Dioxins and Fatty Acids in Breast Milk of Primiparas in Yonago District, Tottori Prefecture, Japan

Yonago Acta medica 2002;45:103–111
Dioxins and Fatty Acids in Breast Milk of Primiparas in Yonago
District, Tottori Prefecture, Japan
Mari Sampei, Koji Kimura*, Kousaku Ohno†, Shiro Ikawa‡ and Kazuo
Yamada§
Department of Women’s and Children’s Family Nursing, School of Health Science, Tottori Uni-
versity Faculty of Medicine, *Radioisotope Research Center, Tottori University, †Department of
Child Neurology, Institute of Neurological Sciences, ‡Division of Clinical Laboratory Medicine
and §Division of Medical Biochemistry, Department of Pathophysiological and Therapeutic
Science, School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8503 Japan
We analyzed the concentrations of polychlorinated dibenzo-p-dioxins (PCDDs) and
dibenzofurans (PCDFs) in breast milk collected 1 week after childbirth from 8
primiparas in Yonago district, Tottori Prefecture, and investigated the relationship
between PCDDs or PCDFs and fatty acids in concentration, and the relationship between
dioxin concentration and kind of daily foods. The mean total content of dioxins (PCDDs
and PCDFs) was 0.48 pg-toxic equivalent (TEQ)/g (range 0.12–1.04 pg-TEQ/g) in breast
milk, and 16.7 pg-TEQ/g-fat (range 9.6–32.7 pg-TEQ/g-fat) in total lipids of breast
milk. The 8 primiparas showed a low mean dioxin concentration: the levels were
lower in 6 of them and higher in 2 of them than in primiparas living in other cities in
Japan. For 1 of the 2 mothers, the reason for the high level was thought to be her poor
intake of vegetables in the diet. The total dioxin content was well correlated with the
total lipid content ranging from 1% to 3%. Fatty acids with C16:0 and C18:1 dominated
those with C12:0, C14:0, C16:1, C18: 2 and C18:0, which were commonly detected. The amount
of fatty acids with C10:0, C20:1, C20:2, C20:3, C20:4, C22:5 and C22:6 was small. Gas chromato-
grams of these fatty acids generally showed similar distributions in breast milk of the 8
primiparas. The contents of fatty acids ranged from 17.1 to 31.3 mg/g (average 24.0
mg/g) in bulk breast milk. No clear correlation was found in concentration between
PCDDs or PCDFs and specific fatty acids in breast milk.
Key words: breast milk; fatty acid; food life; lipid; polychlorinated dibenzo-p-dioxin; polychlor-
inated dibenzofuran; primipara
Polychlorinated dibenzo-p-dioxins (PCDDs)
recent years, dioxins in breast milk have been
and polychlorinated dibenzofurans (PCDFs),
detected many times higher than the normal
which are reported as “endocrine disruptors”,
concentration in breast milk, and the influence
have a severe toxicity which acts as internal se-
on babies and infants is a serious problem
cretions causing sexual disturbances (Schuler et
(Ministry of Health and Welfare, 1998). We
al., 1997; Kayama, 1998; Matsuo, 1998). The
wanted to clarify the qualitative and quantita-
presence of dioxins (PCDDs and PCDFs) in
tive relationship between the concentrations of
breast milk has increased the advocation of
dioxins and fatty acids, and the habitual intake
women’s and children’s health (Sakai, 1998;
of daily food. The exposure to dioxins has been
Watanabe et al., 1999; LaKind et al., 2001). In
decreasing as shown by a downward trend of
Abbreviations: GC, gas chromatography; MS, mass spectrometry, PCDD, polychlorinated dibenzo-p-dioxin;
PCDF, polychlorinated dibenzofuran; TEF, toxic equivalency factor; TEQ, toxic equivalent
103

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M. Sampei et al.
