ISSN2434-2688 Asian Journal of Dietetics

Vol.3 No.1, 2021
Contents
Page T Title and authors
Special Topic1

The History of the Nutrition Improvement in Japan:
Japanese Nutrition Changed Food Policy into Nutrition Policy:
No. 3 in a Series
Teiji Nakamura

Special Report
3-6

School Meal Program:
Visit to a Japanese School Lunch: Perspective from a U.S. Registered
Dietitian Nutritionist, No. 1 in a Series
Emily A. Callahan

Originals Research
7-12

Nutritional Status and Nutritional Practice of Cirrhotic Patients at Hanoi
Medical University Hospital, 2020
Trang Thu Nguyen, An Tuong Bui, Linh Thuy Nguyen, Chinh
Tuyet Thi Pham, Oanh Hoang Vu, Shigure Yamamoto

Research Note
13-18

Free Drinking Water Provision at School Canteen and Sugar Sweetened
Beverages Consumption among Junior High School Students in Tomohon
City, Indonesia: A Cross-sectional Study
Ishak Halim Octawijaya, Windy Mariane Virenia Wariki, Ai Hori, Masao Ichikawa

Research Note
19-22

Investigation of Oral Lesion Outbreak among Two Boarding School Students in
Thimphu
Pratap Singh Tamang, Guru Prasad Dhakal, Gyan Prasad Bajgai, Vishal Chhetri,
Laigden Dzed, Hari Prasad Pokhrel

Research Note
23-27

Medical Nutritional Therapy for COVID-19 Inpatients
Basmawati B, Fadhlina AS, Nurul Farahanie Izzaty R, Siti Sarah Zakirah J,
Norazizah M, Noor Zarirah J, Lydianis B and Sarah Khalilah KHistory of the nutrition improvement in Japan
Special Topic: The history of the nutrition improvement in Japan
Japanese Nutrition Changed Food Policy into Nutrition Policy:
No. 3 in a series
Teiji Nakamura
The President of Japanese Dietetics/ President of Kanagawa University of Human Service
Like other Asian countries, Japan was
suffering from malnutrition due to poor foodconditions before and after World War II. Because of
the rice-dependent diet, carbohydrate intake was high,protein food intake was low due to poverty, andvitamins and minerals were lost through advances ingrain processing technology.
As a result ofmalnutrition, newborns and children had poor growthand development, were small in body size, were liable
to various diseases related to malnutrition and there
was a high incidence of infectious diseases such as
tuberculosis, and the average lifespan was short.
Nutrition was introduced from Europe andthe United States after the Meiji era helped to solvethese problems.
In particular, the nutrition
improvement carried out after World War II achieved
remarkable results. At that time, there was no food in
our country because of the war, and we had to rely onfood assistance from international institutions andcharities.
The main food supply was under
government control and the country provided food, but
it was not sufficient to provide the required nutrition.
Many people, knowing that it was illegal, got food on
the black market.
On the other hand, in the victorious UnitedStates, advances in agricultural technology had led toan excess of crops. The US government consideredselling this excess food to foreign countries, and thetarget was Japan, which was suffering from foodshortages. In 1954, a meeting was held between Japanand the United States on " the use of market
development costs associated with the acceptance of
surplus agricultural products in the United States. "However, there was no money in Japan to buy theseproducts, and it was difficult for Japanese people who
ate rice as their staple food to accept wheat bread anddairy products.
After discussions, the decision was made on
the condition that the US government could take overthe money that Japan purchases from American
farmers for a while and use part of the money topromote and spread imported food. In recent years,
some have argued that this was a long-term strategy towesternize the Japanese diet and make it dependent on
American agricultural products. However, the only
way to survive the severe hunger of the time was torely on imported food from abroad. In particular,
nutritionally inadequate Japanese food with highly
nutritious Western food was an effective means ofresolving malnutrition. Furthermore, the important
point is that advertising funds were provided topromote unfamiliar imported food among theJapanese.
Japan actually provided nutritional
education to resolve malnutrition, although it was said
that this was advertising expense for the United States.
In other words, the Japanese government
with the money for advertising expenses, bought a" Kitchen Car" in which the rear part was converted

into a kitchen for cooking demonstration, anddietitians boarded and provided nutrition education to
every corner of Japan. This kitchen car is not a Food
Truck that provides meals that can be seen in the
United States, but a special car that can provide
nutrition education that also serves as a cooking
demonstration (photo).

Kitchen Car in Japan

Food Truck in American“ The Kitchen Car” is a nutrition education
car that also serves as a cooking demonstration, and isdifferent from the “ Food Truck” , which is an
American mobile restaurant. Nutrition improvementin Japan is characterized by the fact that it is based on
nutrition education.

