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https://doi.org/10.1007/s00394-018-1759-1
ORIGINAL CONTRIBUTION
Received: 6 March 2018 / Accepted: 20 June 2018 / Published online: 23 June 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Purpose Teff, an iron-rich staple grain in Ethiopia, is consumed mainly in the form of teff injera (TI). Studies on the associa-
tion of TI consumption with anemia are limited. We aimed to determine the association of frequencies of TI consumption
with anemia, in Addis Ababa, Ethiopia.
Methods We conducted a hospital-based case–control study involving 592 pregnant women: 187 anemic cases, and 405
non-anemic controls. TI consumption was assessed by a food frequency questionnaire (FFQ). Multiple logistic regression,
adjusted for dietary and non-dietary covariates, was performed to determine the relation of TI consumption to anemia status.
Results We found that a decrease in frequency of TI consumption was significantly associated with an increase in the like-
lihood of anemia (p-trend = 0.009). Compared with everyday TI consumption, the adjusted odds ratios (AORs) of anemia
associated with the other frequencies of teff consumption were 1.50 [95% confidence interval (CI) 0.71, 3.23; p = 0.285] for
every other day, 2.13 (95% CI 1.03, 4.41; p = 0.04) for 1–2 times a week, and 3.17 (95% CI 1.62, 6.22; p < 0.001) for once
in 2 weeks.
Conclusions Teff consumption was associated with reduced odds of anemia in pregnant women. Further studies are war-
ranted, including determining the feasibility and effectiveness of TI use for anemia prevention.
Registration The study was registered as https://clinicaltrials.gov/ct2/show/NCT03251664.
* Ahmad Esmaillzadeh
a‑esmaillzadeh@tums.ac.ir Introduction
1
Department of Community Nutrition, School of Nutritional Anemia remains among the major threats to the health and
Sciences and Dietetics, Tehran University of Medical
Sciences-International Campus (TUMS-IC), Tehran, Iran survival of pregnant women across many regions of the
2 world [1]. Progress in the reduction of anemia in pregnant
Unit of Reproductive Health, Addis Ababa City
Administration Health Bureau, Addis Ababa, Ethiopia women has been less promising over the last three decades
3 [1], with an estimated 40.6% prevalence of anemia among
Department of Public Health, Wollo University, Dessie,
Ethiopia pregnant women worldwide in the year 2016. The figure
4 was 43.4% in 1990 [2]. Anemia during pregnancy is a sig-
Endocrinology and Metabolism Research Center,
Endocrinology and Metabolism Clinical Sciences Institute, nificant contributing factor to maternal mortality and poor
Tehran University of Medical Sciences, Tehran, Iran fetal outcomes [1, 3, 4]. Prevention and timely treatment of
5
Obesity and Eating Habits Research Center, Endocrinology anemia in pregnant women is a priority public health agenda
and Metabolism Molecular Cellular Sciences Institute, in Ethiopia, where the maternal mortality rate and anemia
Tehran University of Medical Sciences, Tehran, Iran during pregnancy were estimated to be 412 per 100,000 live
6
Department of Community Nutrition, School of Nutritional births and 23%, respectively, in the year 2016 [5].
Sciences and Dietetics, Tehran University of Medical Pregnant women are at a higher risk of developing ane-
Sciences, Tehran, Iran mia, due to various dietary and non-dietary risk factors.
7
Department of Community Nutrition, Food Security The increased physiological demand for nutrients during
Research Center, Isfahan University of Medical Sciences, pregnancy also makes them more vulnerable to anemia.
Isfahan, Iran
13
Vol.:(0123456789)
2012 European Journal of Nutrition (2019) 58:2011–2018
13
European Journal of Nutrition (2019) 58:2011–2018 2013
Exposure assessment variables, and linearity of the relationship between the inde-
pendent variables and the logit transformation of anemia.
