Environmental and occupational health on the Navajo Nation: a scoping review

Abstract

A scoping review was performed to answer: what environmental health concerns have been associated with adverse health outcomes in the Navajo Nation? The review focused on occupational and ambient environmental exposures associated with human industrial activities. The search strategy was implemented in PubMed, and two investigators screened the retrieved literature. Thirteen studies were included for review. Data were extracted using the matrix method. Six studies described associations between work in uranium mining and cancer. Six studies focused on environmental exposures to uranium mine waste and other metals, with outcomes that included biological markers, kidney disease, diabetes and hypertension, and adverse birth outcomes. One study explored occupational exposure to Sin Nombre Virus and infection. Most research has focused on the health effects of uranium, where occupational exposures occurred among miners and environmental exposures are a legacy of uranium mining and milling. Gaps exist with respect to health outcomes associated with current occupations and the psychosocial impact of environmental hazards. Other environmental exposures and hazards are known to exist on the Navajo Nation, which may warrant epidemiologic research.

Introduction

The Navajo Nation has the second largest tribal membership in the United States and is geographically dispersed, covering lands in Utah, Arizona, Colorado, and New Mexico. The Navajo Nation continues to experience longstanding structural inequalities. For example, more than 75% of the Diné have food insecurity and 40% of households in the Navajo Nation do not have running water [1, 2]. Health disparities continue to exist for Native Americans, including the Navajo Nation. Native Americans have consistently been shown to have high rates of diabetes, cardiovascular disease, metabolic syndrome, and obesity compared to other populations [3].

One example of environmental health disparities that has adversely affected the Navajo Nation relates to the history of extractive activities, especially mining, and general environmental exploitation on or near the Navajo Nation. Such activities are well documented, but the extent of the health repercussions are still not fully understood. Most of the uranium mining on the Navajo Nation occurred between 1948 and 1967, during which time it was a crucial part of the Navajo economy and employed many tribal members. By the 1930s, it was understood that uranium miners experienced high rates of lung cancer, but the causal agent was still being debated. The US Public Health Service, however, did not effectively share knowledge of these hazards with the Navajo Nation. In 1990, the Radiation Exposure Compensation Act was passed, through which the US Government accepted responsibility and compensated uranium miners who developed lung cancer and other lung diseases. Today, there are still over 1,000 abandoned mines and associated mine tailings that continue to be an exposure hazard for the Diné [4].

Full understanding of such environmental health impacts on the Navajo Nation remains important to document in order to draw public interest, extramural funding for research, and possible interventions or reparations for the community. A thorough literature search gives a robust understanding the state of the science regarding environmental health on the Navajo Nation, and identifies gaps in the current knowledge that will inform future work.

Methods

Consistent with PRISMA guidelines for scoping literature review performance and reporting, we used a multi-step approach of forming the question, defining inclusion/exclusion criteria and search terms, selecting studies, and extracting data [5, 6]. Covidence systematic review software (Veritas Health Innovation, Melbourne, Australia) was used to manage the review process.

The primary research question was as follows: what environmental health concerns have been associated with adverse health outcomes in the Navajo Nation? The focus was on occupational and ambient exposures associated with human industrial activities. The database PubMed was selected for identifying articles owing to its coverage of both biomedical topics as well as public health and occupational and environmental health journals. The following search string was used to search PubMed: (“Navajo” OR “Diné”) AND (“environmental quality” OR “water pollution” OR “air pollution” OR “uranium” OR “mining” OR “oil” OR “gas”) OR (“environmental health” OR “health outcome” OR “epidemiology”) NOT (“indoor air” OR “cook stoves”). The search was limited to articles written in English. Identified literature was exported to Covidence.

Titles and abstracts were independently reviewed by two investigators (SC and RMJ) using a priori inclusion and exclusion criteria. The article inclusion criteria were as follows: 1) the study data were about the Diné people or the Navajo Nation, 2) the study involved original data collection and analysis, 3) the study measured a health outcome, including biological markers of effect and clinical outcomes, and 4) the study considered an exposure to an occupational or environmental health hazard. Owing to our focus on the impacts of human industrial activities (e.g. mining), hazards driven by climate change and indoor air pollution from cookstoves were excluded. The article exclusion criteria were as follows: 1) the study data were exclusively about Native Americans not affiliated with the Navajo Nation or non-native populations on the Navajo Nation, 2) the study was about climate or climate change-related environmental issues, such as drought, 3) the study was about indoor cook stoves and other indoor air quality issues, 4) the study was a review or commentary, and 5) the study did not involve a health outcome. The full texts obtained for literature were obtained after title and abstract review. Full texts were screened by the same two investigators using the inclusion and exclusion criteria. The reference lists of the articles included after full text review, as well as excluded review articles, were searched for additional literature and screened for inclusion.