Corresponding author: nakamura-t@kuhs.ac.jp1Asian Journal of Dietetics 2021
Special Report: School Meal Program
Visit to a Japanese School Lunch: Perspective from a U.S. Registered Dietitian Nutritionist
No. 1 in a Series
Emily A. Callahan
Owner, EAC Health and Nutrition, LLC
As a U. S. Registered Dietitian Nutritionist living
in Japan, I was excited to have an opportunity to visit
a Japanese elementary school and experience its lunch
program. The program originated following WorldWar II, and has since developed impressively andachieved global recognition for its putative roles inpromoting health and helping to maintain therelatively low obesity prevalence among Japaneseyouth. Perhaps the most noteworthy feature of theJapanese school lunch program is that its purview goesbeyond the management and nutritional aspects of thefood served to encompass ( and even emphasize)
integration of the school meal into children’ s
educational, social, and cultural experiences. The
purpose of this article is to share specific examples ofthis integration and inspire colleagues in the UnitedStates to consider how aspects of this program may beemulated in order to improve the health and the foodand nutrition literacy of youth in the United States.
My Japanese school lunch visit was made possible
through a connection with Shigeru Yamamoto, PhD,
RD, Director of the Asian Nutrition and Food Culture
Research Center at Jumonji University, where he isalso Professor of International Nutrition. With animpressive academic career spanning more than 40
years, he is currently highly involved in promoting theJapanese school lunch program.
The visit was hosted by Nobitome Elementary
School in the city of Niiza, northwest of Tokyo. Threeof Dr. Yamamoto’s graduate students in nutrition, twofrom Taiwan and one from Vietnam, also joined thevisit.
Our guide for the afternoon was Ms. Yamaguchi,
the school dietitian and nutrition teacher (Photo 1). In
Japan there is a law with a provision stating that a
dietetics and nutrition teacher is to give children
practical guidance regarding the school lunch. Everyschool in Japan employs a school dietitian/ nutrition
teacher. School dietitians may hold a Nutrition
Teacher License, which requires similar training asteachers of other subjects. A dietitian can obtain thelicense after accumulating 3 years of experience
working in a school and 8- 10 lecture credits. In 2014
there were more than 12,000 school dietitians; about
4,700 of those were also nutrition teachers.
Before entering the school, we changed out of ourshoes into slippers. In Japan, shoes are not worn inside
the home nor in some restaurants and other publicbuildings. Upon entering the school of 650 students,
we were greeted with signs welcoming us in Chinese,
Vietnamese, and English (Photo 2), as well as origami
art featuring our native flags (Photo 3).
Our first stop was a peek into the kitchen to see thestaff preparing homemade dashi (broth) in largecauldrons, using local vegetables and dried anchovies(Photo 4). Off to the side, racks of serving dishes
decorated with small pictures of fruits and vegetables
were piled into carts (Photo 5).

Photo 1: Me (second from right) with the graduate
students and Ms. Yamaguchi

Photo 2 (left): Welcome signs in the languages of thevisitors; Photo 3 (right): Origami art prepared by thestudents, featuring the flags from the visitors’ native
countries.

Photo 4 (left): School lunch workers preparing dashi(broth). Photo 5 (right): Serving dishes ready for thelunch meal.
After the glimpse into the kitchen, Ms.
Yamaguchi led us to the library to share some of her
teaching practices and materials while we sippedgreen tea. As the only other English speaker, Dr.
Yamamoto kindly served as my interpreter for most of
the conversation and to explain the content themes ofthe materials we were reviewing. Ms. Yamaguchi
explained that the school meal teaches children how
to make healthy food choices and embeds food andnutrition education including agricultural practices,
food production and distribution, cultural traditions,and more in other academic subjects. For example:• Geography and science: students may calculate
the distance that the meal’s ingredients traveled toreach their plates, as well as the amount of fuel used
and its effects on the earth’s ecology.

Corresponding author: emily@eachealthandnutrition.com

3Experiencing a Japanese school lunch• Biology: students chart their height and weight
and learn about the nutritional contributors to their
growth.
• English: students learn English words related tothe daily menu, such as the names of foods, cooking
methods, table manners, nutrients, etc.
The emphasis on integrating the school meal into
children’s formal educational environment isexpressed in the concept of shokuiku (pronounced“show-coo-EE-coo”), a Japanese word meaning foodand nutrition education. The Japanese national
Shokuiku Basic Act became law in 2005 and in 2008
school curriculum guidelines were revised to include
provisions related to the promotion of shokuiku.
One of Ms. Yamaguchi’s responsibilities is todevelop more than 200 menus for the school year.
The menus must satisfy not only nutritional
requirements but also student tastes and local andnational food traditions and culture. Nutrition
standards were established based on Japan’s national
nutrition surveys and recommended dietary reference
intakes. A school lunch must provide one-third ofdaily nutrient needs, except for some nutrients withdaily requirements that are more difficult to achieve(such as fiber); those nutrients are therefore provided
in larger amounts. Photos 6 and 7 show examples of ameal calendar for Nobitome Elementary School. The
calorie and protein content for each meal are listed at
the bottom right of each box.

know what the children are eating. This also provides
an interesting and common topic for family
conversation. Many schools also post the daily lunchmenu on the school’s website, along with children’scomments about the meal. When a certain meal proves
to be very popular, Ms. Yamaguchi prepares a note on
the recipes used and sends it home with each student(Photo 8).

Photo 8: Example of one of Ms. Yamaguchi’s recipe
notes from a popular lunch menu.
Menus incorporate seasonal foods from local
producers as much as possible. Packaged andprocessed foods are not commonly used in the meals.
Sometimes meals even incorporate vegetables
harvested earlier that day. Ms. Yamaguchi assembles
a display of the ingredients (even the seasonings!)
used in the day’s lunch, labeled with the name andlocations of the producers who supplied them. Photos
9, 10, and 11 are the display from my visit day.

Photo 6 (top): Example of a monthly meal calendar for
Nobitome Elementary School; Photo 7 (bottom): A
closer look at the menu for the day of the visit(December 9, 2015).

Photos 9, 10, 11: Display of the ingredients used in
the lunch meal on the day of my visit.
Local food producers are invited to visit theschool and explain their trade to students. Students
also visit food producers and become familiar with

Menu calendars are delivered to each student’s
family one month in advance so that family members
4Asian Journal of Dietetics 2021
how food is produced. This broad perspective on foodand nutrition and connection with food producers
helps instill in children a sense of gratitude and respect
for the food they are eating as well as an appreciation
for and interest in its origins. This practice may also
be a contributor to the remarkably low levels of foodwaste reported by many schools.
After our discussion about meal ingredients, we
joined a fourth-grade class for lunch. The students
were excited to have visitors, and had prepared acolorful welcome mural for us on the chalkboard.
After introducing ourselves to the students andhearing about their favorite foods, it was time to eat.
My own childhood experiences with school
lunch had formed my expectation that we would eat ina cafeteria, so I was surprised as the classroom quickly
transformed into a convivial setting for the meal. Aftera quick trip to the hallway sinks to wash our hands, thestudents quickly rearranged their desks and spread out
colorful napkin cloths while the teacher put on music.
The fruit and vegetable dishes I’d seen in the
kitchen earlier were rolled into the classroom
alongside serving trays holding delicious-smelling
food. A subset of students quickly donned blue
sanitary smocks, hair caps, and cloth face masks as
they took their places to dish up the meal for theirclassmates (Photo 12).

experience (Photo 15).

