Case-control study of anaemia among middle-aged and elderly women in three rural areas of China


Song, P.; Li, L.; Man, Q.; Wang, C.; Meng, L.; Zhang, J.

BMJ Open 4(8): E004751

2015


To propose a feasible suggestion to reduce the high prevalence of anaemia in middle-aged and elderly women by investigating risk factors, particularly nutritional factors, and analysing the effect on anaemia in three different rural areas of China. A case-control study. Three counties of China. Women aged 50-75 years in the three counties. Adjusted OR (95% CI) of anaemia associated with diet, lifestyle and blood biochemical indices. Compared with controls, women with anaemia had lower body mass index (22.1 (3.2) kg/m(2) vs 23.2 (3.5) kg/m(2); p<0.001), a higher experience of shortage of food (45.0% vs 36.5%; p<0.001), less soy food intake (0.5 (0.3, 26.7) g/day vs 5.6 (0.4, 27.8) g/day; p<0.048), lower serum iron (13.4 (5.4) μmol/L vs 16.4 (5.7) μmol/L; p<0.001), lower ferritin (109.6 (85.6) ng/mL vs 131.0 (92.0) ng/mL; p<0.001), lower transferrin saturation levels (22.5 (9.5)% vs 26.8 (9.6)%; p<0.001) and higher levels of free erythrocyte protoporphyrin (42.4 (21.2) μg/dL vs 39.6 (17.8) μg/dL; p<0.001). Anaemia was significantly associated with BMI(OR=0.90, 95% CI (0.87 to 0.92)), food shortage experience (OR=1.39, 95% CI (1.15 to 1.69)), total protein (OR=0.66, 95%CI (0.54 to 0.80)), Albumin (OR=0.72, 95%CI (0.59 to 0.87)) in univariate analysis. Multivariate analysis showed that body mass index, experience of food shortage, total protein and albumin were independently related to anaemia. Among middle-aged and elderly women in rural China, the nutrition status of anaemic cases is far below that of controls. Lower body mass index and a greater experience of food shortage are closely related to anaemia. Improving the blood protein status by consuming protein-sufficient foods such as soy food is a feasible approach for elderly anaemic women. Further research is needed on the effect of chronic inflammation and infectious disease on anaemia in elderly women in rural China.

Strengths
and
limitations
of
this
study
The
main
strength
of
the
study
is
the
detailed
analysis
of
the
nutritional
status
of
elderly
women
in
rural
China.
The
main
limitation
was
the
difficulty
to
exclude
anaemia
caused
by
chronic
diseases
and
the
recall
bias
was
inevitable
in
the
observation
nature
of
the
study.
No
sufficient
evidence
to
support
our
claim
that
eating
habits
and
physical
exercises
were
stable
over
time.
Some
continuous
variables
were
categorized
for
analysis
to
increase
the
possibility
of
residual
confounding
and
decrease
the
precision
and
power
of
the
study.
Open
Access
Research
BMJ
Open
Case-control
study
of
anaemia
among
middle-aged
and
elderly
women
in
three
rural
areas
of
China
Pengkun
Song,
Lixiang
Li,
Qingqing
Man,
Chunrong
Wang,
Liping
Meng,
Jian
Zhang
CrossMark
ABSTRACT
Objectives:
To
propose
a
feasible
suggestion
to
reduce
the
high
prevalence
of
anaemia
in
middle-aged
and
elderly
women
by
investigating
risk
factors,
particularly
nutritional
factors,
and
analysing
the
effect
on
anaemia
in
three
different
rural
areas
of
China.
Design:
A
case-control
study.
Setting:
Three
counties
of
China.
Participants:
Women
aged
50-75
years
in
the
three
counties.
Main
outcome
measures:
Adjusted
OR
(95%
CI)
of
anaemia
associated
with
diet,
lifestyle
and
blood
biochemical
indices.
Results:
Compared
with
controls,
women
with
anaemia
had
lower
body
mass
index
(22.1
(3.2)
kg/m
2
vs
23.2
(3.5)
kg/m
2
;
p<0.001),
a
higher
experience
of
shortage
of
food
(45.0%
vs
36.5%;
p<0.001),
less
soy
food
intake
(0.5
(0.3,
26.7)
g/day
vs
5.6
(0.4,
27.8)
g/day;
p<0.048),
lower
serum
iron
(13.4
(5.4)
µmol/L
vs
16.4
(5.7)
µmol/
L;
p<0.001),
lower
ferritin
(109.6
(85.6)
ng/mL
vs
131.0
(92.0)
ng/mL;
p<0.001),
lower
transferrin
saturation
levels
(22.5
(9.5)%
vs
26.8
(9.6)%;
p<0.001)
and
higher
levels
of
free
erythrocyte
protoporphyrin
(42.4
(21.2)
Rg/dL
vs
39.6
(17.8)
lig/dL;
p<0.001).
Anaemia
was
significantly
associated
with
BMI(OR=0.90,
95%
CI
(0.87
to
0.92)),
food
shortage
experience
(OR=1.39,
95%
CI
(1.15
to
1.69)),
total
protein
(OR=0.66,
95°/0CI
(0.54
to
0.80)),
Albumin
(OR=0.72,
95°/0C1
(0.59
to
0.87))
in
univariate
analysis.