Table 1. Primiparas’ data, dietary life and living environments
Status of
Lipid content
Meal*
Sample Age
Height Weight
milk
in breast milk
number (year)
(cm)
(kg)
secretion
(% )
Vegetable Meet
Fish Residence
1
30
155
60.0
Good
2.49
–
2+
2+
Yonago city
2
25
157
53.5
Normal
2.32
2+
2+
2+
Yonago city
3
27
160
71.3
Good
1.25
2+
2+
2+
Yonago city
4
31
158
61.0
Good
3.03
2+
2+
2+
Saihaku-county
5
33
161
56.2
Not so good
3.26
3+
2+
+
Yonago city
6
27
150
63.0
Normal
3.54
2+
2+
2+
Tohaku-county
7
27
152
64.5
Good
4.31
2+
3+
2+
Saihaku-county
8
30
150
59.8
Very good
2.47
3+
2+
2+
Tohaku-county
* 3+, often; 2+, common; +, rare; –, little.
dioxins both in human breast milk and serum
twice a day between day 3 and day 7. The col-
lipids during the last 20 to 30 years (Kiviranta et
lected quantity was 10 to 20 mL each, totaling
al., 1999; Ministry of Health, Labour and Wel-
approximately 100 mL. The specimen was then
fare of Japan, 2000; Przyrembel et al., 2000);
stored in a refrigerator at –80?C until analysis.
however, the level of dioxin content has not
Age and occupation of the primiparas were
been made clear in smaller cities, which we
not fixed and control of meals was not perform-
think should be made evident. In the San-in
ed. However, they ate hospital food during
region of Japan, except for Shimane Prefecture,
their hospitalization. Table 1 shows the condi-
breast milk has still not been analyzed for
tions of the primiparas and other information.
dioxins. Little information is available for
The 8 primiparas well understood the pur-
allowing a good assessment of breast milk in
pose of the study as we explained it to them, and
mothers especially in Tottori Prefecture. A
their consent to publish the data was obtained.
solution to the actual situation in Yonago dis-
trict has long been awaited in order to help
GC/MS conditions for dioxin analysis
expecting mothers who visit in Tottori Univer-
sity Hospital learn more about breastfeeding.
A high-resolution gas chromatograph/high-
For this study, we analyzed and estimated
resolution mass spectrometer (double-focusing
the contents of PCDDs, PCDFs and lipids in
type) is normally used for dioxin analysis. Gas
breast milk of primiparas (mothers of firstborn
chromatography/mass spectrometry (GC/MS)
children) who live in Yonago district, and dis-
operating conditions recommended for dioxin
cussed the quantitative relationships among
analysis by the guideline of the Ministry of
them.
Health, Labour and Welfare of Japan are i) the
resolution must be above 10,000 and ii) every
m/z set up must be less than 4 decimal points
Materials and Methods
(Ministry of Health and Welfare of Japan, 1997;
Environment Agency of Japan Dioxin Risk
Evaluation Committee, 1998a). The analysis of
Breast milk samples
dioxins was done at the Hiroshima Environ-
Breast milk was obtained from 8 primiparas in
ment and Health Association.
good health who were hospitalized at Tottori
University Hospital and had a normal delivery.
Samples were collected after suckling the baby
104

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Dioxins and fatty acids in breast milk
Table 2. Concentration of PCDDs and PCDFs in breast milk
Sample PCDD/total milk* PCDF/total milk* PCDD/total lipids† PCDF/total lipids†
number
(pg/g) (pg-TEQ/g)
(pg/g) (pg-TEQ/g) (pg/g-fat) (pg-TEQ/g-fat) (pg/g-fat) (pg-TEQ/g-fat)
1
9.40
0.68
0.30
0.15
380
26.7
0
6.0
2
3.40
0.17
0.10
0.05
150
7.60
4
2.0
3
2.50
0.12
0.00
0.00
200
10.1
0
0.0
4
2.50
0.18
0.20
0.10
83
6.60
7
3.5
5
11.0
0.73
1.10
0.31
330
22.7
32
9.6
6
3.00
0.28
0.22
0.11
86
7.60
6
3.0
7
6.10
0.43
0.38
0.13
140
9.30
9
3.3
8
5.50
0.27
0.24
0.12
230
10.9
10
5.0
PCDD, polychlorinated dibenzo-p-dioxin; PCDF, polychlorinated dibenzofuran; TEQ, toxic equivalent.