Consistent with the approach of a scoping review, included literature was not formally assessed for quality. The matrix method was used to abstract information from literature into spreadsheets, including the following variables: agent(s), study location, date, sample demographics, exposure route, health outcomes, study design, and key findings.

Results

The literature search identified 140 articles (Figure 1). Title and abstract screening eliminated 100 articles. The remaining 40 articles had the full text reviewed and 28 were excluded, leaving 12 articles. The references of these articles and excluded review articles were reviewed and screened, with one additional article identified for inclusion. A total of 13 articles were analyzed. All of the included articles were published in 1980 or later.

Figure 1:

PRIMSA flow diagram.

Seven studies were about lung cancer in Navajo uranium miners (Table 1). All studies with quantitative exposure assessment measured exposure as working level months (WLM) exposure to radon, where WLM is the cumulative underground exposure defined as the product of the working level (1 WL=1.3 × 10⁵ MeV of potential alpha energy from radon daughters per liter of air) and working months (170 h per month) [7]. Most studies, however, had incomplete exposure quantification and none performed dose-response analyses using WLM. All of the studies found that uranium mining was associated with lung cancer, regardless of smoking history, though only Gilliland et al. [8] presented a risk statistic (RR=28.6 (95% CI 13.2–61.7)).

Table 1:

Epidemiological studies of Navajo uranium miners exposed to uranium.

Reference	Study design	Sample	Exposure assessmenta	Sample size	Summary of findings
Gottlieb et al. [7]	Retrospective case series	Male Navajo patients with lung cancer diagnosis admitted to Shiprock Indian Health Service Hospital or Navajo Family Health Center, Feb 1965–May 1979	Range of 58.8–2,125 (mean 1,140) lifetime WLM	17	Lung cancers observed similar to those observed among white U miners and most subjects were non-smokers, indicating radiation exposure, not smoking, is the primary cause of lung cancer in U miners. Ninty four percent of cases were miners.
Butler et al. [9]	Retrospective case series	Navajo men living in UT, AZ, NM and diagnosed with lung cancer 1969–1982; New Mexico Tumor Registry	Range of 103–2,698 (mean 1,334) lifetime WLM for 13 miners.	26	Distribution of lung-cancer types was similar to that of the general population. Eighty one percent of cases were miners.
Gilliland et al. [8]	Population-based retrospective case control	Navajo men living in NM and AZ diagnosed with lung and other cancers 1969–1993; New Mexico Tumor Registry	WLM available for 73% of miners but values not reported	94 cases, 282 controls	RR=28.6 (95% CI 13.2–61.7) for lung cancer with documented history of underground U mining compared to no history of mining.
Mulloy et al. [10]	Case study	A non-smoking male Navajo miner who lived in the Navajo Nation in AZ	506 WLM	1	Diagnosis of squamous cell carcinoma. This case of lung cancer is related to mining and could be compensated under RECA.
Roscoe et al. [11]	Retrospective cohort	Non-white male miners (99% Navajo) in the Colorado Plateau study. Vital status ascertained 1960–1990; worked ≥1 month in underground U mine before 1964 and participated in U.S. Public Health screening 1950–1960.	Range of 30–3,896 (mean 1,517) WLM for miners	757 (34 miners)	Standardized mortality ratio (SMR)=3.3 (95% CI 2.3, 4.6) for lung cancer, SMR=2.6 (95% CI 1.4, 4.6) for tuberculosis, SMR=2.6 (95% CI 1.6, 4.0) for pneumoconiosis and other respiratory diseases relative to non-white population of NM and AZ
Samet et al. [12]	Population-based retrospective case control	Navajo men living in NM and AZ diagnosed with lung and other cancers 1969–1981; New Mexico Tumor Registry	Range of 30–2,698 (median 1,207) for 14 cases	32 cases, 64 controls	Uranium mining was associated with lung cancer (p<0.001), with 72% of cases attributed to mining. Miners developed lung cancer at a younger age than non-miners

^aWLM, working level months.

Two studies explored the effects of environmental and occupational exposures on pregnant women and birth outcomes (Table 2). Dashner-Titus et al. [13] found that urinary arsenic, but not urinary uranium, was associated with increased markers of oxidative stress. Median urinary uranium levels among Navajo women were more than twice that of levels in the general US population reported in the National Health and Nutrition Examination Survey (NHANES), but still below concentrations found in experimental studies to elicit a measurable oxidative stress response. Shields et al. [14] assessed exposures of parents and grandparents of children born in the Shiprock Indian Health Service Hospital with a variety of adverse birth outcomes, and though some statistically significant associations were observed (Table 2), the lack of dose-response relationship and biological plausibility for the exposure-outcome relationships for some adverse birth outcomes limits confidence that radiation exposures were associated with the observed adverse genetic outcomes.