Photo 13 (left): The lunch meal on the day of the visit:
milk, rice, miso soup, and tuna with vegetables andpeanuts; Photo 14 (right): Close-up of the tuna dish.
When everyone finished eating, the clean-up was
executed as quickly as the set-up. Each student helped
stack dishes and flattened their milk cartons. Allaround the room, I heard students saying “gochisosama deshita,” a Japanese expression of thanks for agood meal (literally, “it was a feast”).
Ms. Yamaguchi explained that for the entire
school (approximately 650 students), food waste
averages around two cups per meal.
Before we departed, the students serenaded us
with “The 12 Days of Christmas” in English as well as
their school anthem, then we posed for a group photo(Photo 16).
As we prepared to leave the classroom, dozensof origami figures appeared from inside the desks andwere pressed into our hands as parting gifts (Photo 17).

Photo 12: The lunch line in a fourth-grade classroom.
As is typical throughout Japan, younger children
do not bring their own lunches from home. All thestudents are served the same meal, and à la carte
options and vending machines are not usuallyavailable. Municipalities provide funding for thelunch program’s labor costs, and parents/guardians ofstudents pay for the food, an average $2.50/day USD.
The students waited until everyone had been
served before they began eating. When everyone’s
meals had been placed at their desks, one student went
to the front of the room and with clasped hands and aslight bow led everyone in a chorus of “Itadakimasu!,”a common Japanese phrase spoken at the start of a in”
or “bon appétit,” but it also conveys an offering of
thanks to the chef and to those who produced theingredients, as well as an expression of gratitude forthe food itself. The essence of the word is related to
the Buddhist principle of respect for all living things;
Buddhism is a prevalent religion in Japan.
The meal included milk, rice with lightseasoning, miso soup with mixed seasonal vegetables,and maguro (a type of tuna) in a light breading andsauce with vegetables and peanuts (Photo 13). It was
all delicious, but the tuna was my favorite (Photo 14).
Overall, the meal was a thoroughly enjoyable

Photo 15: Here I am enjoying the meal with Dr.
Yamamoto and some of the students.

Photo 16: The students and visitors.

5Experiencing a Japanese school lunch
On the way to our last stop at the school, theprincipal’ s office, Ms. Yamaguchi paused in the
hallway where carts of used serving dishes from eachclassroom were waiting to be rolled back to the
kitchen for cleaning. Any uneaten food from thestudents’ dishes is placed back in the serving dishes sothat it can be inventoried daily. As Ms. Yamaguchi
pulled the lid off each serving dish, I was stunned tosee how little food waste remained (Photo 18).
In the principal’s office, we were served anotherround of green tea as we discussed current events
influencing the school lunch. One of the discussion
topics was related to the fact that funding for the 2020
Olympics (to be hosted in Tokyo) and funding for theschool lunch program was housed in the samedepartment of the Ministry of Education. Hosting the
Olympics would be costly, and there was speculationthat the school lunch program funding would be
reduced as a result. As part of the effort to prevent thisconsequence, Dr. Yamamoto’ s research center
published a collection of short articles and essays
about the school lunch program on the Asian Nutrition
and Food Culture Website in hopes of increasing theJapanese public’s and policymakers’ recognition of ofthe value and significance of the program. Positive
comments from foreigners will help make their efforts
even more compelling.
The visit made clear to me that the Japanese
school lunch program is commendable both for thequality of the food and the integration of the meal into
the broader educational milieu. The program is truly
outstanding in the context of global attempts to
structure school settings and meals to cultivate
students’ knowledge and interest in food and nutrition,
improve their health, and foster lifelong healthfuleating habits.

Photo 17: The students presented the visitors withorigami gifts at the end of the visit.

Photo 18: Example of a near-empty serving dish froma classroom at the school.

6

Asian Journal of Dietetics, 2021
Original Research

Nutritional Status and Nutritional Practice of Cirrhotic Patients at Hanoi Medical
University Hospital, 2020

Trang Thu Nguyen1*, An Tuong Bui1, Linh Thuy Nguyen1, Chinh Tuyet Thi Pham1,
Oanh Hoang Vu1, Shigure Yamamoto2
1

Hanoi Medical University, 1st Ton That Tung, Dong Da district, Hanoi, Vietnam
Nutrition and Food Culture Research Center, Jumonji University, Saitama, Japan

