The Journal of Nutrition 153 (2023) S1–S6

journal homepage: https://jn.nutrition.org/

Sponsored Supplement Publication

Exploring the Anemia Ecology: A New Approach to an Old Problem

Daniel J. Raiten 1, Denish Moorthy 2, *, Laura S. Hackl 2, Omar Dary 3
1
Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, United States;
2
USAID Advancing Nutrition, JSI Research and Training Institute, VA, United States; 3 Division of Nutrition and Environmental Health, Office of
Maternal and Child Health and Nutrition, Bureau for Global Health, United States Agency for International Development, Washington, DC, United
States

A B S T R A C T

Our ability to identify anemia and all its permutations demands an approach that integrates the key elements of a complex “ecology,” which
intertwines biology and mechanistic aspects of nutrients with both the health status and underlying factors—physical, economic, social,
behavioral, demographic, and environmental. The complexity of anemia demands an ecologic approach that appreciates systems biology,
translates sensitive and specific assessment methodologies and interventions, and ultimately improves clinical and public health outcomes.
This series of technical papers on anemia by the U.S. Agency for International Development (USAID) Advancing Nutrition Anemia Task
Force (ATF) is a first step in translating our ecologic approach to anemia with a view toward balancing research with its translation to
effective programs, interventions, and policy. This introductory overview describes the components of our ecologic approach—linking the
biology of anemia with its assessment and using the learning from that confluence to devise context-specific interventions. This introductory
review briefly discusses the topics that underlie the biology and primary etiologies of anemia and presents a framework for public health
assessment of anemia, leading to appropriate public health interventions. The other 3 manuscripts in the supplement provide the details of
the arguments laid out in the introduction.

Keywords: anemia ecology, etiology, assessment methods, public health interventions

Statement of the problem 2. Applying that biology to its assessment

Although the exact global prevalence of anemia is unknown,
estimates place it between 23% [1] to 33% worldwide [2].
Reducing anemia prevalence has become an enduring target
for strategies to improve global health, engaging a broad swath
of the international research, policy, and program community.
We understand that anemia decreases the oxygen carrying ca-
pacity of the organism, thus affecting critical aspects of human
function and development; however, is that understanding
enough to be able to accomplish our communal goals for
reduction of this scourge? The following conceptual overview
introduces the series of papers of the U.S. Agency for Inter-
national Development (USAID) Advancing Nutrition Anemia
Task Force (ATF) representing a continuum of thought:
1. Developing an understanding of the biology of anemia and its
various etiologies
3. Developing and applying a framework to translate that sci-
ence to inform choice about context-specific interventions to
address anemia in individuals and populations.
Anemia coexists with pandemics of food/nutrition insecurity,
malnutrition, and infectious and noncommunicable diseases.
The manifestations of this confluence are most severe in women,
infants, and children [3]. Our ability to identify anemia and all
its permutations demands an approach that integrates the key
elements of a complex “ecology.” Box 1 highlights critical
operating assumptions about how to address anemia. (The ATF
papers describe how genetic factors may influence anemia, other
hematologic conditions, and iron status. The ATF working group
chairs recognize that race and ethnicity are social constructs that
lack a biological foundation and fail to take account of the extent
of variability in the myriad nongenetic determinants of physi-
ology [4,5]. Accordingly, the task force will not use racial and

Abbreviations: ATF, Anemia Task Force; BRINDA, Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia; IDA, iron deficiency anemia.
* Corresponding author. E-mail address: denish_moorthy@jsi.com (D. Moorthy).

https://doi.org/10.1016/j.tjnut.2023.07.016
Received 8 December 2022; Received in revised form 28 February 2023; Accepted 31 July 2023; Available online 30 September 2023
0022-3166/© 2023 The Authors. Published by Elsevier Inc. on behalf of American Society for Nutrition. This is an open access article under the CC BY license (http://
creativecommons.org/licenses/by/4.0/).
D.J. Raiten et al.
BOX 1
Operating assumptions about how to address anemia. These are our assumptions that underpin our approach to anemia.
Operating Assumptions
- Anemia, which is a reflection of the health of the hematological system, has multiple causal factors (i.e., an ecology existing of genetics, disease,
nutrition, and the environment).
- An ecology defines the interactions between a complex system, here anemia’s interactions with internal (biology, health context) and external
(nutrition, food insecurity, physical, social, and behavioral) environments.