* Total breast milk.
† Total lipids of breast milk.
GC and GC/MS conditions for fatty acid
Separation before GC and GC/MS analy-
analysis
ses
The analysis of fatty acids was performed at the
The extraction of dioxin types was performed
Tottori University Faculty of Medicine Mass
based on guidelines set by the Environment Agen-
Spectrometry Laboratory. Breast milk was
cy of Japan Dioxin Risk Evaluation Committee
methylesterized according to the method of
(1998a). The typical process has usually followed
Yamamoto (1962). Quantitative analysis was
the guideline of the Environment Agency of
performed by a Hitachi G-5000 gas chromato-
Japan. Separation, extraction and methylesteri-
graph. A JMS-DX 303 (JEOL, Tokyo, Japan)
fication of fatty acids were based on the modi-
and a GC 5890 (Hewlett Packard, Avondale,
fication of the method of Yamamoto (1962) and
PA) were used for qualitative analysis by GS/
Maeda et al. (1996).
MS.
GC conditions for the analyses were as fol-
lows: Carrier gas was helium (35 mL/min).
Results
The initial temperature was held at 150?C for 2
min, and then raised at a ratio of 5?C/min to
Dioxin content in breast milk
270?C and finally retained at 270?C for 15 min.
The temperature of the injector port was 250?C,
Tables 2 and 3 show the PCDD and PCDF con-
and detector, 300?C. A capillary column DB–5
tents in breast milk samples obtained from the 8
(J & W Scientific Co., Folsom, CA) (weak po-
primiparas. The concentration of dioxin is re-
larity; internal diameter 0.25 mm; film 0.25 µm;
ported by a quantity, that is, toxic equivalent
length 30 m) for GC fatty acid analysis was
(TEQ) of total dioxins (PCDDs + PCDFs). The
employed.
TEQ is the sum of every chemical isomers. The
Mass spectra were measured by positive
toxicity of dioxin differs for every chemical iso-
electron impact ionization at 70 eV and 300 µA.
mer. Because the toxicity of 2,3,7,8-4 chlorida-
The capillary column from the CBP 1 (J & W
tion is the strongest among isomers, that of the
Scientific Co.) (internal diameter 0.25 mm;
other isomers is expressed by toxic equivalency
length 25 m) was employed for GC/MS use.
factor (TEF), as relative toxicity for 2,3,7,8-4
The fatty acid concentration was standardized
chloridation (TEF = 1) (Miyata, 1998a). We
by heptadecanoic acid (C17:0) as the standard by
calculated total dioxins as the sum of PCDDs
an area ratio.
and PCDFs in pg-TEQ, to exclude coplanar-
polychlorinated biphenyl.
105

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M. Sampei et al.
Table 3. Concentration and TEQ of total dioxins (PCDDs + PCDFs)
Sample PCDDs + PCDFs/total breast milk PCDDs + PCDFs/total lipids of breast milk
number
(pg/g)
(pg-TEQ/g)
(pg/g-fat)
(pg-TEQ/g-fat)
1
9.7
0.83
380
32.7
2
3.5
0.22
154
9.6
3
2.5
0.12
200
10.1
4
2.7
0.28
90
10.1
5
12.1
1.04
362
32.3
6
3.2
0.39
92
10.6
7
6.5
0.56
149
12.6
8
5.7
0.39
240
15.9
PCDD, polychlorinated dibenzo-p-dioxin; PCDF, polychlorinated dibenzofuran; TEQ, toxic equivalent.
5
International ranges of the contents excluding Japan
Domestic ranges of the contents
4
3
requency
2
F
1
0
0-4
5-9
10-14
15-19
20-24
25-29
30-34
35-39
40-44 45-49 (pg-TEQ/g-fat)
Total dioxins in total lipids of breast milk
Fig. 1. Histogram of toxic equivalents (TEQ) for total dioxins (PCDDs + PCDFs)
in the total lipids of breast milk.