2

ABSTRACT Background and purpose. Liver cirrhosis (LC) is one of the leading causesof mortality worldwide. Malnutrition frequently imposes a burden on patients with LC,
and it is an independent predictor of lower survival. As a result, it is essential to manage
LC patients' nutritional status and dietary intake for better treatment. However, inVietnam, there are limited data regarding this issue. This study aimed to describe thenutritional status, dietary intake, and nutritional practice of cirrhotic patients at Hanoi
Medical University Hospital (HMUH) in 2020. Method. A cross-sectional study was
conducted among 40 patients who were admitted to the HMUH from December 2019 toApril 2020. For nutritional status assessment, body mass index (BMI), subjective global
assessment (SGA) questionnaire, and muscle strength by handgrip strength (HS) were
measured. The 24-hour dietary recall method, as well as some open questions, were alsocollected for the nutritional practice assessment. Results. The prevalence of malnutrition
determined by BMI was 12.5%; however, the rate was remarkably high from SGA with
60% and from HS with 75%. The mean energy and protein consumption per ideal bodyweight (IBW) were 24.6 ± 12.0kcal/IBWkg and 1.0 ± 0.5g/IBWkg, respectively.
Moreover, 40% of the patients claimed that they restricted animal protein. The
percentage of study’s patients who had ≥4 meals/day and who ate a late evening snack
was only 32.5% and 22.5%, respectively. As for those who took an LES, the averageenergy, carbohydrate, and protein in this study were only 140kcal, 19g, and 5.1g
respectively. Conclusion. The prevalence of malnutrition in LC patients determined by
SGA and HS was remarkably high. Considering this result, HS rather than BMI is areliable, non-invasive, and effective tool for malnutrition assessment for cirrhotic
patients in Vietnam’s clinical settings. Consequently, the mean dietary intakes of LC
patients were lower than the recommendation; therefore, nutritional education and a lateevening snack diet need to be provided to LC patients.
Key words: Cirrhosis, nutritional status, dietary intake, nutritional practice.
INTRODUCTION
Liver cirrhosis (LC) is one of the leading causesof mortality worldwide, and it is associated with asignificant reduction in disabilities- adjusted lifeyears. In the report of Global Health Estimates( 2016) , LC was the 11th most common cause ofdeath each year in the world with 2. 1% of total
deaths(1). According to Institute for Health Metrics
and Evaluation ( IHME) , in 2019, LC ranked 7th
among the top 10 most common causes of death inVietnam with a 47. 3% increment from 2009 to2019( 2) . The etiologies of LC are most commonly
alcohol, hepatitis B, hepatitis C, and non- alcoholic
fatty liver disease or sometimes autoimmune
hepatitis. Alcoholic liver disease and hepatitis B are
the most common causes in most parts of Asia ( 3) .
According to the report of the World HealthOrganization (WHO) on hepatitis B in Vietnam, it isestimated that the number of cases of hepatitis Brelated decompensated cirrhosis was 90,704 in 2017and is projected to increase 10% by 2030( 4) .
Cirrhosis is defined as the histological developmentof regenerative nodules surrounded by fibrous bands
in response to chronic liver injury, which leads toportal hypertension and end- stage liver disease. In
the asymptomatic phase of the disease, usuallyreferred to as compensated cirrhosis, patients may
have a good quality of life, and the disease may
progress undetected for several years.
Thedecompensation phase is regularly marked byascites, gastrointestinal bleeding due to esophageal
varices, hepatic encephalopathy ( HE) , and jaundice(5).
Malnutrition is frequently a burden in patientswith LC; it is usually related to the clinical stage ofchronic liver disease, increasing from 20% inpatients with well-compensated disease to more than
60% in patients with advanced cirrhosis ( 6) .
Malnutrition and muscle mass loss ( sarcopenia) areassociated with a higher rate of complications suchassusceptibility
toinfections,
hepatic
encephalopathy ( HE) , and ascites, as well as being
independent predictors of lower survival in cirrhosis
and in patients undergoing liver transplantation ( 7).
Various mechanisms are considered to contribute tomalnutrition in cirrhosis such as poor oral intake,increased intestinal protein loss, decrease protein
synthesis, disturbances in substrate utilization,________________________________________________________________________*To whom correspondence should be addressed:
trangnn27@gmail.com

7

Nutritional status and nutritional practice of cirrhosis patients
hyper-metabolism, and malabsorption(8). Therefore,
assessment of nutritional status is essential toincrease the number of recovering cases anddecrease the mortality rate. It is recommended by the
ESPEN guideline that subjective global assessment( SGA) should be used as a “ gold standard” formalnutrition assessment in LC patients ( 6) . In
addition, handgrip strength ( HS) is a reliable, noninvasive, and cost- effective tool to identify
malnutrition in cirrhotic patients ( 9) . However, inmany of Vietnam’ s practical clinics, body index
mass ( BMI) is still widely used for nutritional
assessment though it can be inaccurate due to ascites
and/or edema in LC patients. As a consequence, theprevalence of LC patients in Vietnam has not beenwell-studied.
There has been controversy over the years about
the amount of protein intake for LC patients with theold concept restricting the intake in order to limit thesynthesis of ammonium and the deamination ofprotein to aromatic amino acids especially in patientswith HE. However, malnourished and sarcopenic
cirrhotic patients can experience protein depletion.
Increased protein intake is generally well tolerated
and safe in cirrhotic patients and ameliorates protein
anabolism as shown in previous studies ( 10, 11) .
According to ESPEN's clinical nutrition practiceguideline for LC patients in 2019, cirrhotic patientswith conditions of increased energy expenditure ( i.
e. acute complications, refractory ascites) or
malnutrition should ingest an increased amount ofenergy (30-35 kcal/kg/d of energy and 1.2-1.5 g/kg/dof protein ( 6) . Nonetheless, in Vietnam’ s clinicalsetting, a restricted protein-diet is still recommended
for LC patients (12).
In addition, several guidelines haverecommended short periods of starvation with 4 - 6
meals a day, as well as a 50g carbohydrate and/ or
15g protein- containing late evening snack thanks to
its benefits to the level of serum albumin, liver
enzyme, and nitrogen balance (7, 8, 13, 14). Hence,patients’ practice with regard to food intake is also
necessary for the investigation of an adequate supplyof food and monitoring food consumption. With
Vietnam’ s climbing number of new LC cases, it is
crucial to evaluate the nutritional status andnutritional practice of these patients; however, there
have been relatively limited studies on this issue. For
these reasons, we decided to conduct this study todescribe the nutritional status, dietary intake, andnutritional practice of cirrhotic patients at Hanoi
Medical University Hospital in 2020.

