Jurnal Gizi dan Dietetik Indonesia
(Indonesian Journal of Nutrition and Dietetics)
Vol. 9, No. 2, 2021: 77-84

Available online at: http://ejournal.almaata.ac.id/index.php/IJND
DOI : http://dx.doi.org/10.21927/ijnd.2021.9(2).77-84

Effect of Sago worm flour (Rhynchhorus feirugineus) on Albumin
and Haemoglobin in Protein Energy Malnutrition (PEM) Wistar rats
Aleda Florince Oyay1*, Muchlis Achsan.Udji Sufro2, Gemala Anjani3
Master Student of Nutrition, Faculty of Medicine, Diponegoro University, Jalan Prof Sudharto Semarang 50275,
Indonesia
2
Department of Interna, Faculty of Medicine, Diponegoro University, Jalan Prof Sudharto Semarang 50275, , Indonesia
3
Department of Nutrition, Faculty of Medicine, Diponegoro University, Jalan Prof Sudharto Semarang 50275, Indonesia
*Correspondence: florincealeda@gmail.com
1

ABSTRAK
Latar Belakang: Kurang energi protein (KEP) merupakan salah satu penyakit gangguan gizi yang penting di
Indonesia. Dampak kekurangan protein yang parah umumnya terjadi pada bayi dan balita. Dalam keadaan
KEP terdapat perubahan nilai Hemoglobin dan albumin dalam darah. Ulat sagu dikenal sebagai makanan yang
kaya akan protein, sehingga diharapkan dapat memperbaiki status albumin dan Hemoglobin anak dengan KEP.
Tujuan: Mengetahui pengaruh pemberian tepung ulat sagu terhadap kadar albumin dan Hemoglobin (Hb)
tikus wistar KEP
Metode: Penelitian true experimental dengan Pre post test control group design. Menggunakan 24 ekor tikus
wistar kemudian dibagi menjadi 4 kelompok: K- (tikus normal); K+(tikus KEP); P1(tikus KEP dengan intervensi
tepung ulat sagu 0,36g/100gBB); dan P2(tikus KEP dengan intervensi tepung ulat sagu 1,36g/100gBB). Intervensi
dilakukan selama 28 hari. Analisis statistik menggunakan metode Shaphiro Wilk, One Way Anova.
Hasil: Terdapat perbedaan yang signifikan (p>0,05) pada berat badan, kadar albumin, dan Hemoglobin
pada intervensi pemberian tepung ulat sagu pada tikus wistar KEP.
Kesimpulan: Tepung ulat sagu meningkatkan berat badan, kadar albumin, dan kadar Hb tikus wistar KEP.
KATA KUNCI: Albumin; Hemoglobin; Kurang energi protein (KEP); tepung ulat sagu

ABSTRACT
Background: Protein energy malnutrition (PEM) is one of the most important nutrition disorder in Indonesia.
The impact of a severe protein deficiency generally occurs in infants and toddlers. In the PEM there is a
change in the albumin and Hemoglobin (Hb) levels. Sago caterpillar flour contain high protein, so it can
improve the nutritional status of albumin and Hemoglobin levels in children with PEM.
Objectives: To observe the effect of sago caterpillar flour on albumin and Hemoglobin (Hb) levels on PEM
Wistar rats
Methods: True experimental pre-post control group design. 24 Wistar rats were divided into 4 groups:
K-(normal rats); K+(PEM rats); P1(PEM rats with intervention of 0.36g/100gBW sago caterpillar flour);
P2(PEM rats with intervention of 1.36g/100gBW sago caterpillar flour). Statistical analysis using Shapiro
Wilk method and One Way ANOVA.
Results: There were significant differences (p.0.05) in body weight, albumin levels, and Hemoglobin in the
intervention of sago caterpillar flour in PEM Wistar Rats.
Conclusions: Sago caterpillar flour increased body weight, albumin levels, and Hemoglobin levels in
PEM Wistar Rats
KEYWORDS: Albumin; Hemoglobin; Protein energy malnutrition (PEM); Sago worm flour