Table 2 shows the PCDD content in total breast
TEQ/g-fat (average 16.7 pg-TEQ/g-fat). Figure 1
milk ranging from 0.12 to 0.73 pg-TEQ/g and
shows a histogram of the total dioxin content in
the PCDF content ranging from 0 to 0.31 pg-TEQ/
the total lipids of breast milk. Primiparas 1 and
g. The total dioxin (PCDDs + PCDFs) content in
5 had abnormally high levels at 32.3 and 32.7
total breast milk ranged from 0.12 to 1.04 pg-
pg-TEQ/g-fat, but the other 6 primiparas had
TEQ/g (average 0.48 pg-TEQ/g) (Table 3).
lower levels, 9.6 to 15.9 pg-TEQ/g-fat.
On the other hand, the PCDD content in the
Their PCDD/PCDF ratio was about 2 times
total lipid amount of breast milk ranged from
higher than that (42/30 = 1.4) analyzed from
6.6 to 26.7 pg-TEQ/g-fat and the PCDF content,
food intake in an adult population in the United
from 0 to 9.6 pg-TEQ/g-fat (Table 2). The total
States (Schecter et al., 2001).
dioxin (PCDDs + PCDFs) content in the total
lipid of breast milk ranged from 9.6 to 32.7 pg-
106

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Dioxins and fatty acids in breast milk
(pg-TEQ/g)
1.2
Relationship between the dioxin and li-
No. 5
pid contents
1.0
Figure 2 shows the relationship of the dioxin
No. 1
content in TEQ to the lipid content in breast
0.8
milk. The lipid content was 1.25% to 4.31% in
xins
No. 7
breast milk (Table 1). Exclusive of primiparas
0.6
1 and 5, the dioxin content in TEQ showed a
otal dio
No. 8
No. 6
high correlation (r2 = 0.819) to the lipid content.
T
0.4
Correlations were also high between TEQ-
in total breast milk
No. 4
No. 2
based contents of PCDDs and PCDFs in total
0.2
y = 0.132x - 0.044
No. 3
breast milk and in total lipids of breast milk
r 2 = 0.819
(Fig. 3).
0.0 0
2
4
6 (%)
Total lipids of breast milk
Fatty acid composition of breast milk
Fig. 2. Relationship between the total lipid and
The representative GC tracings of isolated fatty
dioxin contents in breast milk. TEQ, toxic equiva-
acids and internal standard fatty acid are shown
lent.
in Fig. 4 (methylesters). Identification of each
fatty acid methylester was from a fragment pat-
tern in the mass spectrum (Fig. 5). The most
concentrated fatty acids in breast milk of the 8
C10:0, C20:1, C20:2, C20:3, C20:4, C22:5 and C22:6.
primiparas were C16:0 and C18:1. The common-
GC showed a similar tendency in the distribu-
est fatty acids were C12:0, C14:0, C16:1, C18:2 and
tion patterns of these fatty acids throughout the
C18:0. The fatty acids in trace amounts were
8 primiparas.
(pg-TEQ/g)
(pg-TEQ/g-fat)
0.4
12
y = 0.330x + 0.003
r 2 = 0.738
0.3
8
0.2
PCDFs
PCDFs
4
0.1
in total breast milk
y = 0.279x + 0.515
r 2 = 0.544
in total lipids of breast milk
0.0
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
0
10
20
30
40
(pg-TEQ/g)
(pg-TEQ/g-fat)
PCDDs
PCDDs
in total breast milk
in total lipids of breast milk
Fig. 3. Relationship between the PCDD and PCDF contents in total breast milk of 8 primiparas (left)
and in total lipids of breast milk (right). PCDD, polychlorinated dibenzo-p-dioxin; PCDF,
polychlorinated dibenzofuran; TEQ, toxic equivalent.
107

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M. Sampei et al.
C16:0
C18:1
15.9
22.5
C14:0
1.1
1
C12:0
Standard
C20:4
7.4
C17:0
C20:3
28.1
C
19.2
20:2
C
28.8
18:2
C
C
18:0
20:1
C
29.5
C
16:1
22:6
22.0
29.7
C
C
23.3
22:5
10:0
15.1
34.8
4.6
35.0
5
(min)
10
15
20
25
30
35
40
45
50
Retention time
Fig. 4. Gas chromatogram of methylester of fatty acids from primipara 3.