morbid conditions requiring dietary modification
and restrictions for different reasons except fordiabetes, hypertension, dyslipidemia, ( c) patientswith medical conditions that would prevent
understanding for food record and/ or providing
answers or anthropometric measurements. In theend, 40 patients were enrolled in the study.
Data collection. All the questionnaires were filled
out by investigators. The investigators weredietitians who were trained to collect study data. The
included information in this study is listed below.
Demographic data. The data were collected frommedical records, caregivers, and subjects.
Nutritional status assessment. Bodyweight andheight were measured in light clothing and without
shoes. Body mass index (BMI) was computed as theratio of weight (kg) per height squared (m2). A BMI<18.5 kg/m2 was considered underweight. 8 patientswith ascites and/ or edema were excluded from BMI
evaluation. Subjective global assessment ( SGA)
questionnaire was also conducted. Patients with
SGA classification A were labeled as wellnourished, and patients with classification B and C
were labeled as malnourished ( 16) . Handgrip
strength ( HS) is a non- invasive, simple, and quick
method that has been used for the assessment of
nutritional status especially because malnourishedpatients present with lean mass depletion and low
muscle strength. Low handgrip strength is suggested
as <26 kg for men and <18kg for women (17).
Nutritional practice. Assessment of individual
patients’ oral energy and protein intake wasdetermined by 24 h diet recall one day before their
hospitalization. The average intakes of energy andprotein were recorded in calories and grams per day
and grams per ideal body weight ( IBW) per day,respectively. In addition, a 7-day food frequency andsome open questions regarding nutritional practicewere also collected.
Data analysis. Input data were entered into REDcap
software. Stata version 15. 0 was used for data
analysis. Data were expressed as mean ± SD,
median, interquartile range ( IQR) . For comparisonof categorical variables, chi-square was used, and forcontinuous variables, Student’ s t- test and Wilcoxon
sign rank test were used, as appropriate. The
probability level of p < 0. 05 was set for statisticalsignificance.
RESULTS
The total participants of the study were 40
patients, of which 35 ( 87. 5% ) were males and 5(12.5%) were female. Figure 1 shows the prevalenceof malnutrition according to BMI was 12.5% (4/32);
at the same time, from HS 75% ( 30/ 40) of thepatients were malnourished, and from SGA 60%(24/40).
The mean energy and protein consumption
based on IBW were 24.6 ± 12.0kcal/IBWkg and 1.0± 0.5g/IBWkg (Table 1), respectively. Furthermore,males’ intake was higher than females’, though only
the protein index was statistically significant.
Regarding vitamins, dietary vitamin B1 was
1 . 2 mg/ d. As for mineral intake, the mean intake ofiron from meals was 9.6mg/d and the median intake
of zinc was 8.0 mg/d.

METHODS
Settings and sample. A cross- sectional study was
conducted from December 2019 through April 2020
at Hanoi Medical University Hospital ( HMUH) , a
general hospital in Vietnam. All the newly admitted
patients ( within 0- 24 hours) who met the inclusion
criteria: (a) diagnosed with cirrhosis of any etiology( alcoholism, hepatitis C, cryptogenic/ NAFLD,
autoimmune), (b) age 18 or over, and (c) agreeing toparticipate in this study were included in this study.
The exclusion criteria involved: (a) patients with HE,
active gastrointestinal bleeding, acute liver failure,
hepatocellular carcinoma, (b) patients with other co-8

Asian Journal of Dietetics, 2021

Malnourished100.0%
90.0%
80.0%
70.0%
60.0%
50.0%
40.0%
30.0%
20.0%
10.0%
0.0%

Well-nourished

25.0%
40.0%
87.5%
75.0%
60.0%
12.5%
BMI (n=32)

HS (n=40)

SGA (n=40)

Fig 1. Nutritional status of LC patients by different methods *8 patients with edema and/or
ascites were excluded from BMI evaluation
In general, the mean intakes of energy, protein,vitamins, and minerals by malnourished patients andwell- nourished patients classified by BMI and HS
were not significantly different (Table 2).

Nevertheless, in SGA classification, the mean
intakes of energy, protein, carbohydrate, lipid, iron,and zinc by well- nourished patients weresignificantly higher than by malnourished patients.

Table 1. Dietary intake of LC patients (N = 40)
Total
ESPEN guidelines2019 Vietnamese recommendation 2016
Mean ± SD
Median (IQR)

Dietary intake
Energy (kcal/IBWkg)

24.6 ± 12.0

25 -3530 -35

Protein (g/IBWkg)

1.0 ± 0.5

1.2-1.5

Carbohydrate(g/IBWkg)
Lipid (g/IBWkg)
Fiber (g/d)
Fe (mg/d)

4.0 ± 0.350-60% of total energy

Compensated: 1.0-1.2
Decompensated: 0.8-1.0
50-60% of total energy

0.45 (0.3; 0.6)
5.6 (2.4; 7.7)
9.6 ± 5.7-

Zinc (mg/d)

8.0 (5.3; 11.4)-

Vitamin B1 (mg/d)

1.2 (0.7; 1.6)-

15-25% of total energy
20-30
Male: 7.9mg/day
Female: 6.7mg/day
Male: 10.0mg/day
Female: 8.0mg/day
Male: 1.2mg/day
Female: 1.0mg/day

IBW: Ideal body weight; *p<0.05

Table 2. The dietary intake of LC patients as their nutritional status
BMI (n=32)
Dietary intake

Malnourished(n = 4)Well-nourished(n = 28)

HS (n = 40)

SGA (n = 40)

Malnourished Well-nourished(n = 30)(n = 10)

Malnourished Well-nourished(n = 24)(n = 16)

Mean ± SD; Median (IQR)
Energy (kcal/IBWkg)

19.0 ± 7.3

28.4 ± 2.0

24.2 ± 1.8

25.9 ± 5.4

19.4 ± 2.1

32.4 ± 2.5*

Protein (g/IBWkg)

0.8 ± 0.3

1.1 ± 0.1

1.0 ± 0.1

1.1 ± 0.2

0.8 ± 0.1

1.3 ± 0.1*

Carbohydrate (g/IBWkg)