Data collection was conducted by trained data collectors, Bivariable analyses were conducted using independent t test
together with the midwives or nurses of the participating for continuous variables and Chi-square test for categori-
health facilities. The main exposure of interest was the cal variables. The bivariable tests were done to identify the
frequency of TI consumption in the year before the study. potential covariates (confounders) which might affect the
‘Injera’ can be prepared from various grains or a mixture association of the variables of interest (TI and anemia).
of grains. In this work, we were particularly interested Sociodemographic, disease, or dietary factors which dem-
in injera made of mainly teff flour (> 50% teff content), onstrated p values ≤ 0.20 during bivariable analyses, were
referred to in this document as TI. Moreover, a compre- considered as potential confounders, such that the final
hensive assessment of anemia determinants was performed multiple logistic regression analysis was adjusted for these
using a pre-tested questionnaire that was adapted from the factors. Interaction of teff with other food items of known
Ethiopian Demographic and Health Survey [5] as well anemia influence was also checked, with the aim of provid-
as the World Food and Agriculture Organization (FAO) ing estimates by subgroups if interaction was found. Where
dietary assessment [21] tools. Data were collected on no adequate evidence of interaction was observed, only main
the sociodemographic, anthropometric, dietary, hygiene, variables were entered in the multiple regression model.
reproductive, and health condition of the study partici-
pants. Weight, height, and mid-upper arm circumference
(MUAC) were measured following the standard procedures
[22]. Stool and blood samples were taken for laboratory Results
examination, the former for intestinal parasites and the
later for Human Immunodeficiency Virus (HIV) and Hb. Characteristics of study participants
Dietary practice was assessed by a food frequency ques-
tionnaire (FFQ), using the FAO women dietary diversity Table 1 presents the sociodemographic, anthropometric, and
scoring (WDDS) tool. The WDDS is a simplified tool health characteristics of study participants, disaggregated
designed for a rapid assessment of micronutrient intake by cases and controls. In total, 592 pregnant women were
adequacy. The tool has been widely used by previous stud- included; 187 anemic cases and 405 non-anemic controls.
ies in Ethiopia as well as validated in similar setups as a There were significant discrepancies between cases and con-
proxy measure of micronutrient intake [21, 23]. The FAO trols by education level, household income, MUAC, and ges-
WDDS tool categorizes food items into nine groups, namely tational age. Controls were more educated than cases (mean
(1) cereals, roots, and tubers; (2) legumes and nuts; (3) meat, education: 11 and 9 years among controls and cases, respec-
poultry, and fish; (4) vitamin A-rich fruits and vegetables; tively, p < 0.001). The mean monthly household income (in
(5) other vitamin A-rich fruits and vegetables; (6) other fruit Ethiopian Birr) of cases was 2966, whereas that of control
and vegetables; (7) dairy; (8) fats and oils; and (9) eggs. was 3159 (p < 0.001). The mean MUAC (cm) of cases was
Participants were asked to recall the usual frequency of con- lower than that of controls (23.6 vs. 24.3, p < 0.001). A
sumption of those food groups, including TI, over the last greater proportion of cases (42.2%) than controls (23.2%)
one year before the date of data collection. were in the first trimester of gestation; whereas a greater
proportion of controls (38.3%) than cases (10.7%) were in
Statistical analysis the second trimester. There were no significant differences
between cases and controls concerning age, height, weight,
Data entry and cleaning was achieved using Epi Info™ Pro- religion, occupation, household size, hygiene practice, gra-
gram version 3.4 (Center for Disease Control and Preven- vidity, pregnancy interval, HIV status, chronic illness, iron
tion, Atlanta, Georgia, United States). Statistical analysis supplement use, or intestinal parasites.
