDD collaborated with ICP to structure more
effective service delivery, and now travels to Navajo Nation to complete evaluations in the community. CDD works closely with Native American professionals in organizations such as ICP and GIB as cultural liaisons to provide
guidance and feedback on culturally sensitive practices and support for communication in their Native language. As a result, virtually all families currently
are attending scheduled appointments and families are receiving specialized
evaluations and intervention services when appropriate.
Even when families are able to access these services, clinicians have
limited information from the scientific research literature to guide culturally
sensitive practices surrounding developmental disabilities in Native
Americans. To our knowledge, normative data for developmental delays in
Native children are either very limited or unavailable for either clinicianadministered developmental assessments or parent questionnaires. Clinicians
often use assessments (Mullen, 1995; Bayley, 2006; Bricker, Squires,
Kaminski, & Mounts, 2006; Squires, Bricker, & Potter, 1996), such as the
Mullen Scales of Early Learning, the Bayley Scales of Infant and Toddler
Development–Third Edition, or the Ages and Stages Questionnaire as
measures of a child’s abilities with the caveat that the scores are an estimate
of the child’s functioning because normative data are not available for Native
American populations. The risk in this approach is that a child could be
nondifferentially misclassified as either having or not having developmental
concerns due to the lack of culturally appropriate normative data. Given the
lack of available alternatives, these assessment tools continue to be used.
Recognizing the problem presented by the lack of standards appropriately normed for the culture, the NBCS is working with the developers of
the Ages and Stages Questionnaire, with permission from Navajo Nation

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J. Lewis et al.

Human Research Review Board, to develop Navajo-specific norms based on
the anticipated 1,500 children in the birth cohort study. As this instrument
forms the initial screening tool for GIB, culturally appropriate norms will provide more accurate identification of at-risk children. The administration of
the screening instrument to all participants in the NBCS will also allow a
broader characterization of the percentage of children at risk, and the types
of delays most prevalent to further inform the activities of both GIB and
CDD, who are partners in the study.

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Are Community Concerns About Exposures to Environmental Metal
Contaminants and the Health of Their Children and Future
Generations Well Founded?
Although the prenatal period is recognized as a very vulnerable time, and birth
defects are known to contribute significantly to lifelong mental and physical
disabilities, limited research has investigated the relationships between in
utero exposures to contaminants and birth outcomes. Even less research
has examined racial and ethnic differences in exposure–birth outcome relationships and the effects of exposures to mixtures of contaminants. Existing
work has shown in utero exposures to arsenic, lead, and mercury, in addition
to other environmental contaminants, can be directly linked to specific birth
defects (Weinhold, 2009). Much current scientific evidence demonstrates that
environmental exposure beginning in utero can affect infant, childhood, and
adult health conditions (Burton, Barker, Moffett, & Thornburg, 2011; La Merrill
& Birnbaum, 2011; La Merrill et al., 2013). Children, from birth through age 12,
are particularly susceptible to the toxic effects of environmental exposure (Au,
2002). As mentioned in the beginning of this article, Native American communities have disproportionately high exposure potential to waste metals
from abandoned hard-rock mines in the Western United States. Mining
regions specifically have vast areas of disturbed soils contaminated with a variety of environmental metals including arsenic, lead, nickel, uranium,
vanadium, copper, and iron, as well as many others depending on the location
and type of minerals being mined (Ahern et al., 2011; Wu, Zhang, Pei, Chen, &
Zheng, 2014). More than 161,000 abandoned hard-rock mines are located in
12 Western states (GAO, 2014)—the same states that have the highest percentage of Native American population in the country (U.S. Census Bureau,
2012)—providing ample opportunity for maternal and child exposures to
environmental metal mixtures. However, little scientific evidence is available
to help us understand the degree and types of risks associated with metals
from mining operations and pregnancy outcomes among Native populations.
As mentioned, uranium mine waste presents a risk at more than 4,000 of the
abandoned mine sites, and is the major waste source in the Navajo Nation
affecting the participants in the NBCS, so we start with that body of evidence.

