1 INTRODUCTION

Anemia is a blood disorder characterized by insufficient oxygen transport by hemoglobin (Hb) in erythrocytes and is commonly defined as Hb levels below age- and sex-specific cutoffs (WHO, 2011). It afflicts ~27% of people worldwide, 89% of whom live in low- and middle-income countries (Kassebaum, 2016). Anemia is associated with negative health outcomes including fatigue, headaches, poor growth, reproductive disorders, low blood pressure, shortness of breath, reduced infection resistance, and lower cognitive function (Kassebaum, 2016). Dietary iron is needed for Hb function, with iron requirements varying by age, sex, menstrual cycle status, and reproductive state. Pregnancy and growth increase iron requirements leading to the highest rates of anemia in young children and women (Kassebaum, 2016; Kim, Yetley, & Calvo, 1993). Since anemia is readily treatable by addressing the underlying causes, the WHO considers this health challenge a global priority (WHO, 2011).

Anemia prevalence among South American Indigenous neotropical populations range from 19% to 100% in women, 6% to 79% in men, and 39% to 98% in children (Table 1). These generally high rates are attributed to low dietary iron and vitamin intake, blood loss from intestinal macroparasites, infection with H. pylori, and inflammation from other infections (Kassebaum, 2016). Yet, it is unclear how lifestyle changes within these populations influence anemia rates. Data from Shuar of Amazonian Ecuador allow for an analysis of how market integration (MI: the degree of consumption from and production for a market economy; Lu, 2007) affects anemia rates (Liebert et al., 2013). Most Shuar live in two main regions of the Morona-Santiago province in Ecuador: the Upano Valley (UV), which has greater access to healthcare facilities and market centers (Liebert et al., 2013; Urlacher et al., 2016), and Cross-Cutucú (CC), which is more remote and generally associated with high rates of parasitic infection (Cepon-Robins et al., 2014; Gildner et al., 2016, 2020).

We hypothesize that anemia prevalence will vary according to MI status, with region serving as a proxy for MI. Specifically, we hypothesize that CC Shuar will have higher rates of anemia than UV Shuar. Further, we expect anemia prevalence will be associated with sex, age, and body mass index (BMI).

2 METHOD

3 RESULTS

Based on WHO (2011) criteria, anemia rates among most Shuar age- and sex-groups identified in this study are considered of mild public health significance (Table 2). Anemia prevalence for children under 15 years (12.2%), adult women (10.5%), and adult men (5.3%) were less than half that of the next lowest neo-tropical Indigenous comparator (Tsimane; Table 1). Analyses showed that anemia rates did not differ significantly by region (OR = 0.47, p = .52).

In participants under 15 years, anemia prevalence was higher in boys than girls (13.9% and 10.5%, respectively), but the difference was not significant (OR = 0.41, p = .09). However, controlling for pregnancy, adult women ≥15 years had higher rates of anemia (11.8%) than adult men (5.6%; OR = 0.69, p = .01). Anemia risk was significantly associated with age, with rates highest among the youngest and oldest participants (edf = 4.73, p < .001; Figure S1). Finally, participants with higher BMI levels had lower prevalence of anemia (OR = 0.47, p = .002).

4 DISCUSSION

Anemia prevalence among Shuar is generally low compared to other South American populations and comparable to levels in high-income countries (Kassebaum, 2016). Furthermore, there was no difference in anemia prevalence between UV and CC Shuar. Yet, BMI was negatively associated with anemia, suggesting that lifestyle (e.g., diet) might influence anemia rates, despite the lack of regional differences (Liebert et al., 2013). The low rate of anemia is surprising given that Shuar have a relatively heavy parasitic and infectious disease burden (Cepon-Robins et al., 2014; Gildner et al., 2016, 2020), severe enough to cause growth faltering in children (Urlacher et al., 2018). However, parasitic species known to contribute most heavily to anemia (e.g., hookworm; Kassebaum, 2016) do not appear to be common in this population (Cepon-Robins et al., 2014; Gildner et al., 2020).

The low rates of anemia among Shuar and lack of regional differences may be due to a variety of factors. Traditional Shuar diet includes iron-rich fish and hunted game, but consumption varies between and within communities. Common staples (e.g., plantains, sweet potatoes, yams) also contain some non-heme iron. Wheat and corn, which inhibit iron absorption and limit bioavailability, are rarely consumed (Liebert et al., 2013). In Ecuador, the National Food Nutrition Program (PANN, 2000) for children 6–24 months includes iron fortification, which reduces anemia (Lutter et al., 2008), yet implementation appears uneven across Shuar communities and Shuar have lower anemia prevalence than Ecuadorians in general (Sackey, Weigel, & Armijos, 2003). Low levels of malaria could also be a contributing factor as the UV is generally above the malarial zone and endemic malaria in CC was reduced through control efforts.

Anemia prevalence among the Shuar is comparable to Europeans, Canadians, and Australians, and lower than Ecuador overall and other South American Indigenous populations (Coa and Ochoa, 2009; Le, 2016; Sackey et al., 2003; Stevens et al., 2013). These findings suggest that subsistence-based lifestyles are not always associated with high rates of anemia. For example, CC and UV anemia rates were similar despite UV Shuar generally exhibiting higher MI, including access to healthcare infrastructure and market centers, and CC having greater reliance on fish and game (Liebert et al., 2013; Urlacher et al., 2016). Future research will consider the relative contributions of dietary factors, infection rates, and infrastructure as contributors to the relatively low anemia prevalence among Shuar. The low prevalence of anemia and similarity between regions are unexpected findings: understanding these results could identify key factors that can be targeted to reduce high anemia rates among at-risk populations and to maintain low anemia prevalence among the Shuar as integration into the market economy accelerates.

AUTHOR CONTRIBUTIONS

Alicia DeLouize: Data curation; formal analysis; visualization; writing-original draft; writing-review & editing. Melissa Liebert: Data curation; formal analysis; funding acquisition; investigation; writing-original draft; writing-review & editing. Felicia Madimenos: Funding acquisition; investigation; writing-review & editing. Samuel Urlacher: Funding acquisition; investigation; writing-review & editing. Joshua Schrock: Funding acquisition; investigation; writing-review & editing. Tara Cepon-Robins: Funding acquisition; investigation; writing-review & editing. Theresa Gildner: Funding acquisition; investigation; writing-review & editing. Aaron Blackwell: Formal analysis; funding acquisition; investigation; visualization; writing-review & editing. Christopher Harrington: Investigation. Dorsa Amir: Investigation; writing-review & editing. Richard Bribiescas: Investigation; writing-review & editing. James Snodgrass: Funding acquisition; methodology; project administration; supervision; writing-review & editing. Lawrence Sugiyama: Conceptualization; funding acquisition; investigation; methodology; project administration; supervision; writing-original draft; writing-review & editing.

CONFLICT OF INTEREST

The authors declare no conflict of interest.