- Our understanding of the components of the anemia ecology is critical to our efforts to identify and treat with precision at both individual and
population levels.
ethnic classifications for reference intervals in diagnostic eval-
uation or for other descriptive purposes.)
Anemia exemplifies the challenges of the global health and
nutrition enterprise (i.e., how to understand health and disease
in a complex global health environment, how to assess a complex
problem, and how to develop context-specific interventions to
address that complexity). Fundamentally, if reducing anemia is
the public health target, we need to answer critical questions,
such as the following:
1. What are the contributions of various factors (genetic, phys-
iologic, and nutritional) to the causation of anemia?
2. Among the nutritional causes of anemia, which of the
following nutrients—iron, folate, vitamin B12, vitamin A,
riboflavin, and perhaps, vitamin B6—are responsible, indi-
vidually or in combination?
3. How do we address challenges of assessment, including:
— How do we make a differential diagnosis about causes of
anemia particularly at population levels?
— What are appropriate approaches for measuring hemo-
globin (venous and/or capillary blood samples)? [6]
— Can/should we make judgments about the role of nutrition
in the absence of relevant biomarkers of iron or other sus-
pected nutrients and indicators of infection/inflamm-ation?
The presumption in many circles is that anemia is synony-
mous with iron deficiency, and the latter is commonly attributed
to only low-iron intakes when infection/inflammation are
equally important causes of functional iron deficiency. A com-
mon view persists that 50% of anemia is caused by iron defi-
ciency [7]; however, recent estimates indicate that perhaps as
low as 25% or 37% in preschool children and women of repro-
ductive age, respectively, of anemia is because of iron deficiency
[8].
Although all anemia is not iron deficiency and all iron defi-
ciency is not anemia, iron deficiency remains a significant factor
in our ability to comprehensively address anemia—and a sig-
nificant global health concern in its own right. Despite signifi-
cant strides to reduce its prevalence, iron deficiency affects
~40% of the world’s women [9]. Although iron deficiency re-
mains the most significant micronutrient deficiency worldwide
(either because of low-iron intakes or low bioavailability or
impaired metabolism because of infection/inflammation and
parasitism), the conflation of iron deficiency with anemia im-
pairs our ability to address anemia comprehensively from a
public health perspective. (The ATF makes the following
distinction between bioavailability and micronutrient
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absorption: bioavailability reflects the physiochemical proper-
ties of the micronutrient form, food matrix, the composition of
the diet, and interactions with the gut environment, whereas
absorption is a metabolic process that also includes the con-
sumer’s health context as influenced by developmental stage,
genetics, infections, inflammation, etc. Within the context of the
overall ATF conceptual approach, bioavailability is a reflection
of the external environment, and absorption is the combined
influence of external and internal environments.) In addition to
the challenges of making differential diagnoses about prevalent
causes of anemia, the following factors also impact our ability to
address iron deficiency:
1. Because of the myriad of factors that affect it, questions remain
about the utility of the hemoglobin concentration, which
although valuable if measured correctly, as a bioindicator of
anemia, lacks the sensitivity and specificity to serve as a
biomarker of iron status and thus is not an appropriate trigger
for public health interventions to address iron nutrition [10].
2. Safety concerns exist about iron supplementation, particu-
larly in the context of malaria or other infections [11].
3. Limitations exist in using and interpreting current biomarkers
to distinguish between nutritional (dietary) iron deficiency
and responses to infection/inflammation [12].
4. There is a lack of precision in our ability to determine the
amount of remedial iron needed to improve and maintain iron
status to ensure health, particularly in different disease or
geographic contexts (in individuals or populati-ons).
In the absence of answers to these questions, our ability to
intervene is compromised both at the individual and population
level. The complexity of anemia demands an ecologic approach
that appreciates systems biology, translates sensitive and specific
assessment methodologies and interventions, and ultimately
improves clinical and public health outcomes. Our ability to
assess iron status and deficiency in individuals or populations is
challenged by the inability to differentiate between a dietary
insufficiency and a physiologic response to a concurrent health
issue (e.g., infection and/or inflammation).
In an effort to address the range of issues described above, the
USAID Advancing Nutrition ATF organized this series of papers
based on the continuum of thought represented in Figure 1. The
following sections provide a conceptual framework for address-
ing anemia used by the ATF in its deliberations. The 3 papers in
this supplement are linked and are informed by each other.