2.8 ± 1.0

4.7 ± 0.3

3.9 ± 0.7

4.0 ± 0.4

3.2 ± 0.4

5.3 ± 0.4*

Lipid (g/IBWkg)

0.4 (0.1; 0.8)

0.5 (0.4; 0.6)

0.45 (0.3; 0.6)

0.49 (0.1; 1.0)

0.4 (0.2; 0.5)

0.6 (0.4; 0.8)*

Fiber (g/d)

1.7 (1; 5.1)

6 (4.1; 7.8)

5.1 (3.0; 7.6)

6.0 (2.4; 7.8)

4.8 (1.7; 7.4)

6.1 (4.2; 7.7)

Fe (mg/d)

8.5 ± 6.7

11.1 ± 5.1

9.3 ± 5.0

10.5 ± 7.6

8.2 ± 5.4

11.8 ± 5.6*

Zinc (mg/d)

5.3 (3.6; 10.3)

7.3 (5; 10.7)

10.5 (5.5; 15.1)

5.9 (3.3; 9)

11 (8.2; 13.5)*

Vitamin B1 (mg/d)

1.2 (0.6; 1.7)

9.4 (6.5; 11.5)
1.4 (1.1; 1.7)

1.1 (0.7; 1.6)

1.6 (0.3; 1.6)

1.1 (0.6; 1.6)

1.3 (1.1; 1.6)*

8 patients with edema and/or ascites were excluded from BMI evaluation.

9

Nutritional status and nutritional practice of cirrhosis patients
Figure 3 reveals that only 32.5% of patients had≥4 meals/day and the number of respondents who
had a late-evening snack (LES) was only 9 (22.5%).
Moreover, the mean energy, carbohydrate, andprotein of the late-evening snack were 1 4 0 . 4 ±60.7kcal; 19.1 ± 9.0g; 5.1 ± 2.5g respectively (Table
3)

Figure 2 shows that alcohol, animal protein, andfat/ oil had the highest number of patients who wererestricted in eating them: 67. 5% , 40% , 35% ,respectively. Meanwhile, LC patients reportedly
increased their intake of vegetables ( 25% ) , fruits( 37. 5% ) , and dairy ( 40% ) , and only 5% increased
legumes. Most of the patients continued their intake
of starch ( 87. 5% ) and confectionery/ soft drinks(77.5%).

Percentage of patients

Unchange
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%

7.5
5

Restricting/Not consuming

5
0

10

Increasing

0

0
25

35

15

37.5

40

5

2.5

57.5

57.5

7.5

40

7.5

67.5

95

87.5

77.5

67.5

65
50

32.5

Fig 2. Nutritional practice characteristics of LC patients after being diagnosed with LC (N = 40)
No

LES

Yes

77.5%

≥4 meals

22.5%

67.5%

0%

10%

20%

30%

40%

32.5%

50%

60%

70%

80%

90%

100%

Fig 3. The number of meals/day that LC patients had and late-night snacks (LES) (N = 40)

Table 3. The energy intake of the late-evening snacks (LES) (n = 9)
MaleFemaleAll(n = 7)(n = 2)(n = 9)Energy (kcal)
151.7 ± 65.1
101 ± 11.3
140.4 ± 60.7

p
0.33

Carbohydrate (g)19.0 ± 10.4

19.6 ± 1.6

19.1 ± 9.0

0.94

Protein(g)5.8 ± 2.4

2.7 ± 1.6

5.1 ± 2.5

0.13

should be used for LC patients instead of BMI (6, 7).
Unlike BMI, which is only considered about
patients’ anthropometry, SGA is relied on not only
the aforementioned but also the process of losing
weight,patients’
dietary
decrement,
hypermetabolism, and clinical symptoms also ( 16) .
However, in most Vietnamese hospitals, BMI is themain method of malnutrition screening and

DISCUSSION
With the increasing burden of liver diseases on
the world’ s and Vietnam’ s mortality, proper
nutrition for hepatic patients has become a challenge,
in order to achieve that appropriate nutritional
assessment methods are also needed. In many
international guidelines, SGA is considered as the“ gold standard” for nutritional assessment and10