Table 2:

Pregnancy and birth outcomes in Navajos from familial exposure to environmental contaminants.

Reference	Study design	Sample	Sample size	Exposure assessment	Health outcome	Summary of findings
Dashner-Titus et al. [13]	Prospective cohort	Pregnant women living on the Navajo Nation for ≥5 years, aged 14–45 years, recruited since 2013; Navajo Birth Cohort Study	132	Urinary total As, AsIII, DMA, U; Serum Zn	Biomarkers of oxidative stress: 8-iso-PGF2alpha, PGF2alpha, prostaglandin ratio	Median urinary U levels were more than double that in the general US population, but were not significantly associated with oxidative stress biomarkers. Urinary total As was associated with 8-iso-PGF2alpha, which was not mediated by Zn.
Shields et al. [14]	Population-based retrospective case control	Navajo births at the Shiprock Indian Health Service Hospital 1964–1981	266 matched pairs	Parental and grandparental time of work in U mine or mill; residence within 0.805 km of U mine, mine dumps or mill tailings; living in a home of U mine rock; work by parents in electronics plant (potential solvent, 85Kr and 60Co exposures)	Singleton births with congenital abnormalities, still births, development disorders and infant deaths from causes other than injuries. Controls were chronologically nearest normal singleton birth matched by sex, mother’s age and gravidity	For all outcomes, OR=1.83 (95% CI 1.00, 3.46) for mothers living near tailings or mine dumps; and OR=2.56 (95% CI 1.14, 6.28) and OR=2.05 (95% CI 1.16, 3.76) for fathers and mothers prior history of work at electronics plant; no effect of reported duration of either exposure

Studies of other health effects included biomarkers of cardiovascular disease and autoimmunity associated with exposure to uranium, arsenic and other metals, and infection with Sin Nombre Virus (SNV) (Table 3). In a follow-up of the Diné Network for Environmental Health Project, household proximity to abandoned uranium mines was associated with the presence of antibodies to denatured DNA and chromatin [15], and with serum inflammatory potential [16]. SNV, which is carried by rodents, causes hantavirus disease, but Zeitz et al. [17] did not detect serologic signs of infection among workers in areas affected by hantavirus outbreaks, including among workers at the Navajo Agriculture Product Industry.

Table 3:

Epidemiological studies of other outcomes in Navajos with environmental exposures.

Reference	Study design	Sample	Sample size	Exposure assessment	Health outcome	Summary of findings
Hund et al. [18]	Cross-sectional	Adult Navajo in NM; participants from phase I of the Diné Network for Environmental Health Project; Jun 2010 to May 2011	1,304	Composite binary variable of exposures during “active” mining period (1946–1986) and “legacy” exposures through contact with abandoned mines, mills and waste sties	Self-reported kidney disease, diabetes or hypertension	Active exposure associated with kidney disease, while active and legacy exposure associated with hypertension. Exposure increases risk for multiple chronic diseases.
Erdei et al. [15]			263	Proximity to uranium mining and milling waste sites; self-reported mining exposure and contact with uranium waste; drinking water sources and water quality; urinary arsenic, nickel, uranium and vanadium	Autoantibodies against: histones, denatured DNA, chromatin, and native DNA	Long-term exposure to abandoned U mines was associated with presence of antibodies against denatured DNA and chromatin, but these antibodies were negatively associated with As exposure. U waste may enhance antibodies while arsenic is immunosuppressive
Harmon et al. [19]			145		Cardiovascular disease biomarkers: total serum cholesterol, HDL, LDL, triglycerides, CRP, IL-6, HbA1c; inflammatory potential assay	Household proximity to abandoned U mines was associated with overall serum inflammatory potential, not drinking water.
Harmon et al. [16]			252		Cardiovascular disease biomarkers: oxidized LDL and CRP	As and U intake were positively and negatively associated with oxidized LDL, respectively.
Zeitz et al. [17]	Cross-sectional	Workers at the Grand Canyon National Park (AZ), Navajo Agriculture Product Industry (Navajo Nation), and utility workers (NM)	494	Jobs with risk of exposure to hantavirus-infected rodents in region of 1993 Sin Nombre Virus outbreak	Sin Nombre Virus-specific IgG	All participants were seronegative for Sin Nombre Virus.

Discussion

Uranium mining in the Navajo Nation occurred from 1944 to 1986, and many of the Diné people worked in mines off the Navajo Nation. This review identified seven studies of lung cancer among Diné uranium miners published since 1980 (Table 1), but there is additional literature from earlier describing lung cancer among non-Diné uranium miners who worked on the Colorado Plateau [20]. Though radon exposures among miners in Europe were well-known to cause lung cancer by 1944, these risks were not communicated to Diné miners, nor were existing, effective workplace protections put into place in uranium mines until the 1960s when lung cancers began to appear in Navajo uranium miners [4]. The involvement of federal agencies, including the US Public Health Service, in this “experiment of opportunity” is unconscionable [21]. Given the cessation of active uranium mining in the Navajo Nation, lung cancer among miners is not a current occupational health risk.