Multivariate
analysis
showed
that
body
mass
index,
experience
of
food
shortage,
total
protein
and
albumin
were
independently
related
to
anaemia.
Conclusions:
Among
middle-aged
and
elderly
women
in
rural
China,
the
nutrition
status
of
anaemic
cases
is
far
below
that
of
controls.
Lower
body
mass
index
and
a
greater
experience
of
food
shortage
are
closely
related
to
anaemia.
Improving
the
blood
protein
status
by
consuming
protein-sufficient
foods
such
as
soy
food
is
a
feasible
approach
for
elderly
anaemic
women.
Further
research
is
needed
on
the
effect
of
chronic
inflammation
and
infectious
disease
on
anaemia
in
elderly
women
in
rural
China.
INTRODUCTION
Anaemia
affects
about
one-quarter
of
the
world's
population,
especially
pregnant
women,
young
children
and
elderly
people.
1
In
America,
10.2%
of
women
aged
65
and
older
are
anaemic.
2
The
prevalence
among
independent
community-dwelling
persons
is
more
than
20%
and
among
hospitalised
geri-
atric
patients
the
rate
is
up
to
40%.
3
In
China
the
results
of
several
surveys
indicate
that
the
prevalence
of
anaemia
in
elderly
people
is
20-39%,
reaching
60%
in
some
very
poor
rural
areas.
4
In
recent
years,
with
the
rapid
development
of
the
economy,
there
have
been
remarkable
changes
in
dietary
patterns
and
lifestyle
in
China,
particularly
in
urban
regions.
With
the
improvement
in
living
standards,
the
rate
of
malnutrition
in
elderly
people
has
decreased
significantly.
However,
the
problem
of
under-
nutrition
such
as
anaemia
is
still
very
severe
among
elderly
people
in
rural
areas.
Data
from
the
2002
China
National
Nutrition
and
Health
Survey
(CNNHS)
indicated
that
the
prevalence
of
anaemia
in
women
aged
60
years
and
older
in
rural
areas
was
almost
1.5
times
that
of
urban
women
of
the
same
age
group.
Compared
with
data
from
the
1992
National
Nutrition
Survey,
the
reduction
in
the
preva-
lence
of
anaemia
in
elderly
urban
women
reached
33.6%
while,
for
elderly
women
in
To
cite:
Song
P,
Li
L,
Man
Q,
et
aL
Case-control
study
of
anaemia
among
middle-aged
and
elderly
women
in
three
rural
areas
of
China.
BMJ
Open
2014;4:e004751.
do1:10.1136/bmjopen-2013-
004751
Prepublication
history
for
this
paper
is
available
online.
To
view
these
files
please
visit
the
journal
online
(http://dx.dolorg/10.1136/
bmjopen-2013-004751).
Received
31
December
2013
Revised
7
July
2014
Accepted
21
July
2014
Elderly
and
Clinical
Nutrition
Laboratory,
Institute
of
Nutrition
and
Food
Safety,
Chinese
Center
for
Disease
Control
and
Prevention,
Beijing,
China
Correspondence
to
Professor
Jian
Zhang;
zhjian6708@aliyun.com
BMJ
Song
P,
et
at
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjopen-2013-004751
1
Open
Access
3
rural
areas,
the
reduction
was
just
4.8%.
It
is
therefore
important
to
investigate
the
risk
factors
for
anaemia
in
elderly
women
in
rural
areas
of
China
and
to
provide
sug-
gestions
for
improving
the
health
status
of
this
population.
Elderly
people
are
more
prone
to
becoming
anaemic,
5
which
adversely
affects
muscle
strength,
8
phys-
ical
performance,
7
cognition
8
and
longevity
9
and
thus
adds
an
economic
burden
on
society.
The
physiological
and
metabolic
characteristics
of
elderly
people
are
quite
different
from
other
populations.
In
elderly
people
the
metabolic
rate
slows
down
and
they
are
more
vulnerable
to
environmental
deficiencies
and
recovery
becomes
more
difficult.
The
causes
are
complicated,
particularly
those
involving
blood
loss
caused
by
some
chronic
dis-
eases.
However,
some
studies
have
shown
that
anaemia
in
elderly
people
is
also
closely
related
to
nutritional
status,"
especially
iron-deficient
anaemia
(IDA).
We
pro-
posed
that,
among
all
the
reasons,
malnutrition—low
bioavailability
of
iron
caused
by
a
poor
quality
diet
(simple
foods
composed
particularly
of
low
animal
or
soy
food
consumption)—may
be
the
main
reason
for
anaemia
in
elderly
women
living
in
most
rural
areas
of
China.
We
undertook
a
case-control
study
to
investigate
the
nutritional
causes
of
anaemia
in
elderly
women.
It
is
hoped
that
the
results
will
promote
an
increasing
cap-
acity
for
elderly
individuals
and
communities
to
prevent
anaemia
and
provide
useful
experience
for
making
recommendations
for
this
high-risk
population.
METHODS
Study
populations
and
sample
collection
Women
aged
50-75
years
were
selected
from
three
rep-
resentative
rural
areas
of
China
according
to
the
2002
CNNHS.
11
The
three
rural
areas
were
Qidong,
Jiangsu
Province
(East
China),
Huangling,
Shaanxi
Province
(Northwest
China)
and
Xiuning,
Anhui
Province
(Middle
China).