Article info:
Article submitted on April 14, 2021
Articles revised on May 25, 2021
Articles received on June 3, 2021

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Aleda Florince Oyay, Muchlis Achsan, Udji Sufro, Gemala Anjani, Vol 9 No.21, 2021: 21-28

INTRODUCTION
Protein Energy Malnutrition (PEM) form of
malnutrition caused by a lack of energy and protein
in various proportions. PEM divided into three
categories: kwashiorkor, marasmus, and marasmus
kwashiorkor (1). The prevalence of PEM mostly
found in children under five years and pregnantlactating women. In children under 5 years, the
most common cases of PEM are marasmus and
kwashiorkor (2). PEM often founding in developing
countries, one is Indonesia. Data from Basic Health
Research of Indonesia (RISKERDAS) in 2018 show,
13.8% of children with malnutrition and 3.9% of
children with severe malnutrition (3). The distribution
of PEM prevalence in Indonesia covers 19 provinces
from a total of 34 provinces. Province of Papua and
West Papua included in the PEM distribution area
(4,5).
The impact of severe protein deficiency is
related to changes in Hemoglobin and albumin
levels. The albumin levels selected as an indicator
for determining of PEM because it is the most
abundant manifestation of protein plasma in the
blood (6). Function of serum albumin is to maintain
plasma osmotic pressure and carry the various types
of substance and hormones to the organs (7,8,9). In
the condition of PEM, one of the clinical symptoms
that can be observed is anemia (10). It is related
because erythroprotein plays a role in stimulating
the production of red blood cells (11).
Various alternatives for handling incidence
of PEM have been carried out. One of them is the
assistance for family food security by utilization
of local food materials. Sago worm is one of the
local food ingredients that can be found in eastern
of Indonesia (mainly in Papua and West Papua)
and has health benefits effect (12). Papua Sago
worm contain high protein (10.39gr/100gr) and has
good digestibility (92%) (13). All types of essential
amino acid are found in Papua Sago worms (14).
The highest amino acid in Papua Sago worm are
phenylalanine and lysine. Study show, intervention
of sago worm flour decrease parasitemia index and
increase the Hemoglobin levels of mice induced with
malaria (15). Studies related sago worm still very

limited, so this study aim to observe the effect of
sago worm flour on albumin and Hemoglobin levels
in PEM model rats.
MATERIALS AND METHODS
True experimental pre-post control group
design with 24 male rats (Rattus norvegicus)
aged 4 weeks with 100 gr weight. Subject divided
into 4 group: K- (normal rats); K+(PEM rats
model); P1(PEM rats model with intervention of
0.36gr/100grBB sago worm flour); and P2(PEM
rats model with intervention of 1.36gr/100grBB
sago worm flour). Dose calculation of sago worms
based on lysin content and conversion of Laurence
and Bacharach table (16,17). Protein Energy
Malnutrition (PEM) rat model was made by feeding
with low protein (0%) for 14 days. Rats was PEM
if the albumin levels was <3 g/dL and Hemoglobin
levels was Hb<10 g/dL, hair loss, dull in color, and
the cornea is cloudy. The rats were given standard
feed of comfeed AD II 10gr/100grBB/day and ad
libitum water (18). Intervention of sago worm flour
given by 28 days with syringe. Sago worm flour
made by bake at 1000C then mashed and sieved
with an 80 mesh sieve. (19). Blood samples for
observe albumin and Hemoglobin levels were
obtained from plexus retroorbitalis. Albumin and
Hemoglobin levels were analyzed with DiaSys
kit. The manufacture of sago worm flour, animal
maintenance, treatment, sampling, and analysis of
albumin and Hemoglobin levels were carried out at
the Central Laboratory of Food and Nutrition Studies,
Gadjah Mada University, Yogyakarta.The ethical
clearance for the study obtained from Dr. Kariadi
Central Hospital Semarang with number No.111/
EC/H/FK-UNDIP/XI/2020. Statistical analysis using
Shaphiro Wilk then continued with One Way Anova.
Data with abnormal distribution were analyzed using
Kruskal-Wallis.
RESULTS AND DISCUSSIONS
Body Weight
Body weight is an anthropometric indicator
that used to assess nutritional status. Body weight

Effect of Sago worm flour (Rhynchhorus feirugineus) on Albumin and Haemoglobin in Protein Energy Malnutrition (PEM) ...

greatly influenced by food and nutrition because it
will affect the body condition (20). Adequate of food
and nutrition intake will increasing the body weight.