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To date, most of what is known about uranium-induced developmental
toxicity has come from experimental work performed in animal models.
Effects including decreased fertility, embryo and fetal toxicity including
teratogenicity, and reduced growth rate of offspring have been observed following uranium exposure at different gestation periods (Domingo, 2001).
These reproductive effects are based primarily on the chemical nature and
properties of uranium rather than its radioactivity. Despite the large numbers
of Native women who live in regions with heavy uranium mining history,
only one study has evaluated the risk of adverse outcomes of pregnancy in
relation to uranium exposure from mining and milling operations. This study,
which included more than 13,300 Navajo children born at the Public Health
Service=Indian Health Service Hospital in Shiprock, New Mexico, was the
first to describe a link between living near uranium tailings or mine waste
dumps and adverse birth outcomes in a Native population (Shields et al.,
1992), although a possible confound of exposures at an electronics plant
limited the interpretation of those data. More than two decades later, initial
biomonitoring results from the NBCS indicate that a higher percentage of
mothers in our study show evidence of continuing exposure to uranium as
measured in urinary uranium, with 81.2% of mothers at enrollment during
pregnancy exceeding the 50th percentile, and 16.1% exceeding the 95th
percentile observed for the U.S. population as a whole as reported in the
National Health and Nutrition Examination Survey (NHANES; Centers for
Disease Control and Prevention [CDC], 2013).
Beyond the scant population-based evidence already described, there
is little else to inform the risk association between uranium and other metals
from mining operations and pregnancy outcomes in Native populations.
However, information from other populations does support concerns about
the risks for birth defects and child development. For example, living in
close proximity to surface coal mines has been associated with birth defects
involving the circulatory and respiratory system, the central nervous system,
and musculoskeletal, gastrointestinal, and urogenital defects (Ahern et al.,
2011). In addition to organic toxicants, coal also contains mixtures of
metals. Elevated arsenic and lead in soils near the homes of mothers during
pregnancy in areas of coal mining and down gradient of coal mining have
been associated with neural tube defects (Wu et al., 2014). Evidence linking
birth defects to metals exposure has also emerged from Iraq, where mercury, lead, and depleted uranium (metal components of bullets and other
ammunition) were six times higher in hair samples from children with birth
defects (heart defects, neural tube defects, and cleft lip or palate) and five
times higher in their parents compared to normal children and parents. Lead
levels in teeth were also higher in parents and their children for children
with anencephaly, hydrocephalus, limb deformities, omphalocele, or short
extremities compared to unaffected children and parents (Al-Sabbak et al.,
2012).

