Low prevalence of anemia among Shuar communities of Amazonian Ecuador

Abstract

Objective
Anemia is an important global health challenge. We investigate anemia prevalence among Indigenous Shuar of Ecuador to expand our understanding of population‐level variation, and to test hypotheses about how anemia variation is related to age, sex, and market integration.

Methods
Hemoglobin levels were measured in a total sample of 1650 Shuar participants (ages 6 months to 86 years) from 46 communities between 2008 and 2017 to compare anemia prevalence across regions characterized by different levels of market integration.

Results
Shuar anemia rates among children under 15 years (12.2%), adult women (10.5%), and adult men (5.3%) were less than half of those previously documented in other neo‐tropical Indigenous populations. Anemia prevalence did not vary between more traditional and market integrated communities (OR = 0.47, p = .52). However, anemia was negatively associated with body mass index (OR = 0.47, p = .002).

Conclusions
Compared to other South American Indigenous populations, anemia prevalence is relatively low among Shuar of Ecuador and invariant with market integration. Understanding this pattern can provide valuable insights into anemia prevention among at‐risk populations.

Full text

SHORT REPORT
Low prevalence of anemia among Shuar communities of
Amazonian Ecuador
Alicia M. DeLouize
1
| Melissa A. Liebert
2
| Felicia C. Madimenos
3,4
|
Samuel S. Urlacher
5,6
| Joshua M. Schrock
1
| Tara J. Cepon-Robins
7
|
Theresa E. Gildner
8
| Aaron D. Blackwell
9
| Christopher J. Harrington
1
|
Dorsa Amir
10
| Richard G. Bribiescas
11
| James Josh Snodgrass
1,12
|
Lawrence S. Sugiyama
1
1
Department of Anthropology, University of Oregon, Eugene, Oregon
2
Department of Anthropology, Northern Arizona University, Flagstaff, Arizona
3
Department of Anthropology, Queens College (CUNY), Flushing, New York
4
New York Consortium in Evolutionary Primatology (NYCEP), New York, New York
5
Department of Anthropology, Baylor University, Waco, Texas
6
Child and Brain Development Program, CIFAR, Toronto, Canada
7
Department of Anthropology, University of Colorado-Colorado Springs, Colorado Springs, Colorado
8
Department of Anthropology, Washington University in St. Louis, St. Louis, Missouri
9
Department of Anthropology, Washington State University, Pullman, WA
10
Department of Psychology, Boston College, Chestnut Hill, Massachusetts
11
Department of Anthropology, Yale University, New Haven, Connecticut
12
Center for Global Health, University of Oregon, Eugene, Oregon
Correspondence
Alicia M. DeLouize, Department of
Anthropology, 1218 University of Oregon,
Eugene, OR 97403, USA.
Email: adelouiz@uoregon.edu
Funding information
Evonuk Foundation; Foundation for the
National Institutes of Health, Grant/
Award Number: DP1OD000516-04;
Harvard University Sheldon Traveling
Fellowship; Leakey Foundation; Lewis
and Clark Exploration Grant; National
Science Foundation (NSF) of the United
States, Grant/Award Numbers: BCS-
0824602, BCS-0925910, BCS-1340958,
BCS-1341165, BCS-1650674, DGE-
1144152, DGE-2011109300, SMA-1606852;
Ryoichi Sasakawa Young Leaders
Fellowship Fund; University of Oregon;
University of Oregon Anthropology
Department; University of Oregon Center
for Latino/a and Latin American Studies;
University of Oregon Institute of Cognitive
and Decision Sciences; Wenner-Gren
Abstract
Objective: Anemia is an important global health challenge. We investigate
anemia prevalence among Indigenous Shuar of Ecuador to expand our under-
standing of population-level variation, and to test hypotheses about how ane-
mia variation is related to age, sex, and market integration.
Methods: Hemoglobin levels were measured in a total sample of 1650 Shuar
participants (ages 6 months to 86 years) from 46 communities between 2008
and 2017 to compare anemia prevalence across regions characterized by differ-
ent levels of market integration.
Results: Shuar anemia rates among children under 15 years (12.2%), adult
women (10.5%), and adult men (5.3%) were less than half of those previously
documented in other neo-tropical Indigenous populations. Anemia prevalence
did not vary between more traditional and market integrated communities
(OR = 0.47, p= .52). However, anemia was negatively associated with body
mass index (OR = 0.47, p= .002).
Conclusions: Compared to other South American Indigenous populations,
anemia prevalence is relatively low among Shuar of Ecuador and invariant
Received: 26 June 2020 Revised: 17 February 2021 Accepted: 18 February 2021
DOI: 10.1002/ajhb.23590
Am J Hum Biol. 2021;e23590. wileyonlinelibrary.com/journal/ajhb © 2021 Wiley Periodicals LLC. 1of7
https://doi.org/10.1002/ajhb.23590