Brittenham et al. [13] describe the systemic and biologic un-
derpinnings of anemia, which is connected to the review of the
D.J. Raiten et al.
assessment of anemia and its causes by Williams et al. [14].
Loechl et al. [15] use the findings in the biology and assessment
of anemia papers to suggest evidence-based context-specific
interventions.
Biology of anemia prevalence and primary
etiologies
When considering the causes of anemia, the review by Kas-
sebaum et al. [16] is the point of reference for determining the
prevalence and primary causes of anemia globally. Although a
myriad of potentially concomitant causes of anemia exists [17],
for the purposes of the ATF deliberations, key elements of the
anemia ecology highlighted in Figure 1 were adapted to provide
focus. Specifically, we focus on the 3 core classes of etiology:
genetics, health status (e.g., infection/inflammation), and
nutrition, as they reflect the most common etiologies and
exemplify the nature of the challenges associated with the
biology, assessment, and translation to interventions confronting
the global health enterprise.
Nutritional causes of anemia
Iron-specific issues
Based on their analysis, iron deficiency anemia (IDA) remains
the leading cause of anemia globally. Although iron deficiency
was identified as the leading cause of anemia globally, the
analysis of Kassebaum et al. [16] was not based on iron
biomarker data (rather, residual unexplained anemia). Kasse-
baum et al. [16] concluded: “If we include those conditions such
as hookworm, schistosomiasis, and gastrointestinal and gyne-
cologic conditions that also manifest as IDA, its importance
grows even more apparent.”
They also observed: “Despite its continued dominance, a
decrease in IDA has been the primary driver of reduced global
anemia burden since 1990,” and added that “the improvements
have been partially offset; however, by increases in anemia
owing to chronic kidney diseases, hemoglobinopathies, malaria,
and schistosomiasis. Most of the increase in these latter condi-
tions is related to population aging (for chronic kidney diseases)
and population growth in endemic areas.”
These conclusions clearly highlight the following:
1. The complexity of the anemia challenge
2. The need to be able to distinguish between nutrition and
physiology (functional anemia due to infection/inflammation)
because the inclusive characterization of IDA used by Kasse-
baum et al. [16] above encompasses both nutritional and
functional iron deficiency (i.e., measurable deficits in bio-
markers of iron status that may be the result of nonnutritional
causes).
To add to the confusion, Kassebaum et al. [16] also suggested:
“IDA in high-risk, high-prevalence populations is likely due to
impaired micronutrient intake or bioavailability or absorp-
tion or mobilization. Addressing IDA by only increasing
micronutrient supplementation would not be a panacea for
ending anemia, however, because IDA is a final common
pathway of a heterogeneous group of conditions that also
includes acute or chronic hemorrhagic events and disorders of
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iron metabolism that may happen as a result of chronic illness
or malabsorption.”
Although an important acknowledgment of the role of iron in
anemia, this perspective perpetuates the perception about the
predominance of: 1) iron deficiency and 2) conflates nutritional
iron deficiency with impaired iron physiology due to a myriad of
causes.
Core questions remain (which we address in detail in both the
Biology [13] and Assessment [14] papers in this supplement):
1. How do the physiology and response to infection/disease
blend with the specific aspects of dietary iron nutrition and
bioavailability?
2. How should we represent IDA in the context of anemia, given
the latter’s multifactorial causation? Can we improve our
precision by moving away from its use as an umbrella term
inclusive of not only nutritional iron deficiency, but also the
potential role of multiple other nutrients—as well as the use
of iron status to reflect multiple responses to a challenged
physiology (i.e., infection, parasites, and blood loss)?
Other nutritional causes of anemia
Clinicians and researchers have linked multiple nutrients to
anemia. A recent meta-analysis of the impact of both nutrition-
specific and nutrition-sensitive interventions on hemoglobin/
anemia documented an inconsistent response to specific nutrient
interventions (e.g., vitamin A, vitamin C, zinc, and multiple
micronutrient supplements) as opposed to a relatively consistent
response to iron or iron-folic acid supplementation [18].
Whether these findings reflect a limitation in available data
and/or an incomplete understanding of the anemia ecology
needs to be determined.