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Beyond birth defects, metals exposure during pregnancy and child
development are also known to be associated with neurodevelopmental
delays. Lead has been the most widely studied neurotoxic metal with respect
to neurodevelopmental disorders, including decreased cognitive abilities and
IQ, attention disorders, hyperactivity, and impulsive behavior (Braun et al.,
2012; Canfield et al., 2003; Lanphear et al., 2005; Szkup-Jabłońska et al.,
2012). Gestational and childhood exposure to arsenic has also been shown
to negatively impact neurological development of children (Canfield et al.,
2003; Lanphear et al., 2005; Liu, McDermott, Lawson, & Aelion, 2010; Rosado
et al., 2007; Wasserman et al., 2004). The magnitudes of these associations
are similar to those observed with increases in blood lead, an established risk
factor for diminished IQ. Even in areas where residential soil concentrations
of arsenic and lead were below standards set by the U.S. EPA, the concentrations of these metals in the soil around mothers’ homes during pregnancy
affected the severity of intellectual disability in children (McDermott et al.,
2014). Little is understood about how combinations of metals interact to
influence risk. For example, evidence from McDermott et al. (2014) indicates
that the risk of severe intellectual disability differs for differing combination
of arsenic and lead.
Adequate nutrient intake during pregnancy, lactation, and early childhood is essential for healthy birth outcomes and child development. For
example, iodine plays a crucial role in fetal organogenesis and in particular,
brain development. The severity of the outcome depends on the level of prenatal iodine deficiency and ranges from increased neonatal morbidity and
mortality, severe mental dysfunction, hyperactivity, and attention disorders
to a substantial decrease in IQ (Puig-Domingo & Vila, 2013). Iodine
deficiency in early life, ages 5 and younger, has been associated with a
reduction in IQ (Bougma, Aboud, Harding, & Marquis, 2013). Birth defects
such as neural tube defects including spina bifida (somewhat elevated in
Native American populations in the Canfield et al. [2014] study) are strongly
associated with folate deficiency (Kancherla, Oakley, & Brent, 2014). Zinc
deficiency has been associated with a range of teratogenic, growth retardation, immunologic, and behavioral effects (Uriu-Adams & Keen, 2010).
The link between iodine deficiency and development is of particular concern
for noncoastal Native communities, as the primary dietary sources of iodine
include seafood and dairy products, two components not traditionally a part
of those diets. Dietary and biochemical analysis of pregnant and lactating
Navajo mothers conducted in 1981 showed marginal deficiencies in zinc,
vitamin A, folacin, and iron among these women (Butte, Calloway, & Van
Duzen, 1981). The NBCS will be the first study looking at dietary micronutrient sufficiency since then, and current biomonitoring results show more than
40% of mothers are deficient in iodine at enrollment, and more than 78% are
deficient in serum zinc.

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Is There Potential for Interaction Between Environmental
Contaminants and Genetic Factors?
As discussed previously, although genetic factors are frequently linked to
birth defects, much existing research fails to look at overall prevalence of
these factors in the population, the role of environmental exposures in triggering expression of adverse outcomes, or how these interactions contribute
to racial and ethnic differences in birth defects. Data indicating geographic
differences in rates of specific defects in the same populations suggest
gene–environment interactions might play a significant role in birth defects,
but other variables such as cultural, sociodemographic, or reporting and surveillance differences could likewise be contributing to those differences
(Weinhold, 2009). Without specific studies on gene–environment interactions, the contributions are difficult to define.
Interactions between genetics and environmental exposures have been
hypothesized to play a role in developmental disorders such as autism
(London, 2000), with autism spectrum disorder considered a likely candidate
for gene–environment interaction. However, the specific nature of the gene–
environment interactions in developmental disorders likely arises from
complex combinations of genetic and environmental factors (Kelada, Eaton,
Wang, Rothman, & Khoury, 2003). Currently, the medical and scientific communities have limited ability to detect the level of risks from gene–environment interactions within specific populations, such as Native Americans,
although the understanding of etiologic mechanisms continues to evolve.
Expanding the scientific knowledge base of environmental exposure on
human genetics, and subsequent fetal and childhood health, is an important
first step toward developing innovative care and resources for Native women
and their families. Because many diseases result, at least in part, from
complex gene–environment interactions, subtle differences in genetic factors
represent different levels of risk to the same environmental exposure
(Khoury, Davis, Gwinn, Lindegren, & Yoon, 2005). Therefore, environmental
exposures have the potential for far-reaching effects on the developing fetus,
beginning at the cellular level of fetal development.
Gene–environment interaction is the interface between genetic and
environmental factors (Dempfle et al., 2008), and is often thought of in terms
of the same environmental exposures, resulting in differential responses
through interactions with different genetic compositions. Epigenetics is a
term used to describe how genes might interact with their environment to
produce observable changes in an individual without changes to the DNA
sequence (Waddington, 2012). For example, chemical reactions such as the
attachment of methyl groups to DNA can occur as a result of exposure to
environmental contaminants, altering how genes are transcribed and in turn
expressed, activating or deactivating parts of the genome. These altered

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J. Lewis et al.