Fig. 5. Mass spectrum of methylester of C18:2 from primipara 3.
of primiparas are at significantly higher levels
Discussion
of concentration than in multiparas (Vartiainen,
1997; Iida et al., 1999). The total dioxin content
we measured in total lipids of breast milk rang-
Factors controlling the dioxin content in
ed from 9.6 to 32.7 pg-TEQ/g-fat (average 16.7
breast milk
pg-TEQ/g-fat). The ranges of dioxin content
We measured the level of dioxins in breast milk
reported in Europe and Asia were from 6 to 40
of 8 primiparas in Yonago district. Only the
pg-TEQ/g-fat (average 21 pg-TEQ/g-fat) (En-
breast milk of primiparas was used as samples,
vironment Agency of Japan Dioxin Risk Evalu-
because PCDDs and PCDFs in the breast milk
ation committee, 1998b). Domestic research
108

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Dioxins and fatty acids in breast milk
Table 4. Fatty acid compositions in breast milk 1 week after childbirth
Retention
Sample number
Peak
time
2
3
4
5
6
7
8
number
(min)
(mg/g)
(mg/g)
(mg/g)
(mg/g)
(mg/g)
(mg/g)
(mg/g)
A (C10:0)
4.6
0.38
0.16
0.55
0.63
1.10
0.67
0.25
1 (C12:0)
7.4
2.71
1.29
3.71
2.96
5.29
3.28
1.76
2 (C14:0)
11.1
4.75
2.47
6.17
3.45
6.70
4.41
3.27
3 (C16:1)
15.1
1.64
0.92
2.93
1.41
2.95
2.91
1.82
4 (C16:0)
15.9
11.65
7.60
18.35
11.66
17.48
19.47
12.25
6 (unknown)
18.4
0.38
0.08
0.21
0.13
0.25
0.28
0.14
7 (C17:0)*
19.2
3.00
3.00
3.00
3.00
3.00
3.00
3.00
8 (C18:2)
22.0
3.98
4.15
6.52
4.14
9.03
11.66
3.87
9 (C18:1)
22.5
12.58
10.85
14.30
13.86
19.75
21.97
17.83
10 (C18:0)
23.3
3.02
1.58
3.25
3.73
3.45
4.03
3.14
11 (C20:4)
28.1
0.25
0.24
0.49
0.34
0.48
0.59
0.37
12 (C20:3)
28.8
0.22
0.17
0.47
0.22
0.36
0.45
0.24
13 (C20:2)
29.5
0.28
0.26
0.44
0.27
0.56
0.61
0.56
14 (C20:1)
29.7
0.40
0.28
0.53
0.36
0.61
0.75
0.61
15 (unknown)
34.6
0.24
0.17
0.20
0.13
0.15
0.10
0.13
16 (C22:6)
34.8
0.11
0.63
1.12
0.78
0.88
0.72
0.80
17 (C22:5)
35.0
0.14
0.34
0.40
0.23
0.31
0.33
0.42
Total
45.74
34.18
62.63
47.30
72.34
74.56
50.47
* Standard.
has reported levels of 10.9 to 44.6 pg-TEQ/g-fat
According to the Fukuoka Prefecture Health
(average 23.9 pg-TEQ/g-fat) in total lipids of
Environment Research Laboratory (Miyata,
breast milk (Akita 10.9; Sendai 11.4; Niigata
1998a), food fiber including cellulose absorbs
18.3; Saitama 22.8; Hamamatsu 28.1; Osaka 44.6;
dioxins in the small intestine, which are durable
Nara 40.5; Fukuoka 15.0; Okinawa 23.6 pg-
in the excretion of feces. Consequently, the rea-
TEQ/g-fat) (Miyata, 1998b; Saitama Prefecture
son why the dioxin content was high in primip-
Health and Welfare Division, 1998). The mean
ara 1 might have been because of her low vege-
dioxin level we found in Yonago district was
table intake, although the number of breast milk
somewhat lower than these levels.
samples analyzed may not have been neces-
The total dioxin concentrations of the 8 pri-
sarily adequate.