Foundation, Grant/Award Numbers: 7970,
8476, 8749, 9231, Engaged Anthropology
Grant
with market integration. Understanding this pattern can provide valuable
insights into anemia prevention among at-risk populations.
1|INTRODUCTION
Anemia is a blood disorder characterized by insuffi-
cient oxygen transport by hemoglobin (Hb) in erythro-
cytesandiscommonlydefinedasHblevelsbelowage-
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 disor-
ders, low blood pressure, shortness of breath, reduced
infection resistance, and lower cognitive function
(Kassebaum, 2016). Dietary iron is needed for Hb func-
tion, with iron requirements varying by age, sex, men-
strual 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 underly-
ing causes, the WHO considers this health challenge a
global priority (WHO, 2011).
Anemia prevalence among South American Indige-
nous neotropical populations range from 19% to 100%
in women, 6% to 79% in men, and 39% to 98% in chil-
dren (Table 1). These generally high rates are attrib-
uted 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 mar-
ket 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 Val-
ley (UV), which has greater access to healthcare facili-
ties 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 par-
asitic 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
2.1 |Participants
Shuar are an Indigenous lowland neotropical population
of 60 000–110 000 individuals. The CC region is more
geographically isolated than the UV region, leading to
differences in MI, lifestyle, economics, and diet (Urlacher
et al., 2016). Traditional cultigens (including manioc,
plantains, sweet potatoes, and yams) remain dietary sta-
ples in both regions. Reliance on foraging, fishing, and
hunting vary but are generally greater in the CC region
(e.g., Liebert et al., 2013; Urlacher et al., 2016). Shuar
exhibit high rates of stunting and infectious disease bur-
den but with complex inter- and intra-regional variation
in prevalence (e.g., Blackwell, Pryor, Pozo, Tiwia, &
Sugiyama, 2009; Gildner et al., 2016, 2020; Urlacher
et al., 2018). Helminth infection rates of whipworm and
roundworm are high (Cepon-Robins et al., 2014; Gildner
et al., 2016, 2020).
Data were collected across nine field seasons from
August 2008 through November 2017, as a part of the
Shuar Health and Life History Project (shuarproject.org).
Participants included 1650 Shuar (746 men, 904 women
[26 pregnant]) ranging in age from 6 months to 86 years
(M= 19.20, SD = 16.73), including 1062 participants
from 29 UV communities (464 men, 598 women), and
588 participants from 17 CC communities (282 men,
306 women). In instances of repeat Hb measures, only
the visit with the most recent Hb measurement was used
in the analysis; thus, only one measurement was
included per individual. Adults provided informed con-
sent to participate. Parental consent and child assent
were obtained for children and adolescents <15 years
old, the legal age of consent in Ecuador. The study was
approved by the IRB of the University of Oregon, by com-
munity leaders upon community consensus, and by the
Federacíon Interprovincial de Centros Shuar.
2.2 |Measures
2.2.1 |Predictor variables
Age, height, and weight data were collected as described
in detail elsewhere (Liebert et al., 2013; Urlacher
et al., 2016). BMI was calculated using standard methods
(weight [kg]/height [m]
2
).
2of7 DELOUIZE ET AL.