transcription states can be passed on from one generation to the next. Therefore, toxicant exposures might not only have effects on the fetus, infant, and
child by epigenetic mechanisms, but epigenetic changes could affect future
generations as well (Wallace, 2010), producing heritable effects without
changing the genetic makeup.
Given the genetic mutations that have been associated with several
developmental disabilities that occur with higher prevalence in the Navajo
and other Athapaskan tribes, our lack of understanding of the overall prevalence of these mutations in Native populations, and the high potential for
exposures to environmental metals, improving our understanding of gene–
environment interactions might be a critical step in understanding the effects
of toxicant exposures in Native populations. A genetic susceptibility to a
particular developmental outcome that is manifested as a result of environmental exposures, or epigenetic changes resulting from exposures that contribute to that manifestation, would lead to disparities in exposure outcomes
that would not be predicted by studies in populations lacking such susceptibility, and not observed in Native populations lacking exposure.

HOW CAN WE FURTHER OUR UNDERSTANDING OF
RELATIONSHIPS BETWEEN EXPOSURE AND DISEASE TO
ANSWER THE QUESTIONS IN OUR NATIVE COMMUNITIES?
The Navajo Birth Cohort Study
The Pasternak series, originally published as a four-part series in the Los
Angeles Times in 2006, called attention to the problem of developmental
disabilities, such as Navajo neuropathy, and highlighted the communities’
concerns about the impacts of the more than 500 abandoned mines
(Pasternak, 2006a, 2006b, 2006c, 2006d). As mentioned in the introduction
to this article, in 2007, Representative Henry Waxman of California called a
hearing on the Navajo abandoned uranium mine situation that led to a 5-year
plan to scope and begin addressing the concerns. To better understand the
impact of the mine waste on reproductive outcomes and child development,
the NBCS was initiated in 2010 to examine any relationships among uranium
exposure, reproductive outcomes, and child development. The team anticipates that the results of this ambitious effort will finally provide answers to
long-standing concerns, providing not only to Navajo but to other tribal,
rural, and international communities a more comprehensive understanding
of whether exposures to metal mixtures resulting from abandoned mines
can interact with other risk factors to increase disabilities in children in these
exposed communities. Enrollment and data collection are in progress. Preliminary findings are discussed here as they pertain to exposure risk factors
of primary concern in this article. Developmental assessments and medical

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record abstractions are not yet complete enough to determine the relationships between risk factors and outcomes.
The study is funded through a cooperative agreement between the CDC,
the Agency for Toxic Substances Disease Registry (ATSDR) and the UNM Community Environmental Health Program (CEHP) with Dr. Lewis as the principal
investigator. Additional partners include the nonprofit Southwest Research
and Information Center, the Navajo Area Indian Health Service (NAIHS), and
the Navajo Nation Division of Health (NNDOH). The project works through
integrated teams at all phases, with Southwest Research and Information
Center and NNDOH Navajo staff having the primary responsibility for field
work, including participant enrollment, outreach, and developmental and
environmental home assessments, as well as collection and interpretation of
existing environmental data. NAIHS staff participate in recruitment and
abstract medical records for all participants as well as collection and processing
of blood and urine specimens. CDC=ATSDR provides biomonitoring analysis
of blood and urine specimens to confirm exposures, and overall project management. CEHP provides training of all field staff; protocol development and
implementation; outreach media development; data management, analysis,
and interpretation; and quality assurance. It also conducts mechanistic studies
to understand observed relationships between exposures and outcomes.
The study is enrolling pregnant women, interested fathers, and their
babies from six NAIHS service units on Navajo Nation. Home environmental
assessments, surveys, review of existing data sources, and biomonitoring of
blood and urine in mothers, fathers, and babies at multiple times will be used
to determine exposures to uranium as well as other metals associated with
mine wastes or known to be micronutrients. Medical records of participants
will be reviewed, and surveys administered at enrollment and postnatally to
identify potential risk factors for reproduction and development. The Ages
and Stages Questionnaire Inventory is administered at 2, 6, 9, and 12 months
to assess development, with any children with recognized delays referred to
GIB for more in-depth evaluation and referral to services. Nutritional data are
being assessed by food frequency surveys. Laboratory studies at UNM will
follow up key endpoints to investigate mechanisms of toxicity. DNA damage
and repair, as well as immune system function and autoimmune disease, will
be examined in participants and assessed with respect to patterns and
concentrations of metals exposures, as well as other known environmental
risk factors, sociodemographic risk factors, and cultural factors to identify
contributors to risk and protective factors.
Currently 400 of an anticipated 1,500 families are enrolled in the NBCS.
Family units include mothers and children for all, with interested fathers
included for approximately half of participating families. Medical record
abstraction has begun, but is incomplete and quality assurance is in progress
on the initial records. Likewise, the initial developmental assessments are
also in the process of quality assurance, with the initial data set under review