was conducted using Statistical Package for the Social Sci- Table 2 presents comparisons of the frequency of con-
ences (SPSS) Version 23 (IBM Corporation, New York, sumption of food groups between cases and controls. A
United States), with significance determined at a two-tailed higher proportion of anemic cases ate TI less frequently
p value < 0.05. Adjusted odds ratios (AORs), with 95% CI, than controls (teff consumption once per 2 weeks: 41.7%
are reported on the association of frequency of TI consump- cases vs. 20.5% controls), whereas a greater proportion of
tion with anemia. controls ate teff more frequently than cases (everyday teff
Before performing bivariable and multivariable analy- consumption: 38.5% controls vs. 20.3% cases). Consump-
ses, relevant statistical assumptions were checked, includ- tions of dark green leafy vegetables and meat were also
ing normality test for continuous variables, homogeneity of less frequent among cases compared to controls (p < 0.05).
variance, multicollinearity among continuous independent There was no evidence of a significant difference (p > 0.05)
13
2014 European Journal of Nutrition (2019) 58:2011–2018
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European Journal of Nutrition (2019) 58:2011–2018 2015
Teff injera
Every day 38 (20.3) 156 (38.5) < 0.001 between cases and controls concerning the consumption of
Every other day 29 (15.4) 86 (21.2) the other food groups shown in the table.
1–2 times a week 42 (22.5) 80 (19.8) To examine whether eating TI was independently associ-
Once per 2 weeks 78 (41.7) 83 (20.5) ated with anemia, we calculated AORs for the association of
Cereal grainsb frequencies of TI consumption with anemia. The adjustment
Every day 187 (100) 405 (100) NAc was done for both dietary and non-dietary covariates, namely
Meat educational status, household income, MUAC, and con-
Every day 17 (9.1) 75 (18.5) < 0.001 sumption of meat and dark green leafy vegetables. Results
Every other day 34 (18.2) 132 (32.6) are shown in Table 3. Overall, a decrease in the frequency of
1–2 times a week 54 (28.9) 161 (39.8)
TI consumption demonstrated a significant association with
Once per 2 weeks 82 (43.9) 37 (9.1)
an increase in anemia likelihood (p for trend = 0.009). Com-
Legumes
pared to the most frequent category (everyday TI consump-
Every day 187 (100) 405 (100) NA
tion), the odds of anemia associated with the least frequent
Dark green leafy vegetables
Every day 15 (8) 57 (14.1) < 0.001
category (once every 2 weeks) were 3.17 times higher (95%
Every other day 28 (15) 117 (28.9) CI 1.62, 6.22; p < 0.001). The AORs for the other catego-
1–2 times a week 45 (24.1) 195 (48.1) ries of TI consumption, compared to everyday consumption,
Once per 2 weeks 99 (52.9) 36 (8.9) were 2.13 (95% CI 1.03, 4.41; p = 0.04) for 1–2 times in
Vitamin A-rich fruits and vegetables a week, and 1.50 (95% CI 0.71, 3.23; p = 0.285) for every
Every day 12 (6.4) 18 (4.4) 0.511 other day.
Every other day 25 (13.4) 70 (17.3)
1–2 times a week 113 (60.4) 236 (58.3)
Once per 2 weeks 37 (19.8) 81 (20.0) Discussion
Other vitamin A-rich fruits and vegetables
Every day 23 (12.3) 36 (8.9) 0.322 The consumption of teff, in the form of TI, has been prac-
Every other day 40 (21.4) 102 (25.2)
ticed for a long time in Ethiopia and parts of Eritrea. Teff is
1–2 times a week 124 (66.3) 267 (65.9)
the primary staple grain, particularly in central and north-
Other fruits and vegetables
ern Ethiopia where it is widely harvested [10, 12]. Teff is
Every day 31 (16.6) 65 (16.0) 0.338
also widely consumed in urban areas across all regions of
Every other day 83 (44.4) 154 (38.0)
1–2 times a week 53 (28.3) 125 (30.9)
Ethiopia. Provided teff has high iron content [10, 13, 24], it
Once per 2 weeks 20 (10.7) 61 (15.1) could be presumed that teff consumption reduces the risk of
Eggs anemia. However, studies on the relation of frequencies of
Every day 27 (14.4) 68 (16.8) 0.355 TI consumption to hemoglobin status are limited. The exist-
Every other day 70 (37.4) 137 (33.8) ing evidence on the relation of teff consumption to anemia
1–2 times a week 71 (38.0) 172 (42.5) in Ethiopia is largely based on nutrient content analysis and
Once per 2 weeks 19 (10.2) 28 (6.9) biochemical studies. In this study, we examined the associa-
Dairy tion of different frequencies of TI consumption with anemia
Every day 35 (18.7) 77 (19.0) 0.479 and found that TI consumption was independently associated
Every other day 65 (34.8) 124 (30.6) with anemia; i.e., eating TI more frequently was associated
1–2 times a week 79 (42.2) 193 (47.7) with a significant reduction in the odds of anemia.