In
each
county
surveyed
the
selection
process
included
two
steps.
In
the
first
stage,
the
basic
personal
health
survey,
which
included
questions
about
demographic
characteristics,
disease
history,
smoking,
drinking,
physical
activity
and
sleeping,
was
undertaken
among
all
volunteers
aged
50-75
years.
In
addition,
finger
blood
haemoglobin
concentration
was
measured
in
all
volunteers.
Women
with
serious
diseases
were
excluded
according
to
the
exclusion
criteria.
Women
with
haemoglobin
levels
of
90-120
g/L
were
selected
as
subjects
in
the
case
group
and
those
with
haemoglobin
levels
>130
g/L
were
recruited
to
the
control
group.
The
subjects
in
the
two
groups
were
matched
for
age.
In
the
second
stage,
after
a
10-14
h
fast,
venous
blood
samples
were
collected
in
the
morning
and
question-
naires
on
diet,
life
style,
medical
history
and
physical
activity
were
completed.
Food
and
nutrient
intake
was
calculated
based
on
consecutive
individual
three-day
food
records.
In
order
to
evaluate
the
whole
diet
quality
we
calculated
the
dietary
balance
index
(DBI).
12
Anthropometric
measurements
including
height,
weight
and
waist
circumference
were
measured
at
the
working
site.
Height
was
measured
to
the
nearest
centimetre
without
shoes,
weight
was
measured
to
the
nearest
0.1
kg
in
light
clothing
and
waist
circumference
was
measured
midway
between
the
lower
rib
margin
and
the
superior
anterior
iliac
spine
to
the
nearest
0.5
cm
with
a
non-
stretching
tape
applied
horizontally."
Body
mass
index
(BMI)
was
calculated.
The
study
was
approved
by
the
Ethics
Committee
of
the
National
Institute
of
Nutrition
and
Food
Safety,
Chinese
Center
for
Disease
Control
and
Prevention
and
all
the
women
voluntarily
joined
the
study
with
informed
consent.
Clinical
and
biomarker
measurements
Several
indicators
such
as
haemoglobin,
serum
iron
(SI)
and
ferritin
(FER)
have
been
used
as
clinical
parameters
that
reflect
iron
metabolism
status.
14
The
ferrozine
method
was
used
to
measure
SI
and
unsaturated
iron
binding
capacity
(UIBC)
and
immunonephelometry
was
used
to
detect
FER,
transferrin
(TF)
and
C-reactive
protein
levels.
Free
erythrocyte
protoporphyrin
(FEP)
was
measured
by
haematofluorometry.
Total
iron
binding
cap-
acity
(TIBC)
and
transferrin
saturation
(TS)
were
calcu-
lated
from
SI
and
UIBC
(TIBC=SI+UIBC,
TS=SI/TIBC).
Statistical
analysis
All
data
were
collected
by
Epidata
3.02
and
data
analysis
was
performed
by
SAS
for
Windows
V.9.1.3
(SAS
Institute,
Cary,
North
Carolina,
USA).
Descriptive
statis-
tics
for
variables
were
used
with
tables,
means
and
SDs.
Median
(lower
quartile,
upper
quartile)
values
were
used
to
characterise
the
diet
and
non-normal
distribu-
tion
variables.
In
the
data
analysis
we
used
the
t
test
for
continuous
variables
with
normal
distribution
while,
for
nominal
(categorical)
variables,
we
used
non-parametric
tests
such
as
the
x
2
test,
Fisher
exact
test
or
median
two-sample
test;
p
values
<0.5
were
considered
to
be
stat-
istically
significant.
OR
and
95%
CIs
for
anaemia
were
calculated
by
univariate
regression
and
multivariate
logistic
regression
after
adjustment
for
possible
confoun-
ders
(age,
education
level,
physical
activity
time,
income,
monthly
expenditure
on
food
and
region).
RESULTS
The
number
of
women
who
underwent
haemoglobin
testing
in
Huangling,
Qidong
and
Xiuning
was
2740,
2088
and
862,
respectively
and,
according
to
the
criteria,
572,
472
and
243
women
from
the
three
areas
were
diagnosed
with
anaemia.
Women
with
serious
diseases
and
those
refused
to
participate
in
the
project
were
excluded.
The
final
subjects
of
cases
and
controls
were
1004
and
1025
respectively
with
complete
questionnaire
and
blood
char-
acters
test
by
consideration
of
age
and
living
places
match.
Table
1
showed
the
mean
age
of
the
control
and
case
groups
was
comparable
(60.8
years
vs
61
years).
The
pro-
portion
of
people
with
primary
school
education
and
below
was
86.4%
in
the
case
group
and
86.5%
in
the
2
Song
P,
et
al.
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjapen-2013-004751
0
Open
Access
Table
1
General
information
of
cases
and
controls
Variables
Cases
(n=1004)
Controls
(n=1025)
p
Value
60.8
(7.4)
887
(86.5)
500
(0,
2000)
100
(50,
150)
374
(36.5)
10.0
(2.7)
Age
(years)
61.0
(7.8)
Educational
level"
(n,
%)
867
(86.4)
Annual
incomet
(Yuan,
RMB)
300
(0,
2000)
Monthly
expenditure
on
food
(Yuan,
RMB)
100
(50,
150)
Food
shortage
experience,'
(n,
%)
452
(45.0)
Physical
activity
time
(h/day)
9.9
(2.8)
*Educational
level
at
primary
school
level
and
below.
tp
Value
by
Mantel-Haenszel
x
2
test.