TABLE 1 Comparison of Shuar mean Hb values and anemia prevalence with other South American populations
Group
Children Adults
References
Anemia
(%)
WHO
significance
Age
(yrs)
Women Men
Age
(yrs)
Anemia
(%)
WHO
significance
Anemia
(%)
WHO
significance
Aruak/Karibe (Brazil) 66 Severe 0.5–10 Mondini, Rodrigues, Gimeno, &
Baruzzi, 2009
Suruí (Brazil) 81 Severe 0.5–10 Orellana, Coimbra Jr, Lourenço, &
Santos, 2006
Terena (Brazil) 51 Severe 2–4 Morais, Alves, & Fagundes-
Neto, 2005
Indigenous (Brazil) 51 Severe 0.5–5 Leite et al., 2013
Pueblo Tacana (Bolivia) 42 Moderate 0.5–10 Benefice, Monroy, Jiménez, &
López, 2006
Tsimane (Bolivia) 39 Moderate 0.5–15 23 Moderate 19 Mild 15+ Blackwell, unpublished
Qom/Toba (Argentina) 28 Moderate 18+ Goetz & Valeggia, 2017
Indigenous (Colombia) 31 Moderate 6 Mild 18+ Castillo, Oliveros, & Mora, 2014
Quechua (Peru) 49 Moderate 0.5–12 Cabada et al., 2015
Indigenous (Peru) 51 Severe 0.5–11 Anticona and San Sebastian 2014
Bari (Venezuela) 54 Severe 1–18 Diez-Ewald et al., 1997
Piaroa (Venezuela) 98 Severe 1–10 88 Severe 79 Severe 11+ Nieves García-Casal et al., 2008
Warao (Venezuela) 61 Severe 7–14 Wilbert & Layrisse, 1980
Interior Alto Ocamo Yanomamo
(Venezuela)
84 Severe 0.5–14 100 Severe 58 Severe 15+ Grenfell et al., 2008
Ocamo Yanomamo (Venezuela) 57 Severe 0.5–14 100 Severe 8 Mild 15+ Grenfell et al., 2008
Quechua (Ecuador) 50 Severe 47 Severe 15+ Pleasants, 2014
Secoya (Ecuador) 19 Mild 26 Moderate 15+ Pleasants, 2014
Cofán (Ecuador) 31 Moderate 29 Moderate 15+ Pleasants, 2014
Shuar (Ecuador) 12 Mild 0.5–14 11 Mild 5 Normal 15+ This study
Trans Cutucú Shuar
(Ecuador)
12 Mild 0.5–14 10 Mild 6 Mild 15+ This study
Upano Valley Shuar
(Ecuador)
13 Mild 0.5–14 11 Mild 5 Normal 15+ This study
DELOUIZE ET AL.3of7

2.2.2 |Hemoglobin
A finger prick with a sterile, disposable lancet was used
to collect one drop (10 μl) of whole capillary blood into
a microcuvette and analyzed using a HemoCue Hb201+
analyzer (HemoCue AB, Cypress, CA). No daily smokers
were in the sample; therefore, Hb levels were only
adjusted for minor variation in altitude between commu-
nities (WHO, 2011).
2.2.3 |Anemia
Anemia prevalence was evaluated according to
WHO (2011) standard cutoff levels for defined anemia
groups: children under 5 years, 5–11 years, and
12–14 years; nonpregnant women; pregnant women; and
men aged 15 years or older.
2.2.4 |Statistics
Binary logistic regressions with mixed effects were per-
formed to predict anemia from region, sex, and BMI;
each predictor was entered into individual models. For
analyses between anemia and region and anemia and
BMI, sex, age, pregnancy status, and year of data collec-
tion were controlled for by including WHO defined ane-
mia groups (WHO, 2011) and year of data collection as
random intercepts. For analyses between anemia and
sex, juveniles and adults were analyzed separately, preg-
nancy was included as a fixed effect for adults, and com-
munity and year of data collection were included as
random intercepts. A binary logistic generalized additive
regression was performed to predict anemia from thin
plate splines fit to age using REML, while controlling for
community, year of data collection, sex, and pregnancy
status. Analyses were conducted in R 3.6.1 with α= .05.
All statistical assumptions were met before analysis.
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%, respec-
tively), 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 com-
pared to other South American populations and compa-
rable 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 life-
style (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 rela-
tively 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
TABLE 2 Shuar anemia prevalence and hemoglobin levels by WHO age/sex criteria
Shuar age class n
Hb M
(mg/dl)
Hb SD
(mg/dl)
Mild
anemia (%)
Moderate
anemia (%)
Severe
anemia (%)
Anemia
prevalence (%)
Children (0–4 yrs) 127 11.75 1.03 15.7 4.7 0.0 20.4
Children (5–11 yrs) 653 12.61 1.00 6.1 4.7 0.0 10.9
Children (12–14 yrs) 164 13.30 1.44 6.7 3.7 0.6 11.0
Nonpregnant Women (≥15 yrs) 382 13.31 1.33 6.2 3.7 0.5 10.5
Pregnant women (>15 yrs) 26 12.10 1.06 7.7 3.8 0.0 11.5
Men (≥15 yrs) 265 15.08 1.36 3.4 1.5 0.4 5.3
Note: The hemoglobin (Hb) cutoff values for anemia, mild anemia, moderate anemia, severe anemia, and anemia cutoff values were determined by current
World Health Organization guidelines (WHO, 2011).
4of7 DELOUIZE ET AL.