79

The increasing of rat body weight affected by the
feed intake and consumption.

Table 1. Rats Body Weight Before and After Intervention
Groups
KK+
P1
P2

Pre
Mean ± SD
122.29 ± 1.49
111.86 ± 1.34
112.14 ± 1.67
112.43 ± 1.90

Post
Mean ± SD
115.14 ± 2.34
120.71 ± 2.05
130.57 ± 1.98
138.00 ± 2.58
P: Paired t-test

Table 1 show the result of normality test for
rat body weight using Saphiro wilk test (p>0.05)
has normal distribution. The Paired t-test show the
different of rat body weight in the all groups. P2 group

Δ

P-Value

-7.15 ± 0.85
8.85 ± 0.71
18.43 ± 0.31
25.57 ± 0.68

0.007
0.008
0.000
0.026

(PEM rat model with intervention of 1.36g/100gBB
sago worm flour) show the increasing of body weight
on protein energy malnutrition rats model compared
with K+ group and P2 group. (25.57 gr).

180.00
160.00

Body Weight (g)

140.00
120.00
100.00
80.00

Pre

60.00

Post

40.00
20.00
0.00

K-

K+

P1

P2

Intervention Groups
Figure 1. Body Weight Comparation

Intervention with sago worm flour show the
increasing of rat body weight. The increasing
of body weight is the result of a growth process
at the cellular level which in affect to all body
components. In human, the largest organ growth
occurs in long bones, skeletal muscles, digestive
system, respiratory system, blood circulation
and blood volume. Child have early growth and
development of the brain, eyes, and ears. New
born baby has 25% weight of adult human brain.
At 2 years, brain develops up to 75% from adult

brain and at 10 years, the brain has 95% of
the adult brain. Lymphoid tissue has maximum
growth before adulthood and decreases with
age. Reproduction organs develop slowly in
preadolescence and significancy increasing in
adolescence. (21,22,23).
Nutrition has important role in growth and
development. Macronutrient like carbohydrate,
fat, and proteins are necessary in the process of
growth and development. Carbohydrate are the
main nutrients for supplying energy to body for

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Aleda Florince Oyay, Muchlis Achsan, Udji Sufro, Gemala Anjani, Vol 9 No.21, 2021: 21-28

carry out the activities. Carbohydrates needed
in every life cycle. In toddler, carbohydrates
needed due to the high level of children’s activity
and energy for brain development (24). Fat is an
energy storage in the body. Fat contains essential
fatty acid which have role in regulating nervous
system, strengthening cardiovascular system,
build up the immune system, and help the body
for absorb nutrients (25). Fat also play a role
for transporting and dissolving vitamins in the
body which will affect the toddler growth function
(26). Protein is a macronutrient for building the
tissue system. Body need the protein for growth,
building body structure like muscles, skin, and
bones, and tissue regeneration. Protein has the
most important value because it is related to life
processes. All living cells related to proteins.
Protein play a role for transporting nutrients from
digestive tract through the intestine walls to the
blood circulation (25).

Albumin Levels
Albumin is a water soluble protein that
synthesized in the liver and plays a role for maintaining
blood colloid osmotic pressure (6). Albumin has
a large molecular weight and shape, so it cannot
penetrate the vessels walls or capillaries and will help
to maintain fluid vascular system (9). Albumin is the
most abundant protein plasma in the human body,
55-60% of the measured protein serum (27). Albumin
plasma levels has correlated with protein storage
in the body. Decreasing of plasma albumin levels
indicates protein deficiency in the body. Albumin levels
measurements used to indicate nutritional and health
status for detecting the protein energy malnutrition
(PEM) (28). Intervention with sago worm flour show the
increasing of rat albumin levels. Normal albumin levels
in male Wistar rat is 3.0-5.1 g/dL (29). Intervention of
sago worm flour in PEM rat model proven to increase
albumin levels. High protein intake shows a tendency
towards better nutrition improvement in PEM rat model.