*The
remaining
money
except
for
basic
living
expenditure,
including
money
from
their
sons
or
daughter.
§p
Value
by
median
two-sample
test.
11Exposure
to
the
Chinese
famine
(1959-1961)
during
childhood.
0.539
0.9571
-
0.150§
0.797§
<0.001t
0.315
control
group.
The
annual
income
in
the
control
group
was
500
Yuan
(RMB),
which
was
higher
than
that
of
cases
but
the
difference
was
not
statistically
significant.
Monthly
expenditure
on
food
was
about
100
Yuan
(RMB)
in
both
groups.
The
proportion
who
experienced
food
shortage
during
childhood
in
the
case
group
was
higher
than
in
the
control
group
(45.0%
vs
36.5%)
and
the
difference
was
statistically
significant
(
p<0.001).
The
anthropometric
measurements
were
shown
in
table
2.
The
average
height,
weight,
BMI
and
waist
cir-
cumference
of
the
case
group
were
all
significantly
lower
than
those
in
the
control
group
(
p<0.001).
According
to
the
cut-off
point
of
BMI
and
waist
circumference,
15
64.2%
of
cases
and
55.3%
of
controls
were
in
the
normal
range,
but
11.1%
of
cases
a
had
low
BMI,
signifi-
cantly
more
than
in
the
control
group
(
p<0.001).
With
regard
to
biomarkers,
anaemic
women
had
lower
serum
total
protein,
albumin,
SI,
FER
and
TS
levels
(
p<0.001),
while
FEP
and
FEP/Hb
ratio
in
anaemic
women
were
higher
than
that
in
controls
(
p<0.001).
There
was
no
difference
for
TF
and
TIBC
between
cases
and
controls
(table
3).
Table
2
Anthropometric
assessments
of
elderly
women
among
cases
and
controls
Anthropometric
measurements
Cases
(n=1004)
Controls
(n=1025)
p
Value
Height
(cm)
152.4
(6.2)
153.3
(5.9)
0.001
Weight
(kg)
51.4
(8.7)
54.6
(9.5)
<0.001
BMI
(kg/m
2
)
22.1
(3.2)
23.2
(3.5)
<0.001
Low
weight
(<18.5)
(n,
%)
111
(11.1)
80
(7.8)
<0.001
Normal
(18.5-23.9)
(n,
%)
644
(64.2)
567
(55.3)
Overweight
(24.0-27.9)
(n,
%)
201
(19.6)
283
(27.6)
Obesity
(28.0)
(n,
%)
48
(5.1)
95
(9.3)
Waist
circumference
(cm)
74.4
(8.6)
78.6
(9.2)
<0.001
Adequate
(<80.0)
(n,
%)
744
(74.1)
559
(54.5)
<0.001
Increased
(>80.0)
(n,
%)
260
(25.9)
466
(45.5)
BMI,
body
mass
index.
Table
3
Blood
indices
of
elderly
women
among
cases
and
controls
Biochemical
indices
Cases
(n=1004)
Controls
(n=1025)
p
Value
Haemoglobin
(g/L)
113.7
(6.8)
140.0
(8.8)
<0.001
Total
protein
(g/L)
79.3
(9.2)
81.0
(6.3)
<0.001
Albumin
(g/L)
48.1
(3.7)
49.4
(3.6)
<0.001
Serum
iron
(gmol/L)
13.4
(5.4) 16.4
(5.7)
<0.001
Ferritin
(µg/L)
109.6
(85.6)
131.0
(92.0)
<0.001
Transferrin
(g/L)
2.6
(0.5)
2.6
(0.4)
0.765
Free
erythrocyte
protoporphyrin
(µg/dL)
42.4
(21.2)
39.6
(17.8)
0.001
Total
iron
binding
capacity
(Rmol/L)
61.2
(11.4)
62.1
(10.1)
0.074
Transferrin
saturation
(%)
22.5
(9.5)
26.8
(9.6)
<0.001
C-reactive
protein
(mg/L)
6.9
(8.6)
7.9
(6.8)
0.007
FEP/Hb
ratio
(gg/g,
%)
3.8
(2.0)
2.8
(1.3)
<0.001
FEP,
free
erythrocyte
protoporphyrin.
Song
P,
et
aL
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjapen-2013-004751
3
0
Open
Access
Table
4
Food,
energy
and
iron
intake
in
cases
and
controls
(median
(lower quartile,
upper
quartile))
Food
and
nutrient
intake
Cases
(n=1004)
Controls
(n=1025)
p
Value*
Staple
food
-
I
-
(g)
155.6
(114.4,
320.8)
155.6
Animal
food$
(g)
22.2
(0,
50.8)
22.2
Soy
food§
(g)
0.5
(0.3,
26.7)
5.6
Vegetable
(g)
150.0
(50.8,
283.3)
150.0
Fruit
(g)
14.8
(4.9,
41.7)
15.0
Pure
energy
food,'
(g)
19.4
(13.9,
37.2)
18.0
DBI
_
LBS
49
(43,
53)
49
Total
energy
intake
(MJ)
7.5
(5.8,
9.0)
7.5
(111.1,
325.0)
(0,
55.6)
(0.4,
27.8)
(44.4,
281.7)
(5.5,
41.7)
(13.9,
33.3)
(43,
53)
(5.7,
9.1)
0.875
0.955
0.048
0.982
0.876
0.163
0.490
0.641
Protein
intake
(g)
46.1
(34.1,
60.8)
46.9
(34.0,
60.7)
0.387
Carbohydrate
intake
(g)
273.2
(208.6,
326.8)
274.8
(212.3,
333.1)
0.739
Fat
intake
(g)
54.0
(39.3,
68.4)
52.8
(38.1,
67.9)
0.412
Iron
intake
(mg)
17.0
(13.7,
22.6)
17.0
(13.4,
21.6)
0.982
*p
Value
by
median
two-sample
test.