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J. Lewis et al.

to begin the process of norm development by the developers. Although it is
too early to draw conclusions from the data for either rates of disabilities,
birth outcomes, or effects of exposures, several findings are noteworthy from
the ongoing biomonitoring and home environmental assessments.
Metals are measured in blood and urine of mom, dad (when enrolled),
and baby at multiple time points. As mentioned, uranium concentrations in
the urine of mothers at enrollment show approximately 16.1% of our population exceed the 95th percentile observed for the U.S. population as a whole
(NHANES, CDC, 2013). Similar results have been observed in fathers, where
21.6% currently exceed the NHANES 95th percentile. Preliminary results also
show that babies are being born with detectable uranium in urine. Limited
results with completed analyses to date show 30.1% of the 73 babies tested
at birth exceed the adult 50th percentile in NHANES. By 2 to 6 months of age,
75% of 16 children tested to date exceeded the adult 50th percentile, with
18.8% exceeding the 95th percentile. Numbers of analyses are still small,
but the trend is disturbing and will be closely monitored as results continue
to come in. No data sources are available to use as a reference for these
results in children. Although timing of sample collection does not allow for
calculation of placental transfer factors, these early data do indicate that
babies are being born with uranium, and subsequent measurements through
the first year of life also indicate that uranium concentrations in urine can
continue to increase throughout the first year of life in some children.
A second unexpected finding has been the observation of iodine
deficiency referenced previously. For mothers, 40.2% were iodine deficient
at enrollment and 52.7% at delivery, relative to the World Health Organization sufficiency level of 99.0 mg=L (ug=L). As discussed earlier, iodine has
been found to be a key nutrient for fetal organogenesis and for brain development. Primary sources of iodine are from seafood and dairy products in
the diet. As these are not common dietary components of Native communities in the interior of the country, this raises concerns for sufficiency in other
Native populations as well, and suggests a potential intervention that could
yield dramatic improvements in developmental outcomes in Native children.
Also, the potential for this deficiency to interact with metal exposures, potentially exacerbating effects, is a concern that will be evaluated as birth and
developmental data become available.
Despite the observed zinc deficiency in NBCS mothers, at birth, only
12.5% of babies have been deficient, and only 21.6% of fathers. This observation of zinc deficiency in pregnant women is common in many studies
internationally and suggests the serum zinc levels are lowered due to transfer
to the baby leading to reduction of circulating zinc. The sufficiency of fathers
and babies suggests that the deficiency is not a result of inadequate dietary
zinc, nor has it been related to reported use of prenatal vitamin supplements.
This question is an important area for future study that we will be following
up in laboratory studies, as zinc has also been reported to reverse the toxic