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 com-
munities. Common staples (e.g., plantains, sweet pota-
toes, yams) also contain some non-heme iron. Wheat and
corn, which inhibit iron absorption and limit bioavail-
ability, are rarely consumed (Liebert et al., 2013). In
Ecuador, the National Food Nutrition Program (PANN,
2000) for children 6–24 months includes iron fortifica-
tion, which reduces anemia (Lutter et al., 2008), yet
implementation appears uneven across Shuar communi-
ties and Shuar have lower anemia prevalence than
Ecuadorians in general (Sackey, Weigel, &
Armijos, 2003). Low levels of malaria could also be a con-
tributing 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 Indige-
nous 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 ane-
mia 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 infra-
structure 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 preva-
lence among the Shuar as integration into the market
economy accelerates.
ACKNOWLEDGMENTS
We thank the Shuar for their participation and hospital-
ity. We also thank the Federación Interprovincial de
Centros Shuar (FICSH), former Dirigentes de Salud
Oswaldo Mankash and Favio Chinkim, and our numer-
ous colleagues, research assistants and friends who made
this research possible including: Ruby Fried; Tiffany
Gandolfo; Estella, Luzmila, Katy, and Charo Jempekat;
Samantha,Utitiai; Marcia Saramiento; Dona Berta and
Don Guimo; Nelly Sardi; Cesar Kayap; and Medardo
Tunki.
AUTHOR CONTRIBUTIONS
Alicia DeLouize: Data curation; formal analysis; visuali-
zation; writing-original draft; writing-review & editing.
Melissa Liebert: Data curation; formal analysis; funding
acquisition; investigation; writing-original draft; writing-
review & editing. Felicia Madimenos: Funding acquisi-
tion; 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 Black-
well: Formal analysis; funding acquisition; investigation;
visualization; writing-review & editing. Christopher
Harrington: Investigation. Dorsa Amir: Investigation;
writing-review & editing. Richard Bribiescas: Investiga-
tion; writing-review & editing. James Snodgrass:
Funding acquisition; methodology; project administra-
tion; 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.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are avail-
able on request by emailing the form found at https://www.
shuarproject.org/data-sharing to shuarproject@gmail.com.
The data are not publicly available due to privacy or ethical
restrictions.
ORCID
Alicia M. DeLouize https://orcid.org/0000-0002-9045-
6428
Melissa A. Liebert https://orcid.org/0000-0001-8013-
6773
Felicia C. Madimenos https://orcid.org/0000-0001-
5442-232X
Samuel S. Urlacher https://orcid.org/0000-0002-6489-
4117
Tara J. Cepon-Robins https://orcid.org/0000-0002-4508-
8507
Theresa E. Gildner https://orcid.org/0000-0001-7486-
5208
Aaron D. Blackwell https://orcid.org/0000-0002-5871-
9865
DELOUIZE ET AL.5of7