Once per 2 weeks 8 (4.3) 11 (2.7)
The finding of our study is in agreement with our hypoth-
Coffee/tea
esis that TI would be associated with reduced odds of ane-
No 54 (28.9) 126 (31.1) 0.512
mia. A study in southern Ethiopia [17] also reported a simi-
Yes 120 (64.2) 242 (59.8)
lar finding that pregnant women who ate teff-based food
Not using 13 (7.0) 37 (9.1)
products more frequently had lower odds of anemia. Two
NA not applicable studies conducted in the UK also reported that teff-based
a
Chi-square test was used to determine the differences between cases food products improved Hb and body iron levels [18, 19].
and controls Furthermore, the findings are in concordance with the nutri-
b
Includes all cereal grains includes bread or injera made of wheat, tional composition of teff, which contains a higher amount
sorghum, corn, rice or mixture of grains
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2016 European Journal of Nutrition (2019) 58:2011–2018
OR odds ratio, CI confidence interval, DGLV dark green leafy vegetables, MUAC mid-upper arm circum-
ference
a
Multiple logistic regression used to determine statistical significance
b
Variables are adjusted for each other
c
Ethiopian currency
d
No evidence of interaction and removed from the multivariable model
of iron than any other cereal grain [10, 13]. Prone to vary undernutrition [28, 29], one could presume a high burden of
by growing conditions, the average iron contents of different anemia among pregnant women. However, over the past five
teff varieties (mg/100 gm) are white teff (9.5–37.7), red teff decades, anemia prevalence among Ethiopian women has
(> 11.6), and mixed teff (> 11.5); these are greater amounts been consistently lower than the global and African averages
compared to the iron content of 100 gm maize (3.6–4.8), sor- [1, 2, 30], even lower than the figures for most of the devel-
ghum (3.5–4.1), wheat (3.7), and rice (1.5) [13]. Like other oped nations [1, 2]. Besides, recent studies have shown that
cereal grains, teff also contains high phytate content [13, the burden of IDA is generally low in Ethiopia [16, 30, 31].
24], which may impair iron absorption by forming insolu- Based on the existing evidence, including the findings of our
ble phytate–mineral or peptide–mineral–phytate complexes study, it could be inferred that the low prevalence of anemia
in the gastrointestinal tract [24, 25]. However, previous among women in Ethiopia might be partly attributable to
studies showed that the phytate in teff would be degraded the consumption of TI, solely of Ethiopians and Eritreans.
significantly during the preparation of TI, which involves a However, this proposition should be confirmed by further
rigorous fermentation process. Before making TI, the teff studies as genetic factors unique to Ethiopians were also
dough is fermented for 2–3 days [12, 26]. The fermentation linked to Hb status [32, 33].
of grains was shown to degrade phytate by activating endog- Our finding bears some policy implications. Given
enous phytases [26, 27]. the importance of dietary diversity in combating anemia,
It would be important to relate our result to the con- exploring teff as an alternative food for the prevention
text of anemia epidemiology in Ethiopia. Provided that of anemia would represent an important consideration.