"[Staple
food: containing
rice,
wheat
and
other
cereals,
potatoes.
*Animal
food:
containing
red
meats,
poultry,
fish,
eggs
and
milk.
§Soy
food:
dry
beans
and
bean
products
(ie,
tofu,
soymilk),
calculated
by
dry
soybean
weight.
liPure
energy
food:
containing
sugar,
alcohol
and
edible
oil.
DBI_LBS,
dietary
balance
index
of
lower
balance
score.
Differences
in
food
intake
and
main
nutrients
were
shown
in
table
4.
The
consumption
of
soy
food
in
women
with
anaemia
was
significantly
lower
than
in
the
control
group
(
p<0.05).
There
was
no
significant
differ-
ence
in
the
consumption
of
staple,
animal
food,
vege-
table,
fruit
and
pure
energy
food
between
the
two
groups.
Based
on
the
DBI
of
lower
balance
score
(DBI_LBS),
12
we
made
an
evaluation
of
diet
quality.
The
total
DBI_LBS
score
was
0-58,
which
was
divided
into
three
levels
(<20,
20-40,
>40).The
median
score
was
49
in
both
the
case
and
control
groups.
Three
regression
models
were
used
to
analyse
the
maximum
likelihood
ratio
(tables
5
and
6).
Model
3
was
optimal
from
the
statistical
and
professional
point
of
view.
Table
5
Models
for
anaemia
and
influencing
factors
by
logistic
regression
Testing
global
null
hypothesis:
j3=0
Model
-2
log
L
x
2
DF
p
Value
Model
1"
2329.12
483.45
29
<0.001
Model
21
-
2347.52
465.05
12
<0.001
Model
3$
2528.47
284.10
8
<0.001
Model
2534.98
277.60
6
<0.001
*Twenty-nine
parameters
in
model
1
were
all
variables
in
tables
1-4.
tEight
parameters
in
model
1
were
deleted
by
p>0.10:
age,
educational
level,
annual
income,
monthly
expenditure
on
food,
physical
activity
time,
vegetable,
fruit,
animal
food,
pure
energy
food,
protein
intake,
iron
intake,
DBI_LBS,
total
energy
intake,
carbohydrate
intake,
transferrin,
C-reactive
protein.
*Parameters
in
model
3
were
as
follows:
experience
of
food
shortage,
body
mass
index,
albumin,
total
protein,
ferritin,
transferrin
saturation,
FEP/Hb
ratio
and
soy
food
intake.
§Parameters
in
model
4
were
as
follows:
experience
of
food
shortage,
body
mass
index,
albumin,
total
protein,
transferrin
saturation,
FEP/Hb
ratio.
DBI_LBS,
dietary
balance
index
of
lower
balance
score;
FEP,
freeI
erythrocyte
protoporphyrin.
Table
7
showed
the
ORs
for
influencing
factors
and
anaemia
by
univariate
and
multivariate
logistic
regres-
sion
modelling.
After
controlling
for
confounding
vari-
ables,
BMI,
experience
of
food
shortage,
total
protein
and
albumin
were
independently
related
to
anaemia.
DISCUSSION
Anaemia
in
elderly
people
has
been
a
public
health
problem
for
decades
in
China
but,
in
comparison
with
the
significant
efforts
made
in
pregnant
women
and
children,
anaemia
in
elderly
people
has
received
less
attention.
To
our
knowledge,
this
case-control
project
is
the
first
study
to
investigate
the
possible
risk
of
anaemia
in
rural
elderly
women.
Through
the
general
health
survey,
diet
questionnaire,
anthropometric
measure-
ments
and
biochemical
analysis,
we
found
that
women
in
the
control
group
had
better
nutritional
status.
Although
both
cases
and
controls
had
low
food
intake
as
there
was
no
statistical
difference
in
DBI_LBS
between
the
two
groups,
the
average
intake
of
most
types
of
foods
in
the
controls
was
slightly
higher
than
in
the
cases.
It
may
be
that
the
long-term
small
difference
in
food
intake
could
contribute
to
the
significant
differ-
ence
in
biochemical
indices
and
anthropometric
measurements.
In
China,
elderly
women
play
a
very
important
role
in
family
life.
They
take
charge
of
much
of
the
housework
and
take
care
of
their
grandchildren,
but
they
have
a
low
income.
16
Elderly
women
seldom
concern
them-
selves
with
their
own
health
and
are
more
often
mal-
nourished.
Several
reports
have
shown
that
the
level
of
education
is
related
to
anaemia.
Women
with
a
higher
level
of
education
pay
more
attention
to
their
health
and
are
inclined
to
purchase
or
select
healthy
and
nutrient-rich
foods.