Asian Journal of Dietetics, 2021
assessment for LC patients. In this study, as per
SGA, 60% of Vietnamese LC patients weremalnourished; however; as per BMI, only 12.5% of
patients were found to be undernourished. This result
was similar to Huisman and et al.’s study in 2011, in
which the prevalence of malnutrition was 5% bymodified BMI for ascites and/ or edema patients,
58% by SGA, and 67% by HS ( 18) . Furthermore,
75% of patients had impaired HS, a reliable, noninvasive, and cost- effective tool to identify
malnutrition in cirrhotic patients ( 9, 19) . The mean
HS in this study was 20. 7 ± 7. 92kg ( based on the
Asian Working Group for Sarcopenia ( AWGS)
criteria) , in which the means for males ( 21. 5 ±7. 98kg) and females ( 15. 2 ± 5. 19kg) were both
below the cut- off value ( <26 kg for males and <18
kg for females) , so their handgrip strength wasclassified as low (17). The mean value of HS in thisstudy was roughly equal to that of D. K. Daphneeand colleagues (20.2 ± 7.9kg), which was used as thestudy's cut- off point, and 99% of patients wereconsidered to have impaired HS (9). The correlation
between HS and mortality is expected, as reduced
intake is associated with reduced body protein mass
and affects muscle function (19). Given these points,
SGA and HS are considered to be the recommended
assessment methods of malnutrition for LC patients
rather than BMI in Vietnam’s clinical facilities.
Despite the high prevalence of malnutrition,
the calorie intakes of LC patients were lower than therecommended calorie intake ( 24. 6 ± 12. 0kcal/ kg/ d
vs 35kcal/ kg/ d of energy) from ESPEN's latest
clinical nutrition practice guideline for LC patients( 2019) ( 6) . Cirrhotic patients are usually in
conditions of increased energy expenditure as
cirrhosis is a catabolic disease, possibly associatedwith hypermetabolism ( 6) . The fact that mostpatients had low- calorie intake confirms what theliterature has shown, that chronic liver disease
patients have a decreased food intake due to thedisease’ s symptoms and dietary restrictions. The
mean total daily energy intake of LC patients in thisstudy was quite the same as a study in 2017 by D.K.
Daphnee and et al. on 93 LC patients ( 1445. 9 ±727.7kcal/d and 1540.7 ± 309.3kcal/d) (9).
The mean protein intake per ideal body weightof the study’ s subjects ( 1. 0 ± 0. 5g/ IBWkg) was
lower than ESPEN’ s recommendation ( 1. 2 –1. 5g/ IBWkg) ( 6) . In the past, there has been
controversy about whether patients who had
advanced cirrhosis or HE should undergo a transient
restriction in protein intake, in order to limit thesynthesis of ammonium and the deamination ofprotein to aromatic amino acids. However, increased
protein intake is generally well tolerated and safe incirrhotic patients and ameliorates protein anabolism,
as shown in previous studies ( 10, 11) . Thus, therecommended protein intake in patients with adiagnosis of liver cirrhosis is 1. 2– 1. 5g/ kg. BW/ d toprevent loss of muscle mass and reverse muscle loss
in those who are sarcopenic( 6, 7) . However, inVietnam’ s clinical practice, LC patients’ protein
intake is still recommended within 0. 81.2g/kg.BW/d (12). Considering the high prevalenceof impaired HS, a sign of sarcopenia, it is essential
to reconsider the protein intake recommendation for
Vietnamese LC patients in future studies.
Nonetheless, the low intake of protein can be theresult of low energy intake; therefore, it is possiblethat LC patients with a proper energy intake canconsume more protein. In future studies, how toincrease energy and protein intake in Vietnamese
LC’s patients needs to be addressed.
As for the minerals, reduced zinc levels arequite common in cirrhotic patients, especially thosewith an alcoholic origin. Zinc deficiency leads tohyperammonemia, anorexia, and altered taste, which
contributes to decreased intake and consequentmalnutrition. In contrast to zinc, iron intake incirrhotic patients needs to be treated cautiously as
their iron regulation may be disturbed, andoverdosing on iron could result in poisoning.
However, the dietary iron of the study's respondents
was higher than the RDA in both genders. This result
can be due to the fact that the proportion of red meat
( like beef and pork) and seafood ( like fish,
shrimp… ) in their meals was high. Furthermore,
vitamin B1 is also most likely to be reduced in liverdiseases. This study’ s subjects’ intakes of vitamin
B1 intake met the requirement.
On analyzing dietary restriction patterns, 35%of the respondents were restricting fats in their diet.
This figure was higher in the study of Nguyen Thanh
Liem ( 2013) , in which almost all the subjects had agood practice of restricting fat (83.3%) and avoiding
greasy food (95%) (20). 67.5% of participants had agood practice of restricting alcohol. While only 5%of patients claimed to increase the intake ofvegetable protein like beans and legumes, 40% of thepatients reported that they restricted their animal
protein intake as they believed that protein, in
general, was harmful to the liver. In any case, themean intake of protein by the current study’s patientswas still below the recommendation, which can becaused by the over- restriction of protein. When
asked the reason for doing so, the answer was
because of the advice of their relatives, friends,
and/ or from the media. As a result, nutritional
education is ensured to deliver the correct
information to the patients.
Not only is meal composition important, butalso the number of meals that LC patients eat, which
is preferably from four to six meals per day withthree main meals and three snacks, especially a lateevening snack ( LES) . A meta- analysis proved that
LES intervention helped to improve liverbiochemical parameters for albumin, ammonia, andprothrombin time, and liver enzymes including
aspartateaminotransferase
andalanineaminotransferase ( 21) . LES also decreased skeletal
muscle proteolysis ( 14) ; therefore it may help toreverse sarcopenia. In addition, increasing thenumber of meals can also help to increase theamount of dietary intake in LC patients. In asystematic review, Tsien et al. recommended a
200kcal with 50g carbohydrate late evening snack tominimize gluconeogenesis and preserve muscle
mass (14), as well as 15g of protein(13). However,the practice of this aspect is poor among the study’ s
patients as most of the subjects believed that a
nocturnal snack would make them gain more fat
mass and overwork their liver, as night is the time
for the liver to rest. As for those who ate a LES, theaverage energy, carbohydrate, and protein in thisstudy were only 140kcal, 19g, and 5.1g respectively,
which were lower than the recommendation, and ina cohort study in Japan ( 22) . In a Vietnamese
hospital, the nutritional intervention regimen for LC
patients consists only of 3 main meals ( breakfast,
lunch, and dinner) . Owing to this fact, in future11

Nutritional status and nutritional practice of cirrhosis patients
studies, it is necessary to estimate the effect of an
appropriate LES on Vietnamese LC patients’ dietaryintake, nutritional status and liver function.
There were several limitations in this crosssectional study. The dietary intake of patients wascollected by the 24- hour recall for only 1 day;however, a 7-day food frequency was used to help toreduce the non- representativeness. Moreover, thesample size of the study was limited due to theimpact of the Covid19 pandemic.
In conclusion, the prevalence of malnutrition
in Vietnamese LC patients was remarkably highfrom SGA with 60% and from HS with 75% .
Considering this result, HS is a reliable, noninvasive, and effective tool for malnutritionassessment for cirrhotic patients in Vietnam’ sclinical settings rather than BMI. Consequently, themean dietary intakes of LC patients were lower than
the recommendation with many Vietnamese LC
patients restricting their protein intake, while few ofthem ate a late- evening snack. In future studies,appropriate nutritional management with a lateevening snack included in the menu to increase
dietary intake needs to be provided to LC patients.