Ethiopia bears a high level of food insecurity and chronic Pregnant women may benefit more from eating teff, as
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European Journal of Nutrition (2019) 58:2011–2018 2017
they are at higher risk of anemia and teff may avoid the Conclusions
problem of intolerance associated with the intake of iron
tablets. Existing dietary and micronutrient assessment In conclusion, this study aimed to determine the associa-
tools, particularly those in use in Ethiopia, may need to tion of various levels of TI consumption with anemia in
be revised or customized in line with the local dietary pregnant Ethiopian women. We found that more frequent
practice. It may also be useful to consider incorporating consumption of TI was significantly associated with a lower
teff into the list of iron-rich food items. The commonly likelihood of anemia. Teff consumption may be a contribut-
used dietary assessment tools in Ethiopia [5, 21] incor- ing factor to the low level of anemia in Ethiopian women.
porate teff into the group ‘cereals, roots, and tubers’. This To make a more definitive conclusion, further randomized
approach could be problematic because teff differs nutri- controlled trials or cohort studies, with better exposure and
tionally from other cereal grains, at least in terms of being outcome assessment, are warranted. The feasibility of TI as
gluten-free and rich in iron. an alternative food for the prevention of anemia needs to be
The main strength of this study was that it was based further explored.
on human subjects, unlike many of the previous studies
which focused on assessing teff’s nutrient contents and Acknowledgements SHM is a recipient of postgraduate scholarship,
chemical properties. Our findings provide insight on the Tehran University of Medical Sciences-International Campus. We are
also grateful for the study participants, data collectors, and hospital
extent of the association of frequencies of TI consump- staff involved in the study.
tion with anemia, which may serve as evidence for further
studies on the suitability of teff as an option for anemia Author contributions SHM, HT, and AE designed the study; HKT
prevention. The comprehensive assessment of anemia coordinated the data collection; SHM and AE conducted the statis-
determinants enabled adjustment for various dietary and tical analysis and wrote the manuscript. SHM, HKT, and TAS took
part in the interpretation of findings; AE and BL critically reviewed
non-dietary factors, thereby minimizing the possibility the manuscript. All authors read and approved the final version of the
that the observed association could be due to confound- manuscript.
ing factors. The study also has many limitations worth
noting to the reader. First, we did not take into account Compliance with ethical standards
differences in teff varieties and growing conditions. The
amount of iron in TI varies by the type of the teff grain Conflict of interest The authors declared no conflict of interest.
used to make it [24]; thus, the extent of TI-anemia asso-
Ethical standards Ethical clearance was obtained from the institutional
ciation may change according to the type of teff eaten. review boards of the University of Gondar and the Addis Ababa City
Second, in this study, TI made of mainly teff flour (> 50% Health Bureau (AAHB-217/15). Permission to conduct the study was
teff) was assessed. However, other forms of injera with also obtained from the participating health facilities. Signed informed
smaller proportions of teff, such as ‘mixed injera’, need consent was obtained from the study subjects before data collection.
We did not include personally identifiable information in the dataset.
to be investigated in future studies. Third, the use of hos- Blood and stool samples were collected for the health facilities’ own
pital-based cases and controls, and only pregnant women, use; thus, we did not hold any biological specimen. Data collectors
would limit the generalizability of the study. Fourth, the advised anemic cases on dietary management of anemia and the impor-
study involved only public health facilities. Teff has tance of further medical care. Refer to this study’s registration status
through its ClinicalTrials.gov identifier (NCT number: NCT03251664)
become an expensive commodity, and individuals going available on https://clinicaltrials.gov/ct2/show/NCT03251664.
to public health facilities tend to be of low socioeconomic
status. Thus, the level of consumption reported by our
study might be lower than the level in the general popu-
lation and resulted in biased estimates. Population-based
studies will have better generalizability. Fifth, due to the References
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