miparas were abnormally higher in 2 mothers
The 2nd-highest content of dioxins was in
(32.3 and 32.7 pg-TEQ/g-fat) than in the 6
primipara 5 which requires another explana-
others (9.6–15.9 pg-TEQ/g-fat). This does not
tion. Although she had a high intake of vege-
seem to be due to their body size (height and
tables, she had lived near a garbage incinerator
weight in Table 1) or breast milk secreting
in Osaka for a long time. Considering that ap-
states, but to differences in dietary habits.
proximately 80% of dioxins comes from trash
Table 1 shows daily food data obtained from the
burning facilities (Miyata, 1998a), the primary
8 primiparas during personal interviews. For
factor of her high content may be because of her
primipara 1 with a high dioxin content in breast
residential environment. To uncover this as a
milk, her vegetable intake was extremely low,
possible cause, it should be further examined
while the other primiparas ate a good amount of
whether the primipara was a first born child or
vegetables every day. This primipara normally
not, or how old she was when she delivered her
ate fish and meat frequently, about 2 to 7 times
first child.
a week.
109

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M. Sampei et al.
(pg-TEQ/g-fat)
Our results suggest that the dioxin content in
35
breast milk is not related to a specific fatty acid.
No. 1
No. 5
However, a probable correlation was indicated
30
between the dioxin and total lipid contents in
breast milk, as shown in Fig. 2. PCDDs and
25
PCDFs are dispersed equally among the lipid
xins
20
compartments of breast milk (Przyrembel et al.,
No. 8
2000). A higher lipid content (2–7%), on the
15
contrary, is negatively correlated with the diox-
No. 7
otal dio
T
in content in total lipids of breast milk (Saitama
10
No. 3
No. 2 No. 4
No. 6
Prefecture Health Welfare Division, 1998).
5
This could be due to a diluting effect of dioxins
in total lipids of breast milk
by lipids. However, our results did not show
0 0
2
4
6 (%)
such a diluting effect, and we proved constant
TEQ-based levels except for the 2 abnormally
Total lipids of breast milk
dioxin-abundant breast milk specimens of pri-
Fig. 6. Relationship between the lipid content in
miparas 1 and 5 (Fig. 6). In these cases, we
breast milk and the total dioxin content in total lipids
must take notice that the total amount of dioxins
of breast milk. TEQ, toxic equivalent.
in breast milk increased as the lipid content in-
creased.
The effects of smoking on the concentration
of dioxins are not discussed in the present pa-
Aknowledgments: We are grateful to Professor Naoki
per.
Terakawa, Division of Reproductive-Perinatal Medi-
cine and Gynecologic Oncology, School of Medicine,
Professor Takako Maeda, Department of Women’s and
Relationship between the dioxin and lipid/
Children’s Family Nursing, School of Health Science,
fatty acid contents
Tottori University Faculty of Medicine, and Chief
Nurse Nobuko Inada, Division of Maternity Services,
The GC patterns of distribution of common
Tottori University Hospital, for thier kindness in en-
fatty acids were similar through out the 8 pri-
couraging us throughout this study. We also thank the 8
primiparas hospitalized at Tottori University Hospi-
miparas, as shown in Fig. 4. These results indi-
tal. Our special appreciation goes to Mr. Takashi
cate that there was no clear relationship be-
Nakamura of the Hiroshima Environment and Health
tween the dioxin content and fatty acid compo-
Association, for his pricise analyses of the dioxin speci-
sition. The most concentrated fatty acids were
mens.
C
This study was supported by a research grant of
16:0 and C18:1, in accordance with previous
Tottori University College of Medical Care Technolo-
reports (Yamamoto, 1962; Maeda et al., 1996).
gy, 1998.
The concentration of all fatty acids in breast
milk ranged from 34.2 to 74.6 mg/g (average
55.3 mg/g) 1 week after childbirth (Table 4),
References
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1 Environment Agency of Japan Dioxin Risk Eval-
1 month after childbirth (data not shown). The
uation Committee. [Risk evaluation of dioxine.]
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110

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Corresponding author: M. Sampei
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