17
In
our
study,
since
the
survey
sites
were
located
in
poor
undeveloped
areas,
no
difference
4
Song
P,
et
al.
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjapen-2013-004751
0
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6
Parame
ter
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t
ima
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in
t
hree
mo
de
ls
BMI,
bo
dy
mass
in
dex;
SI,
serum
iron;
FEP,
free
ery
t
hrocy
te
p
ro
top
orp
hy
r
in;
TIB
C,
to
ta
l
iron
bin
ding
cap
ac
ity
;
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S,
trans
ferr
in
sa
tura
t
ion.
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ter
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O
EL
CO
L
u-
I
Open
Access
was
found
in
the
level
of
education
and
annual
income
between
cases
and
controls.
In
addition,
most
elderly
women
had
experienced
a
poor
malnutrition
status
in
the
country's
economic
difficulties
during
their
adoles-
cence
and
during
pregnancy.
In
our
study,
by
controlling
for
the
main
confounding
factors, multivariate
logistic
regression
showed
that
the
experience
of
food
shortage
was
closely
related
to
anaemia,
but
we
could
not
clarify
the
direct
effect
of
experiencing
food
shortage
on
anaemia.
It
may
be
that
women
who
had
experienced
shortage
of
food
were
more
likely
to
remain
frugal
and
to
maintain
an
economic
lifestyle.
If
they
maintained
this
living
habit
and
did
not
improve
their
living
stand-
ard,
particularly
with
regard
to
the
quality
of
their
diet,
it
would
be
difficult
to
improve
their
poor
health.
A
further
retrospective
cohort
study
nested
in
this
study
was
needed
to
show
the
relationship
between
anaemia
and
the
experience
of
food
shortage.
The
fat-free
body
weight
of
elderly
people
will
grad-
ually
reduce
with
ageing.
BMI,
an
indicator
which
reflects
fat-free
body
weight,
is
a
relatively
accurate
index
used
by
many
researchers.
Waist
circumference
is
much
more
valuable
for
evaluating
the
fatty
body
weight
com-
ponent
of
ageing.
18
In
this
study
we
found
that
BMI
was
lower
in
anaemic
women,
but
most
of
the
women
in
the
case
and
control
groups
were
in
the
normal
BMI
range
(18.5-24.0
kg/m
2
)
according
to
Chinese
criteria.
15
Our
results
showed
the
risk
trend
of
BMI
for
anaemia.
Logistic
regression
showed
that,
if
BMI
values
ranged
from
<18.5
to
18.5-23.9
kg/m
2
,
then
the
OR
ranged
from
1.00
to
0.84
accordingly.
The
higher
the
BMI,
the
lower
the
OR
value.
BMI
was
inversely
associated
with
anaemia.
Women
with
overweight/obesity
were
less
likely
to
be
anaemic
than
women
of
normal
weight.
More
work
is
needed
to
clarify
this
issue.
Many
studies
have
shown
that
diet
and
nutrition
are
related
to
anaemia.
Intervention
studies
to
improve
anaemia
by
iron
supplementation,
19
vitamin
B122°
or
folate
fortification
have
shown
them
to
be
efficacious
in
fighting
the
problem
in
this
at-risk
population
and
have
obtained
some
encouraging
results.
However,
some
studies
have
suggested
that
excessive
iron
stores pose
a
greater
health
risk
than
iron
deficiency
in
the
elderly
because
elevated
iron
stores
have
been
linked
to
chronic
diseases
such
as
cancer,
diabetes
and
heart
disease.
21
In
anaemia,
the
main
materials
for
haemoglobin
synthesis
are
iron
and
protein.
The
amino
acid
and
polypeptide
released
from
protein
could
integrate
with
non-heme
iron
and
form
a
soluble
and
absorbable
composite.
In
this
study
the
biochemical
indices
such
as
total
protein
and
albumin
levels
in
the
case
group
were
much
lower
than
in
the
controls,
which
indicates
that
the
protein
nutrition
status
of
anaemic
women
was
not
as
good
as
in
the
women
in
the
control
group.
Both
univariate
and
multivariate
regression
also
showed
that
blood
total
protein
and
albumin
were
significantly
associated
with
anaemia.