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effects of arsenic in inhibiting repair of DNA damage (Ding et al., 2009). Preliminary studies in our lab indicate this reversal of toxicity might extend to
uranium-induced inhibition of repair of DNA damage as well.
Home environmental assessments have detected uranium in indoor dust
samples in 65% of homes tested, and 62% have had at least one metal
exceeding screening guidelines based on interagency working group guidelines developed for the World Trade Center (U.S. EPA, 2013a, 2013b),
adapted for continuous versus one-time source deposition. Most frequently
observed were lead, arsenic, iron, manganese, and antimony. No screening
value for uranium is being used, as all observed concentrations are of
concern as the focus of this study.
One of the goals of the NBCS is to contribute normative data for the
Ages and Stages Questionnaire–Inventory version (ASQ–I) to better understand development of Native American children. The ASQ–I is a developmental screening tool currently used by a variety of professionals to track
a child’s development in various domains at a specific age or over a period
of time. In collaboration with the developers of the ASQ–I, data collected
from this instrument will be used to establish a set of normative data for this
developmental measure specific to our Navajo population. To our knowledge, this will be the first time that longitudinal data have been collected
from a cohort of Navajo children to track development within the first year
of life. Because the ASQ is so widely used in both clinical and research settings, including by GIB, these data will be valuable for understanding potential developmental differences in this population and guiding referral and
intervention practices in a manner that better reflects cultural differences.

CONCLUSIONS
Existing data demonstrate (a) a strong potential for exposures to metal
mixtures associated with mining wastes in Native American populations in
the Western United States, (b) a linkage of exposures to developmental
disabilities and congenital malformation in population and laboratory studies, (c) higher rates of several congenital anomalies in Native American
populations, and (d) a lack of comprehensive data on rates and types of
developmental disabilities in Native populations.
Although data discussed here indicate a strong reason for concerns
about the impacts of environmental exposures in Native American and
Alaska Native communities, the NBCS will be the first comprehensive examination of these questions. The results should have a significant impact on
our understanding of the complexities and unique aspects of not only
environmental exposures, but their interaction with other socioeconomic,
demographic, and cultural variables in determining reproductive and developmental outcomes. Although tribes make up a small proportion of the U.S.

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J. Lewis et al.

FIGURE 4 Helen Nez and her daughter Seraphina.

population as a whole, they are neglected in the body of literature we use to
inform our policies and decisions. Their connection to the land, the extent of
environmental contamination, and the occurrence of many socioeconomic
factors associated with health disparities, as well as their unique genetics,
make it critical to understand the causes of developmental delays, adverse
birth outcomes, and ultimately disabilities in these populations where determinants might interact in unique ways, and where services remain limited.
In the words of Helen Nez (shown in Figure 4):
We are veterans of war. We gave a lot to help Washington, DC. Our
children had to become warriors. This land that we live on and whatever
they mined from it is a Navajo legacy. Because we helped in this way,
people became sick and many now suffer from long-term exposure.
We did not know that the uranium was going to hurt other people,
too. Because we did not know about the dangers we were played with
like toys. We were moved around in a game of war. There is beauty.
How we value our mother the land. She is filled with sacred elements.
Her elements that protect our people protected the United States: this history has not been told right. We have been wounded with the land. Our
children, and our grandchildren: we do not know what will happen in
the future to our children.

ACKNOWLEDGEMENTS
Our research on Navajo Nation is regularly reviewed and approved by the
Navajo Nation Human Research Review Board. The authors acknowledge

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contributions of Chris Shuey, MPH, and Research Field Staff from Southwest
Research and Information Center; Mae-Gilene Begay and Anna Rondon and
the Community Health and Environment Research Specialists from the
Navajo Department of Health; Doug Peter, MD, and the Cohort Clinical
Liaisons from Navajo Area Indian Health Service; Angela Ragin-Wilson,
PhD, Candis Hunter, MPH, and Elizabeth Irvin-Barnwell, PhD, from the
Agency for Toxic Substances Disease Registry for their work on the NBCS.
We would also like to acknowledge the support and participation of the
hundreds of Navajo community members, agency staff, and tribal leadership
participating in this effort, without whose help these questions would remain
unanswered.

FUNDING
The Navajo Birth Cohort Study (NBCS) is funded through the Centers for
Disease Control and Prevention cooperative agreement U01 TS000135.
Contributions by Drs. Lewis and Gonzales also supported by grant
3P20MD004811-03S1 from the National Institutes of Health.

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