Table 2. Rats Albumin Levels Before and After Intervention
Groups

Pre (g/dl)

Post (g/dl)

Δ

P-Value*

K-

4.70 ± 0.08

4.59 ± 0.05

-0.11 ± 0.03

0.014

K+

1.13 ± 0.07

1.07 ± 0.06

-0.06± 0.01

0.022

P1

1.20 ± 0.07

3.86 ± 0.05

2.66 ± 0.02

0.975

P2

1.19 ± 0.09

4.19 ± 0.11

3.00 ± 0.02

0.001

P: Paired t-test

Table 2 show the albumin levels of rats with
sago worm flour intervention. Intervention with sago
worm flour show the increasing of rat albumin levels.
The result of the normality test for albumin levels in
rats using Shapiro wilk test show normal distribution
(p>0.05). Further test with Paired t-test show the

P2 groups (PEM rat model with intervention of
1.36g/100gBB sago worm flour) has the most
significant increasing of albumin levels (p=0.001).
Increasing of albumin levels in P2 groups is 3.00 g/
dL. Intervention of high dose sago worm flour show
an increase in albumin levels of PEM rat model.

Effect of Sago worm flour (Rhynchhorus feirugineus) on Albumin and Haemoglobin in Protein Energy Malnutrition (PEM) ...

81

Albumin Levels (g/dL)

6
5
4
3

Pre
Post

2
1
0

K-

K+

P1

P2

Intervention group
Figure 2. Albumin Levels Comparation

In Protein Energy Malnutrition (PEM) there is a
degradation of blood albumin levels. Albumin serum
levels are used as an indicator of severe protein
deficiency. PEM lead to hypoalbuminemia. Albumin
serum is the largest component in protein serum and
can be a marker for determining personal nutrition
status. The albumin serum concentration affected
by various factor like infection, trauma, hydration
status, hepatic function and renal disfunction
(11). PEM condition will affect the albumin serum
levels directly or indirectly. On directly pathway,
decreasing of protein synthesis will decrease protein
levels. Inadequate protein intake will aggravate the
condition. Protein amount in liver, gastrointestinal
system, kidney, and heart will decrease too. This
can ve exacerbated by changes of the intestinal
villi which cause protein absorption reduced (11).
Inadaquate protein intake will slow down the
synthesis of albumin mRNA and decreasing the
albumin serum levels. Indirectly decreasing albumin
serum levels commonly happened on stunting
children. In this condition there is an increasing
of oxidative stress and decreasing of immune
system. Oxidative stress will lead the damaged cell
in the body, including hepatic cells or hepatocytes.
Damage of hepatocytes will inhibits the production
of albumin that synthesized by liver cells (7).

Insects are an alternatives source of protein
that has ecological advantages in PEM (30). The
consumption of insect has been carried out by
African, Asian, and European communities to resolve
PEM (31,32). Insect cultivation has begun to become
a government program in Africana and Asian as a
source of animal protein. Intervention with sago
worm flour show significancy effect for increasing
albumin serum levels in PEM rat model. This
influenced by protein intake improvement. Papua
sago worm provides good benefits as a source of
protein in consumption patterns of Papuans (33,34).
Nutritional analysis of sago worm flour shown high
content of protein and antioxidant (15). Nutritional
content of sago worm flour is almost equivalent to
standard protein (Casein). It means that sago worm
flour can used to support growth and maintenance
of body tissue. In 100gr sago worm flour contains
10.39gr protein with bioavailability of 92%. Mono
unsaturated fatty acid (MUFA) contains 8.18gr
(dominated by 45% oleic acid), poly unsaturated
fatty acid (PUFA) contains 79gr (dominated by
linoleate acid), 43.25 μg/gr of α-tokoferol, 24–88%
magnesium and 29–34% zinc (14).
Hemoglobin Levels
Hemoglobin is main component of erythrocytes

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Aleda Florince Oyay, Muchlis Achsan, Udji Sufro, Gemala Anjani, Vol 9 No.21, 2021: 21-28

and a protein that contains a lot of iron. Hemoglobin
plays an important role in oxygen transport from
lungs to all of body tissues (35). Examination of

Hemoglobin levels is done to observe the anemia
status and PEM status that leading the decreasing
of nutrient status.