Dorsa Amir https://orcid.org/0000-0003-0255-0228
James Josh Snodgrass https://orcid.org/0000-0002-
7021-777X
Lawrence S. Sugiyama https://orcid.org/0000-0003-
1279-0006
REFERENCES
Anticona, C., & San Sebastian, M. (2014). Anemia and malnutrition
in indigenous children and adolescents of the Peruvian Ama-
zon in a context of lead exposure: A cross-sectional study.
Global Health Action,7(1), 22888. https://doi.org/10.3402/gha.
v7.22888
Benefice, E., Monroy, S. L., Jiménez, S., & López, R. (2006). Nutri-
tional status of Amerindian children from the Beni River (low-
land Bolivia) as related to environmental, maternal and dietary
factors. Public Health Nutrition,9(3), 327–335. https://doi.org/
10.1079/PHN2005852
Blackwell,A.D.,Pryor,G.,Pozo,J.,Tiwia,W.,&
Sugiyama, L. S. (2009). Growth and market integration in
Amazonia: A comparison of growth indicators between
Shuar, Shiwiar, and nonindigenous school children. Amer-
ican Journal of Human Biology,21(2), 161–171. https://
doi.org/10.1002/ajhb.20838
Cabada, M. M., Goodrich, M. R., Graham, B., Villanueva-
Meyer, P. G., Deichsel, E. L., Lopez, M., …White, A. C. (2015).
Prevalence of intestinal helminths, anemia, and malnutrition
in Paucartambo, Peru. Pan American Journal of Public Health
Revista Panamericana de Salud Pública,37(2), 69–75.
Castillo, M., Oliveros, A., & Mora, A. (2014). Description of the
health status of Colombian indigenous communities through
basic laboratory test. Journal of Life Sciences,8(9), 789–793.
Cepon-Robins, T. J., Liebert, M. A., Gildner, T. E., Urlacher, S. S.,
Colehour, A. M., Snodgrass, J. J., Madimenos, F. C., &
Sugiyama, L. S. (2014). Soil-transmitted helminth prevalence
and infection intensity among geographically and economically
distinct Shuar communities in the Ecuadorian Amazon. Jour-
nal of Parasitology,100(5), 598–607.
Coa, R., & Ochoa, L. H. (2009). Bolivia Encuesta Nacional de
Demografía y Salud: ENDSA-2008. Calverton, Maryland:
Ministerio de Salud y Deportes and Macro International. https://
dhsprogram.com/pubs/pdf/FR228/FR228[08Feb2010].pdf
Diez-Ewald, M., Torres-Guerra, E., Layrisse, M., Leets, I.,
Vizcaíno, G., & Arteaga-Vizcaíno, M. (1997). Prevalence of ane-
mia, iron, folic acid and vitamin B12 deficiency in two Bari
Indian communities from western Venezuela. Investigacion
Clinica,38(4), 191–201.
Gildner, T. E., Cepon-Robins, T. J., Liebert, M. A.,
Urlacher,S.S.,Madimenos,F.C.,Snodgrass,J.J.,&
Sugiyama, L. S. (2016). Regional variation in Ascaris
lumbricoides and Trichuris trichiura infections by age cohort
and sex: Effects of market integration among the indigenous
Shuar of Amazonian Ecuador. Journal of Physiological
Anthropology,35(1), 28.
Gildner, T. E., Cepon-Robins, T. J., Liebert, M. A., Urlacher, S. S.,
Schrock, J. M., Harrington, C. J., Madimenos, F. C.,
Snodgrass, J. J., & Sugiyama, L. S. (2020). Market integration
and soil-transmitted helminth infection among the Shuar of
Amazonian Ecuador. PLoS One,15(7), e0236924.
Goetz Teddy, G., & Valeggia Claudia. (2017). The ecology of ane-
mia: Anemia prevalence and correlated factors in adult indige-
nous women in Argentina. American Journal of Human
Biology,29(3), e22947. http://dx.doi.org/10.1002/ajhb.22947.
Grenfell, P., Fanello, C. I., Magris, M., Goncalves, J.,
Metzger, W. G., Vivas-Martínez, S., Curtis, C., & Vivas, L.
(2008). Anaemia and malaria in Yanomami communities with
differing access to healthcare. Transactions of the Royal Society
of Tropical Medicine and Hygiene,102(7), 645–652. https://doi.
org/10.1016/j.trstmh.2008.02.021
Kassebaum, N. J. (2016). The global burden of anemia.
Hematology/Oncology Clinics,30(2), 247–308.
Kim, I., Yetley, E. A., & Calvo, M. S. (1993). Variations in iron-
status measures during the menstrual cycle. American Journal
of Clinical Nutrition,58(5), 705–709. https://doi.org/10.1093/
ajcn/58.5.705
Le, C. H. H. (2016). The prevalence of anemia and moderate-severe
anemia in the US population (NHANES 2003-2012). PLoS One,
11(11), e0166635. https://doi.org/10.1371/journal.pone.0166635
Leite, M. S., Cardoso, A. M., Coimbra, C. E., Welch, J. R.,
Gugelmin, S. A., Cabral, P., …Lúcia Escobar, A. (2013). Preva-
lence of anemia and associated factors among indigenous chil-
dren in Brazil: Results from the first National Survey of
indigenous People's health and nutrition. Nutrition Journal,
12(69), https://doi.org/10.1186/1475-2891-12-69
Liebert, M. A., Snodgrass, J. J., Madimenos, F. C., Cepon, T. J.,
Blackwell, A. D., & Sugiyama, L. S. (2013). Implications of mar-
ket integration for cardiovascular and metabolic health among
an indigenous Amazonian Ecuadorian population. Annals of
Human Biology,40(3), 228–242.
Lu, F. (2007). Integration into the market among indigenous peo-
ples: A cross-cultural perspective from the Ecuadorian Ama-
zon. Current Anthropology,48(4), 593–602.
Lutter, C. K., Rodríguez, A., Fuenmayor, G., Avila, L.,
Sempertegui, F., & Escobar, J. (2008). Growth and micronutri-
ent status in children receiving a fortified complementary food.
The Journal of Nutrition,138(2), 379–388. https://doi.org/10.
1093/jn/138.2.379
Mondini, L., Rodrigues, D. A., Gimeno, S. G., & Baruzzi, R. G.
(2009). Nutritional status and hemoglobin values of Aruak and
Karibe Indian children: Upper Xingu, Central Brazil,
2001-2002. Revista Brasileira de Epidemiologia,12, 469–477.
Morais, M. B., Alves, G. M. D. S., & Fagundes-Neto, U. (2005).
Estado nutricional de crianças índias terenas: evoluç~
ao do peso
e estatura e prevalência atual de anemia. Jornal de Pediatria,
81(5), 383–389.
Nieves García-Casal, M., Leets, I., Bracho, C., Hidalgo, M.,
Bastidas, G., Gomez, A., …Pérez, H. (2008). Prevalence of ane-
mia and deficiencies of iron, folic acid and vitamin B 12 in an
indigenous community from the Venezuelan Amazon with a
high incidence of malaria. IOrgano Oficial de la Sociedad
Latinoamericana de Nutrición,58,12–18.
Orellana, J. D., Coimbra, C. E., Jr., Lourenço, A. E. P., &
Santos, R. V. (2006). Nutritional status and anemia in Suruí
Indian children, Brazilian Amazon. Jornal De Pediatria,82(5),
383–388.
Pleasants, E. (2014). Food for thought: Impacts of market integration
on diet and health in indigenous communities in the northern
Ecuadorian Amazon. https://doi.org/10.17615/dd9z-v962.
6of7 DELOUIZE ET AL.