There is clearly an association between nutritional status,
broadly, and the status of specific micronutrients. The question
is: which of them has the greatest public health implications, and
how best should we assess and intervene? The ATF focused on
iron, folate, vitamin B12, vitamin A, riboflavin, and vitamin B6
because these nutrients have the greatest public health impli-
cations based on prevalence of insufficiency. However, limiting
the discussion to these nutrients does not imply that we should
exclude other nutrients (micro or macro) from consideration in
either the etiology or assessment of anemia, if the context sug-
gests otherwise (e.g., local prevalence of food/nutrition insecu-
rity and malnutrition).
Anemia assessment
The ATF focused on public health approaches to addressing
anemia with a recognition that ultimately the target is improved
health of people. Figure 2 describes an overall approach to
assessment based on the biology of anemia.
Assessment: vernacular and expectation
Elucidating the interrelationships of diet, nutritional status,
health, and anemia depends on the methods and designs of
observational, preclinical, and clinical studies conducted to:
1. Evaluate programs, policies, and guidance.
2. Develop and support standards of clinical care.
3. Improve individual and population health outcomes.
D.J. Raiten et al.
FIGURE 1. A stepwise approach to addressing anemia. Our stepwise
approach to anemia includes an understanding of biology, linking
biology and biological mechanisms to assessment of anemia, and
finally translating biology and assessment information to action via
effective interventions.
The value and translatability of the results of such efforts
demand a vernacular that is clear in terms of sensitivity and
specificity as well as expectations. The ecologic approach out-
lined above provides an overarching framework for anemia
assessment. Methodologies for the clinical assessment of patients
and the surveillance of populations should also consider an
ecologic approach to address core questions about the assess-
ment of anemia and its causes, as covered by Williams et al. [14]
in this supplement.
The design of rigorous and reproducible studies to charac-
terize the relationships of diet/nutrition and health is a critical
component of anemia, prevention, care, and treatment efforts.
Validated and reliable assessment tools appropriate for the
questions asked and the specifics of the health and environ-
mental contexts must address the following:
1. Nutrient exposure—bioavailable amounts of nutrients
consumed
2. Nutritional status—accepted definitions for adequacy, mar-
ginal status, and deficiency
3. Nutrient function—the metabolic role(s) of specific nutrients
1. Reliance on hemoglobin measurement
2. Prevalence estimates
Anemia
1. Infection/inflammation
2. Nutrition (absolute/dietary or functional deficits)
3. Genetic conditions
Categorical 4. Multi-factorial (combinations of 1–3)
Diagnosis
1. Complete blood count and peripheral blood smear
2. Inflammation and infection markers
Differential 3. Iron and other suspected micronutrient biomarkers
Diagnosis 4. Genetic analyses
FIGURE 2. Anemia assessment process. The anemia assessment pro-
cess begins by estimating the prevalence of anemia by accurate he-
moglobin measurement, followed by a measurement of categorical
causes, such as infection/inflammation, nutrition deficits, genetic
conditions, or a combination of the 3. Within those categories, we
carry out a differential diagnosis by conducting additional tests until
we identify the cause (or causes).
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4. The relevant functional outcome(s).
Finally, it is critical to recognize that individuals are seldom
deficient in single nutrients; multiple nutrients in metabolic
systems typically function in synergy. Moreover, these factors
are not globally common but vary from country to country and
from community to community. These facts should inform our
efforts to develop more precise assessment methodologies and
study designs [19].
The ability to determine the health status of an individual
(i.e., the absence or presence of disease and potential concomi-
tants) can be difficult to achieve. Clinicians must decide not only
what biomarker, but also in what biological milieu (e.g., whole
blood, plasma/serum, urine, etc.), and what other factors to
assess based on their potential to influence the response and/or
significance of the analytic results. The Biomarkers of Nutrition
for Development project [20] employed an ecologic approach to
provide evidence-informed advice to researchers (basic, clinical,
and surveillance), clinicians, program developers/monitors, and
policy makers who rely on biomarkers to evaluate and make
decisions about the role of nutrients in health.
For the purposes of their deliberations, the ATF used the
following definitions:
1. Biomarkers: reflect the amount of specific nutrients inter-
preted within a specific biological context (i.e., health or
disease).
2. Bioindicators: reflect perturbations in biological systems (e.g.,
electroencephalography reflects aberrations in neurophysi-
ology, hemoglobin reflects hematologic status, C-reactive
protein reflects inflammation) but not specific nutrient status
(i.e., they cannot serve as a biomarker of particular nutrients).