However,
there
was
inconsistent
information
between
the
protein
intake
calculated
from
the
three-
Song
P,
et
aL
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjapen-2013-004751
5
Open
Access
Table
7
Logistic
regression
model
to
analyse
the
influencing
factors
Variable
Univariate
regression
Multivariate
regression*
OR
95%
CI
p
Value
OR
95%
CI
p
Value
Experience
of
food
shortage
1.39
1.15
to
1.69
<0.001
1.66
1.26
to
2.19
<0.001
No
1.00
1.00
Yes
1.39
1.15
to
1.69
<0.001
1.66
1.26
to
2.19
<0.001
BMI,
kg/m
2
0.90
0.87
to
0.92
<0.001
0.89
0.87
to
0.92
<0.001
<18.5
1.00
1.00
18.5-23.9
0.84
0.60
to
1.18
<0.001
0.82
0.58
to
1.17
<0.001
23.9-27.9
0.46
0.31
to
0.67
0.006
0.44
0.30
to
0.65
0.005
>28.0
0.34
0.21
to
0.56
<0.001
0.33
0.20
to
0.55
<0.001
Soy
food
0.94
0.78
to
1.15
0.528
0.91
0.74
to
1.11
0.349
Q1
-
1
-
(0.5)
1.00
1.00
Q2
-
1
-
(2.8)
0.34
0.14
to
0.87
0.032
0.35
0.14
to
0.90
0.047
Q3
-
1
-
(13.9)
0.95
0.75
to
1.20
0.070
0.96 0.75
to
1.21
0.046
Q4
-
1
-
(55.6)
0.90
0.71
to
1.14
0.159
0.79
0.60
to
1.04
0.535
Total
protein
0.66
0.54
to
0.80
<0.001
0.62
0.50
to
0.77
<0.001
Q1
-
1
-
(73.3)
1.00
1.00
Q2
-
1
-
(78.1)
0.72
0.55
to
0.95
0.562
0.70
0.52
to
0.92
0.404
Q3
-
1
-
(81.8)
0.64
0.48
to
0.84
0.380
0.58
0.43
to
0.78
0.226
Q4
-
1
-
(86.8)
0.48
0.37
to
0.64
<0.001
0.43
0.32
to
0.59
<0.001
Albumin
0.72
0.59
to
0.87
<0.001
0.70
0.56
to
0.87
0.001
Q1
-
1
-
(44.4)
1.00
1.00
Q2
-
1
-
(47.6)
0.74
0.57
to
0.98
0.686
0.72
0.54
to
0.96
0.516
Q3
-
1
-
(49.9)
0.62
0.47
to
0.81
0.077
0.58
0.43
to
0.78
0.054
Q4
-
1
-
(52.8)
0.58
0.44
to
0.76
0.012
0.52
0.37
to
0.72
0.004
*Controlling
for
age,
education
level,
physical
activity
time,
income,
monthly
expenditure
on
food
and
region.
tAll
the
case
and
control
women
were
combined
together
and
the
quartile
was
used.
BMI,
body
mass
index.
M.
day
food
record
and
blood
protein
status.
As
we
know,
data
testing
in
the
laboratory
is
more
accurate
than
cal-
culation
using
a
food
composition
table
and
question-
naire.
Because
blood
total
protein
and
albumin
reflect
the
long-term
protein
nutrition
status,
in
order
to
improve
protein
status
an
effective
strategy
to
supply
suf-
ficient
food
rich
in
protein,
such
as
soy
food,
is
needed.
Compared
with
animal
foods,
soy
foods
such
as
tofu,
tofu
jelly
and
soy
milk
are
cheap
and
more
accessible,
particularly
in
the
poor
rural
areas
of
China.
However,
consumption
of
only
one
kind
of
food
does
not
provide
sufficient
nutrients
and
a
variety
of
foods
is
important
for
improving
one's
health.
In
our
study
the
food
intake
in
both
cases
and
controls
was
inadequate
according
to
the
'Dietary
guideline
for
Chinese
residents',
which
is
probably
the
reason
for
the
high
prevalence
of
anaemia
in
the
study
population.
Diet
modification
is
an
eco-
nomic
and
sustainable
measurement
for
the
improve-
ment
in
anaemia
generally,
especially
in
rural
areas
of
China.
In
terms
of
haematological
iron
status,
we
selected
TS,
serum
FER
concentration
and
the FEP/haemoglobin
ratio
to
evaluate
the
stage
of
IDA.
SI
represents
combined
TF
iron
in
the
blood
circulation
and
reflects
the
amount
of
iron
used
for
haematopoiesis
in
nucleated
red
blood
cells
in
the
bone
marrow.
However,
SI
does
not
reflect
iron
storage.
SI
always
falls
below
10
µmol/L
22
in
indivi-
duals
with
iron
deficiency.
Serum
FER,
TF
and
TS
are
indicators
of
iron
stores
of
the
body.
23
If
the
TF
concen-
tration
is
normal
or
depressed
while
the
TS
increases,
it
shows
that
the
body
is
malnourished
or
even
has
chronic
disease.
24
IDA
and
the
anaemia
of
chronic
disease
(ACD)
are
common
in
elderly
people,
and
the
differential
diag-
nosis
between
the
two
types
of
anaemia
is
challenging
because
many
factors
affect
iron
absorption.
Hepcidin
2
may
be
a
useful
indicator
of
deficient
iron
stores
which
regulates
iron
absorption
and
recycling
by
inducing
the
degradation
of
ferroportin
in
the
intestine
and
macro-
phages.
sTfR,
26
a
diagnostic
biomarker
which
distin-
guishes
between
IDA
and
ACD,
is
always
used
in
the
elderly
hospitalised
population,
but
the
sensitivity
and
specificity
need
further
testing
in
elderly
persons
in
the
community.
The
criteria
used
to
classify
IDA
and
ACD
differ
from
one
study
to
another,
with
one
study
using
a
cut-off
FER
of
22
pg/L
to
diagnose
iron
deficiency
27
while
another
used
a
FER
level
of
30
pg/L
as
the
cut-off
limit
for
exclusion
of
IDA.
28
However,
IDA
and
ACD
can
coexist,
so
the
detection
of
iron
deficiency
in
the
pres-
ence
of
chronic
disease
can
be
an
important
diagnostic
challenge.
More
research
is
needed
to
analyse
the
aeti-
ology
of
anaemia
in
the
elderly
population.