Table 3. Rats Hemoglobin Levels Before and After Intervention
Groups
KK+
P1
P2

Pre
Mean ± SD
14.32 ± 0.26
8.53 ± 0.36
8.86 ± 0.21
8.92 ± 0.18

Post
Mean ± SD
14.11 ± 0.25
8.31 ± 0.35
11.97 ± 0.45
13.18 ± 0.11

Δ

P-Value*

-0.21 ± -0.001
-0.22 ± -0.001
3.11 ± 0.24
4.26 ± -0.07

<0.001
<0.001
<0.001
<0.001

P : One Way Anova

Table 3 show the increasing of Hemoglobin
levels of PEM rat model with sago worm flour
intervention. P2 groups (PEM rat model with
intervention of 1.36g/100gBB sago worm flour)
has the highest increasing of Hemoglobin levels
(4.27 g/dL). The result of the normality test for

Hemoglobin levels in rats using Shapiro wilk
test show normal distribution (p>0.05). ANOVA
test show the significantly different between
intervention groups after sago worm flour
intervention compared with control groups (0.00
from p<0.05).

Haemoglobin Levels (g/dL)

16.00
14.00
12.00
10.00
8.00

Pre

6.00

Post

4.00
2.00
0.00

K-

K+

P1

P2

Intervention Groups
Figure 3. Hemoglobin Levels Comparation

Hemoglobin synthesis affected by availability
of iron and protein adequacy. Albumin levels in
blood circulation correlate with Hemoglobin levels.
Decreasing of albumin levels in blood circulation will
lead the decrease of Hemoglobin levels. It is correlate
because protein is one of important elements
that needed in Hemoglobin synthesis. When the
albumin levels in body was low. the Hemoglobin
synthesis will defected and lead the decreasing of

Hemoglobin levels in body. Protein in the form of
glycine amino acid and succinyl-coA are needed to
convert protoporphyrin to heme by interacting with
iron and ferrocelatase enzyme. Globin synthesis
need biotin amino acid. folic acid. vitamin B6.
and vitamin B12. To forming Hemoglobin. 4 heme
molecules that binding with 1 globin molecule are
needed (36). Iron and protein deficiency will lead the
disruption of Hemoglobin synthesis resulting anemia

Effect of Sago worm flour (Rhynchhorus feirugineus) on Albumin and Haemoglobin in Protein Energy Malnutrition (PEM) ...

and ultimately occurs PEM.
Apart material for building blocks of heme
and globin. protein is needed as iron transporter.
Iron that has been absorbed by intestinal mucosa
will transported in blood circulation with binding
protein. Binding of iron and protein called transferrin.
Transferrin is stored in liver, spleen, and spinal cord
for formation of red blood cells (eritropoiesis). When
protein intake was inadequate, the Hemoglobin
synthesis will disrupted. In the cells, iron interact
with electron transport protein chains that play role
in the final steps of energy metabolism. Proteins
remove hydrogen and electron form from energyproducing nutrient to bind oxygen and form to water
and produce ATP. Most of the iron storage are in
Hemoglobin and myoglobin in muscles. Protein
in form of transferrin can carrying iron. In the
inadequate protein intake, iron cannot be carried and
lead to disruption of Hemoglobin formation. This will
affect the iron absorption and transportation. (37).
CONCLUSIONS AND RECOMMENDATIONS
Intervention with 1.36gr/100grBW sago worm
flour increasing the body weight. albumin levels. and
Hemoglobin levels in PEM rat model significantly.
From the study. sago worm flour is expected to
be applied directly to improve the PEM condition
in toddler. Further research on the dosage of sago
worm flour still needs to be explored to complement
the research.
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