3. Public health indicators: reflect disturbance in the external
ecology (e.g., socioeconomic status, food insecurity,
disability-adjusted life years, or stunting or underweight).
Because researchers often use these indicators to suggest
causality, this data trigger public health interventions.
Bioindicators and public health indicators may be nutrition-
ally sensitive without being nutrient-specific. As such, practi-
tioners cannot reliably use them to make inferences about diet/
nutrition and health without supporting information [21].
Two additional key issues emerged from the Biomarkers of
Nutrition for Development project’s deliberations that are rele-
vant here:
1. We need to recognize that nutrients often interact in ways
relevant to the selection and interpretation of biomarkers.
2. Nutrient utilization, status, and function can affect and be
affected by key biological/physiologic systems and responses.
The reciprocal relationships between nutrition and inflam-
mation exemplify the latter [22]. In addition, we have come to
appreciate the impact of the inflammatory response on the per-
formance and interpretation of nutritional biomarkers [12].
Some considerations about the importance of
inflammation
Inflammation represents a sequence of events with profound
metabolic and nutritional implications. Our ability to address
D.J. Raiten et al.
nutrition in the context of inflammation is challenged by the
following:
1. The direct impact on nutritional biology (i.e., implications for
all the processes involved in achieving nutritional status)
2. The impact of inflammation on assessment and interpretation
of biomarkers of nutrient status.
The nature of the bidirectional relationship between nutrition
and inflammation (i.e., each affects and is affected by the other)
has been reviewed [22]. With the observed increasing preva-
lence of widening obesity, we need additional research to
delineate the role of specific systemic inflammatory responses
seen in autoimmune diseases from the generalized inflammation
associated with obesity. The implications of inflammation, and
how to account for its impact on biomarker interpretation, is
particularly relevant to efforts to assess and treat anemia—and
has been the focus of a series of studies conducted under the
Biomarkers Reflecting Inflammation and Nutritional De-
terminants of Anemia (BRINDA) project [23–27]. Issues specific
to the intersection of inflammation with the biology and
assessment are covered in detail in the relevant sections of the
ATF papers in this supplement.
Anemia—informing context-specific choices
about interventions
The article by Loechl et al. [15] in this supplement explores
how best to synthesize the key aspects of anemia biology and
assessment to inform choice about context-specific in-
terventions. Recognizing the importance of these considerations
to clinical care, the primary focus for the ATF was on in-
terventions of public health relevance (i.e., those deliverable
at-scale and in a sustainable manner to large population groups).
Given the multifactorial nature of anemia, we consider the
clinical context when exploring intervention priorities. Some
causes of anemia (e.g., inherited blood disorders) are managed at
health facilities by expert personnel, and the efficiency of the
system of referral and follow-up varies by geographic and
resource contexts. A framework is presented for prioritization
that expands on the ecologic underpinning of the ATF’s approach
to allow consideration of a broader perspective of sustainability,
with a focus on relevant social, cultural, and environmental
factors. Although individual interventions are presented, either
independently or in combination, we acknowledge the impor-
tance of these broader considerations.
This series of technical papers on anemia by the ATF is a first
step in translating our ecologic approach to anemia with a view
toward balancing research with its translation to effective pro-
grams, interventions, and policy.
Author contributions
The authors’ responsibilities were as follows – DJR, OD, LH,
DM: designed the review; DJR: wrote the paper; DM: has primary
responsibility for final content; and all authors: read and
approved the final manuscript.
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The Journal of Nutrition 153 (2023) S1–S6
Conflicts of interest
The authors report no conflicts of interest.
Funding
This article is published as part of a supplement sponsored by
JSI Research & Training Institute, Inc. This manuscript was
developed by the USAID Advancing Nutrition Anemia Task Force
(ATF), which is supported by the U.S. Agency for International
Development. The review manuscript was prepared under the
terms of contract 7200AA18C00070 awarded to JSI Research &
Training Institute, Inc. (JSI). USAID staff participated in the ATF
meetings and working groups in their capacity as anemia experts
and served as coauthors of the review papers. The contents of
this manuscript are those of the authors and do not necessarily
represent the official position of the United States Agency for
International Development, the National Institutes of Health, or
the U.S. government.
References
[1] W. Gardner, N. Kassebaum, Global, regional, and national prevalence of
anemia and its causes in 204 countries and territories, 1990–2019, Curr.