The community, however, continues to be impacted by this legacy of injustice, ill health, and loss of life [22]. Uranium mine tailings and abandoned uranium mines on the Navajo Nation continue to pose a risk to environmental health and traditional ways of living, including through metals contamination of water sources [23] and the food chain [24]. Risk mapping efforts have identified that 20.2% of the Navajo Nation has high potential for contamination from abandoned uranium mines [25]. The US Environmental Protection Agency and other federal agencies continue to work with the Navajo Nation to clean up mine and mill sites, remove contaminated structures, and improve drinking water infrastructure [26].

Despite the long recognition of high burdens of infant mortality among the Diné [27] and identification of an association between maternal residence near uranium mine tailings or mine dumps and adverse birth outcomes [14], there has been limited research about environmental determinants of birth outcomes among the Diné. This may be changed by results of the Navajo Birth Cohort Study, a prospective cohort study of pregnancy and neonatal outcomes [22]. Pregnant women in this cohort who had lived on the Navajo Nation for at least five years had values of urinary cadmium, lead, manganese and uranium in excess of respective NHANES values for the US population, as well as exposure to arsenic, yet oxidative stress biomarkers were not elevated [13, 23]. Additional findings from the Navajo Birth Cohort Study are expected in the coming years.

The design of the search strategy did not identify literature about the impact of human industrial activities on mental health, as literature about mental health, including anxiety and depression, has not been assessed specifically in the context of environmental “exposures” to date. These relationships, however, are particularly important given the importance of traditional ecological knowledge – i.e., traditional knowledge passed through generations about the relationship between people and the natural environment – to the Diné [28]. The linkage between people and the natural environment can be a mechanism of resiliency, but also a pathway for psychosocial stress, which impacts mental and physical health. Psychosocial stress from uranium mining activities persists on the Navajo Nation, including fear of environmental contamination, anticipation of ill health, traumatic bereavement, disruption of lifestyle, feelings of betrayal, and distrust of health systems and federal authorities [29], [30], [31]. New environmental contamination events contribute to the burden of psychosocial stress. For example, in 2015, the Gold King Mine spill discharged acid mine drainage into a tributary to the Animas and San Juan Rivers, the latter being a sacred river for the Diné. The spill reduced dietary, recreational, cultural, spiritual, and livelihood uses of the San Juan River by Diné adults and children, and the environmental contamination was perceived as a threat to survival of the Diné culture and way of life, as well as a threat to health [32].

As this study was a scoping literature review, we did not assess included articles for quality, which is typical for systematic literature reviews and meta-analyses. While this means that some of the studies included in this review may be at risk of bias or have other flaws in their design and reporting, they still support our objective of describing the scope of knowledge about environmental health on the Navajo Nation.

The findings from this scoping review indicate need for additional occupational and environmental health research at the Navajo Nation. With respect to environmental hazards, in addition to metals contamination of soil, food, and water, other hazards known to exist on the Navajo Nation include indoor air pollution from solid fuels used for heating [20] and radon [33], and ambient air pollution from oil and gas extraction, among others. Many of these hazards are well known to have adverse health impacts, such as the association between use of wood-burning stoves and acute lower respiratory infection and illness in children [34]. Owing to limited resources, documentation of such hazards should motivate action to reduce exposure even in the absence of measured health impacts. A number of health disparities among Navajos have been directly tied to environmental exposures in other settings, among other determinants, including: childhood asthma, metabolic syndrome, youth and adult type 2 diabetes, and adverse birth outcomes, such as birth defects and developmental delays [29, 35], [36], [37]. Interventions to address these disparities should consider the contribution of occupational and environmental exposures. Further, there is a gap in research about adverse health outcomes associated with occupations other than uranium mining, as well as employment conditions and access to safe, healthy work.

This literature review was specifically focused on the Navajo Nation, and a review of occupational and environmental health research among Native Americans is beyond the scope of this work. However, many of the occupational and environmental hazards and health disparities experienced by the Diné are shared by other tribal nations in the U.S., and by indigenous peoples globally, owing to the systematic marginalization of these peoples and exploitation of natural resources by the U.S. and other governments [22]. As the second largest tribal nation in the United States, the Navajo Nation has greater resources with which to assess and address occupational and environmental health issues than many other tribal nations in the U.S., yet significant gaps in knowledge and health burdens remain. Hopefully, new research initiatives responsive to tribal priorities, inclusive of Native American investigators, and reflective of traditional ecological knowledge, will continue to develop, improving the health and well-being of the Diné and other Native Americans.