Sackey, M. E., Weigel, M. M., & Armijos, R. X. (2003). Predictors
and nutritional consequences of intestinal parasitic infections
in rural Ecuadorian children. Journal of Tropical Pediatrics,49
(1), 17–23.
Stevens, G. A., Finucane, M. M., De-Regil, L. M., Paciorek, C. J.,
Flaxman, S. R., Branca, F., …Ezzati, M. (2013). Global,
regional, and national trends in haemoglobin concentration
and prevalence of total and severe anaemia in children and
pregnant and non-pregnant women for 1995-2011: A systematic
analysis of population-representative data. The Lancet Global
Health,1, e16–e25. https://doi.org/10.1016/S2214-109X(13)
70001-9
Urlacher, S. S., Liebert, M. A., Josh Snodgrass, J., Blackwell, A. D.,
Cepon-Robins, T. J., Gildner, T. E., Madimenos, F. C.,
Amir, D., Bribiescas, R. G., & Sugiyama, L. S. (2016). Heteroge-
neous effects of market integration on sub-adult body size and
nutritional status among the Shuar of Amazonian Ecuador.
Annals of Human Biology,43(4), 316–329. https://doi.org/10.
1080/03014460.2016.1192219
Urlacher, S. S., Ellison, P. T., Sugiyama, L. S., Pontzer, H., Eick, G.,
Liebert, M. A., …Snodgrass, J. J. (2018). Tradeoffs between
immune function and childhood growth among Amazonian
forager-horticulturalists. Proceedings of the National Academy
of Sciences USA,115(17), E3914–E3921.
WHO - World Health Organization (2011). Haemoglobin concentra-
tions for the diagnosis of anaemia and assessment of severity.
Vitamin and Mineral Nutrition Information System. Geneva.
Retrieved from http://www.who.int/vmnis/indicators/
haemoglobin. Accessed November 2019.
Wilbert, J., & Layrisse, M. (1980). . Demographic and biological stud-
ies of the Warao Indians, UCLA Latin American Studies Series,
vol. 45. Los Angeles, CA: UCLA Latin American Center
Publications.
SUPPORTING INFORMATION
Additional supporting information may be found online
in the Supporting Information section at the end of this
article.
How to cite this article: DeLouize AM,
Liebert MA, Madimenos FC, et al. Low prevalence
of anemia among Shuar communities of
Amazonian Ecuador. Am J Hum Biol. 2021;e23590.
https://doi.org/10.1002/ajhb.23590
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