Dev. Nutr. 4 (2020) 830, https://doi.org/10.1093/cdn/nzaa053_035.
[2] N.J. Kassebaum, R. Jasrasaria, M. Naghavi, S.K. Wulf, N. Johns,
R. Lozano, et al., A systematic analysis of global anemia burden from
1990 to 2010, Blood 123 (5) (2014) 615–624, https://doi.org/10.1182/
blood-2013-06-508325.
[3] G.O. Boateng, M.R. Balogun, F.O. Dada, F.A. Armah, Household energy
insecurity: dimensions and consequences for women, infants and
children in low- and middle-income countries, Soc. Sci. Med. 258
(2020) 113068, https://doi.org/10.1016/j.socscimed.2020.113068.
[4] C.P. Duggan, A. Kurpad, F.C. Stanford, B. Sunguya, J.C. Wells, Race,
ethnicity, and racism in the nutrition literature: an update for 2020, Am.
J. Clin. Nutr. 112 (6) (2020) 1409–1414, https://doi.org/10.1093/
ajcn/nqaa341.
[5] A.C. Weyand, P.T. McGann, Eliminating race-based reference ranges in
haematology: a call to action, Lancet Haematol 8 (6) (2021) e462–e466,
https://doi.org/10.1016/S2352-3026(21)00106-X.
[6] L.M. Neufeld, L.M. Larson, A. Kurpad, S. Mburu, R. Martorell,
K.H. Brown, Hemoglobin concentration and anemia diagnosis in venous
and capillary blood: biological basis and policy implications, Ann. N. Y.
Acad. Sci. 1450 (1) (2019) 172–189, https://doi.org/10.1111/
nyas.14139.
[7] A. Lopez, P. Cacoub, I.C. Macdougall, L. Peyrin-Biroulet, Iron deficiency
anaemia, Lancet 387 (10021) (2016) 907–916, https://doi.org/
10.1016/S0140-6736(15)60865-0.
[8] N. Petry, I. Olofin, R.F. Hurrell, E. Boy, J.P. Wirth, M. Moursi, et al., The
proportion of anemia associated with iron deficiency in low, medium,
and high human development index countries: a systematic analysis of
national surveys, Nutrients 8 (11) (2016) 693, https://doi.org/
10.3390/nu8110693.
[9] World Health Organization, The global prevalence of anaemia in 2011,
World Health Organization, Geneva, Switzerland, 2015.
[10] Development Initiatives, Chapter 03. Three issues in critical need of
attention. 2018 Global Nutrition Report: Shining a light to spur action
on nutrition [Internet], Development Initiatives, Bristol, UK, 2018.
Available from: https://globalnutritionreport.org/d20b82.
[11] D.J. Raiten, F.A. Ashour, Iron: current landscape and efforts to address a
complex issue in a complex world, J. Pediatr. 167 (4) (2015) S3–S7,
https://doi.org/10.1016/j.jpeds.2015.07.013, suppl.
[12] P.S. Suchdev, S.M. Namaste, G.J. Aaron, D.J. Raiten, K.H. Brown,
R. Flores-Ayala, Overview of the Biomarkers Reflecting Inflammation
and Nutritional Determinants of Anemia (BRINDA) project, Adv. Nutr. 7
(2) (2016) 349–356, https://doi.org/10.3945/an.115.010215.
D.J. Raiten et al.
[13] G.M. Brittenham, G. Moir-Meyer, K.M. Abuga, A. Datta-Mitra,
C. Cerami, R. Green, et al., Biology of anemia: a public health
perspective, J. Nutr. 153 (2023) S7–S28, https://doi.org/10.1016/
j.tjnut.2023.07.018.
[14] A.M. Williams, K.H. Brown, L.H. Allen, O. Dary, D. Moorthy,
P.S. Suchdev, Improving anemia assessment in clinical and public
health settings, J. Nutr. 153 (2023) S29–S41, https://doi.org/10.1016/
j.tjnut.2023.05.032.
[15] C.U. Loechl, A. Datta-Mitra, L. Fenlason, R. Green, L.S. Hackl, M. Koso-
Thoman, et al., Approaches to address the anemia challenge, J. Nutr.
153 (2023) S42–S59, https://doi.org/10.1016/j.tjnut.2023.07.017.