Limitations
This
study
has
a
number
of
limitations.
First,
we
selected
individuals
with
a
haemoglobin
level
of
90-120
mg/L
as
cases
and
>130
mg/L
as
controls;
individuals
with
6
Song
P,
et
al.
BMJ
Open
2014;4:e004751.
doi:10.1136/bmjapen-2013-004751
Open
Access
serious
diseases
were
excluded
and
the
health
status
of
the
previous
half
year
was
collected
by
questionnaire,
but
it
did
not
effectively
rule
out
the
possibility
of
chronic
diseases
using
the
questionnaire
and
the
bio-
chemical
indices
only.
Some
chronic
diseases
such
as
inflammation,
infection,
tumour
and
liver
diseases
could
also
lead
to
anaemia,
but
we
could
not
examine
chronic
diseases
precisely
in
the
study
field.
We
therefore
could
not
differentiate
the
exact
causes
of
anaemia
in
these
elderly
women,
particularly
in
poor
rural
areas.
Second,
we
measured
food
intake
by
consecutive
individual
three-day
food
records.
Although
face-to-face
interviews
were
carried
out
by
experienced
investigators,
recall
bias
-particularly
in
elderly
people-was
inevitable.
Third,
the
case-control
study
was
designed
from
effects
to
causes;
women
who
were
anaemic
might
take
measures
to
improve
their
anaemia
before
we
conducted
the
study.
However,
subjects
were
questioned
about
whether
haemoglobin
tests
were
conducted
previously
and
the
awareness
and
treatment
of
anaemia
and
it
was
found
that
the
number
of
women
who
tested
the
haemoglobin
concentration
previously
and
the
awareness
of
anaemia
was
very
low.
The
treatment
of
anaemia
was
to
take
drugs
but
not
to
improve
dietary
nutrition
and
take
physical
exercise,
so
we
believe
that
eating
habits
and
physical
exercise
were
stable
over
time
although
we
did
not
have
sufficient
evidence
to
support
our
claim.
Fourth,
when
we
conducted
the
logistic
regression
model,
several
naturally
continuous
variables
(eg,
BMI,
income)
were
categorised
for
the
purpose
of
analysis,
which
might
have
increased
the
possibility
of
residual
confounding
and
decreased
the
precision
and
power
of
the
study.
However,
we
compensated
for
this
limitation
by
choosing
categories
with
a
number
of
sufficiently
narrow
intervals
to
decrease
the
residual
confounding.
Finally,
we
presented
the
OR
for
anaemia
by
logistic
regression
in
the
three
rural
areas
of
China,
and
these
findings
may
not
be
generalisable
to
other
populations.
CONCLUSION
Based
on
the
results,
the
current
investigation
has
two
key
findings
and
implications.
One
is
that
the
over-
whelming
majority
of
surveyed
elderly
women
living
in
poor
rural
areas
were
in
poor
nutritional
status
because
of
low
food
intake.
The
result
of
insufficient
food
and
nutrients
has
implications
that
increasing
whole
food
quality,
such
as
foods
rich
in
protein,
can
be
defined
as
an
effective
strategy.
The
other
key
finding
is
that
the
blood
protein
status
was
associated
with
anaemia.
These
findings
persisted
even
after
taking
account
of
demo-
graphic
and
socioeconomic
indicators.
Further
research
should
focus
on
the
aetiology
of
anaemia
in
the
elderly
and
also
take
into
account
new
biomarkers
to
diagnosis
elderly
anaemia
so
that
more
effective
treatments
and
health
education
strategies
for
reduction
of
anaemia
can
be
robustly
conducted.
Acknowledgements
We
are
grateful
to
all
participants
in
the
study.
We
also
thank
our
colleagues
at
the
laboratory
and
the
staff
at
the
local
Centres
for
Disease
Control
in
Jiangsu,
Anhui
and
Shaanxi
Province.
Contributors
JZ
designed
the
study.
PKS,
LPM,
QQM,
LXL
and
CRW
collected
human
samples
and
clinical
data.
PKS
conducted
the
statistical
analysis
of
the
data.
PKS
and
JZ
wrote
the
paper.
Funding
This
work
was
supported
by
research
grants
from
Chinese
Nutrition
Society
Foundation
(grant
number
05038)
and
Nestle
Foundation
for
the
Study
of
Problems
of
Nutrition
in
the
World.(http://www.nestlefoundation.org/
e/docs/AnnualReport2004.pdf)
Competing
interests
None.
Patient
consent
Obtained.
Ethics
approval
Ethics
approval
was
obtained
from
the
Ethics
Committee
of
the
Institute
of
Nutrition
and
Food
Safety,
Chinese
Center
for
Disease
Control
and
Prevention.
Provenance
and
peer
review
Not
commissioned;
externally
peer
reviewed.
Data
sharing
statement
No
additional
data
are
available.
Open
Access
This
is
an
Open
Access
article
distributed
in
accordance
with
the
Creative
Commons
Attribution
Non
Commercial
(CC
BY-NC
3.0)
license,
which
permits
others
to
distribute,
remix,
adapt,
build
upon
this
work
non-
commercially,
and
license
their
derivative
works
on
different
terms,
provided
the
original
work
is
properly
cited
and
the
use
is
non-commercial.
See:
http://
creativecommons.org/licenses/by-nc/3.0/
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