[16] N.J. Kassebaum, GBD 2013 Anemia Collaborators, The global burden of
anemia, Hematol. Oncol. Clin. North Am. 30 (2) (2016) 247–308,
https://doi.org/10.1016/j.hoc.2015.11.002.
[17] D. Glinz, R.F. Hurrell, A.A. Righetti, C. Zeder, L.G. Adiossan, H. Tjalsma,
et al., Ivorian school-age children, infection with hookworm does not
reduce dietary iron absorption or systemic iron utilization, whereas
afebrile Plasmodium falciparum infection reduces iron absorption by
half, Am. J. Clin. Nutr. 101 (3) (2015) 462–470, https://doi.org/
10.3945/ajcn.114.090175.
[18] D. Moorthy, R. Merrill, S. Namaste, L. Iannotti, The impact of nutrition-
specific and nutrition-sensitive interventions on hemoglobin concentrations
and anemia: a meta-review of systematic reviews, Adv. Nutr. 11 (6) (2020)
1631–1645, https://doi.org/10.1093/advances/nmaa070.
[19] D.J. Raiten, G.F. Combs, A.L. Steiber, A.A. Bremer, Perspective:
nutritional status as a biological variable (NABV): integrating nutrition
science into basic and clinical research and care, Adv. Nutr. 12 (5)
(2021) 1599–1609, https://doi.org/10.1093/advances/nmab046.
[20] D.J. Raiten, S. Namaste, B. Brabin, G. Combs, M.R. L’Abbe,
E. Wasantwisut, et al., Executive summary—biomarkers of nutrition for
development: building a consensus, Am. J. Clin. Nutr. 94 (2) (2011)
633S–650S, https://doi.org/10.3945/ajcn.110.008227.
S6
The Journal of Nutrition 153 (2023) S1–S6
[21] D. Raiten, G. Combs, Biomarkers and bio-indicators: providing clarity in
the face of complexity, Sight and Life Magazine 29 (1) (2015) 39–44.
[22] D.J. Raiten, F.A. Sakr Ashour, A.C. Ross, S.N. Meydani, H.D. Dawson,
C.B. Stephensen, et al., Inflammation and Nutritional Science for
Programs/Policies and Interpretation of Research Evidence (INSPIRE),
J. Nutr. 145 (5) (2015) 1039S–1108S, https://doi.org/10.3945/
jn.114.194571.
[23] L.M. Larson, S.M. Namaste, A.M. Williams, R. Engle-Stone, O.Y. Addo,
P.S. Suchdev, et al., Adjusting retinol-binding protein concentrations for
inflammation: Biomarkers Reflecting Inflammation and Nutritional
Determinants of Anemia (BRINDA) project, Am. J. Clin. Nutr. 106
(suppl 1) (2017) 390S–401S, https://doi.org/10.3945/
ajcn.116.142166.
[24] S.M. Namaste, G.J. Aaron, R. Varadhan, J.M. Peerson, P.S. Suchdev,
BRINDA Working Group, Methodologic approach for the Biomarkers
Reflecting Inflammation and Nutritional Determinants of Anemia
(BRINDA) project, Am. J. Clin. Nutr. 106 (suppl 1) (2017) 333S–347S,
https://doi.org/10.3945/ajcn.116.142273.
[25] F. Rohner, M. Zimmermann, P. Jooste, C. Pandav, K. Caldwell,
R. Raghavan, et al., Biomarkers of nutrition for development–iodine
review, J. Nutr. 144 (8) (2014) 1322S–1342S, https://doi.org/
10.3945/jn.113.181974.
[26] Z. Mei, S.M. Namaste, M. Serdula, P.S. Suchdev, F. Rohner, R. Flores-
Ayala, et al., Adjusting total body iron for inflammation: Biomarkers
Reflecting Inflammation and Nutritional Determinants of Anemia
(BRINDA) project, Am. J. Clin. Nutr. 106 (suppl 1) (2017) 383S–389S,
https://doi.org/10.3945/ajcn.116.142307.
[27] S.M. Namaste, F. Rohner, J. Huang, N.L. Bhushan, R. Flores-Ayala,
R. Kupka, et al., Adjusting ferritin concentrations for inflammation:
Biomarkers Reflecting Inflammation and Nutritional Determinants of
Anemia (BRINDA) project, Am. J. Clin. Nutr. 106 (suppl 1) (2017)
359S–371S, https://doi.org/10.3945/ajcn.116.141762.