1)
2)

3)

4)

5)
6)
7)

8)

9)

10) Nielsen K, Kondrup J, Martinsen L, Døssing H,
Larsson B, Stilling B, et al. Longterm oral
refeeding of patients with cirrhosis of the liver.
Br J Nutr. 74(4):557-567. 1995.
11) Swart GR, Zillikens MC, van Vuure JK, vanden Berg JW. Effect of a late evening meal on
nitrogen balance in patients with cirrhosis of
the liver. BMJ. 299(6709):1202-1203. 1989.
12) Huong Thi Le, Nguyet Thi Phuc Tran. Dinhdưỡng lâm sàng – tiết chế, Nhà xuất bản Y học.
2016.
13) El-Kalla FS, Mansor LO, El-Bassat HA,
Mishaal S, Attia JF. The effect of a lateevening protein-containing snack on nitrogenbalance in cirrhotic patients. Tanta Med J.
42:47-52. 2014 .
14) Tsien CD, McCullough AJ, Dasarathy S. Lateevening snack: exploiting a period of anabolic
opportunity in cirrhosis. J Gastroenterol
Hepatol. 27(3):430-441. 2012.
15) Ministry of Health and National Institue of
Nutrition. Recommended dietary allowances
for Vietnamese. 2016.
16) Detsky, A.S., McLaughlin, J.R., Baker, J.P.,
Johnston, N., Whittaker, S., Mendelson, R.A.,
Jeejeebhoy, K.N. What is subjective global
assessment of nutritional status? JPEN J
Parenter Enteral Nutr. 11(1):8–13. 1987.
17) Liang-Kung Chen, Li-Kuo Liu, Jean Woo, et al.
Sarcopenia in Asia: consensus report of the
Asian working group for sarcopenia. JAMDA.
15(2):95-101. 2014.
18) Huisman, E.J., Trip, E.J., Siersema, P.D., vanHoek, B., van Erpecum, K.J. Protein-energy
malnutrition predicts complications in livercirrhosis. Eur J Gastroenterol Hepatol.
23(11):982–989. 2011.
19) Alvares-da-Silva, M., Silveira, T. Hand-grip
strength or muscle mass in cirrhotic patients:
who is the best? Nutrition. 22(2):218–219.
2006.
20) Liêm N.T., Mai H.X. Khảo sát thực hành dinhdưỡng và một số yếu tố liên quan của bệnhnhân xơ gan tại khoa nội tiết tiêu hoá bệnh việnđa khoa trung ương Cần Thơ. Y học thực hành.
12(899):28-30. 2013.
21) Chen, C.-J., Wang, L.-C., Kuo, H.-T., Fang, Y.C., Lee, H.-F. Significant effects of lateevening snack on liver functions in patientswith liver cirrhosis: A meta-analysis ofrandomized controlled trials. J Gastroenterol
Hepatol. 34(7):1143-1152. 2019.
22) Hanai, T., Shiraki, M., Imai, K., Suetsugu, A.,
Takai, K., Shimizu, M. Late evening snackwithbranched-chain
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supplementation improves survival in patientswith cirrhosis. Journal of Clinical Medicine.
9(4):1013.20.

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http://www.healthdata.org/Vietnam.
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Van Thi Thuy Nguyen, Quang Dai Tran, Anh
Thu Nguyen, et al. Estimates and projection of
disease burden and economic analysis forhepatitis B in Viet Nam. Journal of Viral
Hepatitis. 2018.
Schuppan, D., & Afdhal, N. H. Liver cirrhosis.
Lancet. 371(9615):838–851. 2018.
Plauth M, Bernal W, Dasarathy S, et al. ESPEN
guideline on clinical nutrition in liver disease.
Clin Nutr. 38(2):485-521. 2019.
European Association for the Study of theLiver. European association for the study of theliver: EASL clinical practice guidelines onnutrition in chronic liver disease. J Hepatol.
70(1):172–193. 2019.
Maharshi, S., Sharma, B.C., Srivastava, S.
Malnutrition in cirrhosis increases morbidity
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30(10):1507–1513. 2015.
Daphnee, D.K., John, S., Vaidya, A., Khakhar,A., Bhuvaneshwari, S., Ramamurthy, A.
Handgrip strength: a reliable, reproducible,
cost-effective tool to assess the nutritional
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53. 2017.

12

Asian Journal of Dietetics, 2021

Research Note
Free Drinking Water Provision at School Canteen and Sugar Sweetened Beverages Consumption among
Junior High School Students in Tomohon City, Indonesia: A Cross-sectional Study
Ishak Halim Octawijaya1*, Windy Mariane Virenia Wariki2, Ai Hori3, and Masao Ichikawa3
1

Graduate School of Comprehensive Human Sciences, University of Tsukuba, Ibaraki, Japan
Faculty of Medicine, Sam Ratulangi University, North Sulawesi, Indonesia
3
Faculty of Medicine, University of Tsukuba, Ibaraki, Japan
2

ABSTRACT Background: Globally, concerns are raised about sugar-sweetened beverages(SSBs) as a risk factor for child obesity. In Indonesia, SSBs are commonly sold at schools while
drinking water is hardly available for free. We investigated whether students in schools withfree drinking water consume less SSBs at schools than their counterparts. Methods: We
conducted a questionnaire survey, incorporating food frequency questionnaire, among 813
students in seven junior high schools with and without free drinking water at school canteen in
the city of Tomohon, North Sulawesi Province. We compared their SSB consumption at schools
with and without drinking water, using Mann Whitney U test or chi square test. The availability
and sale of SBBs were also compared between schools with and without drinking water.
Results: The proportion of students who reportedly drink SSBs at school at least once a day
was not lower in schools with drinking water than in schools without drinking water, and so
was the daily frequency of SSB consumption among daily SSB consumers. The number of SSB
brands and varieties sold at school appeared to be higher in schools with drinking water thantheir counterparts. Conclusions: There was no difference in SSBs consumption among students
between schools with and without free drinking water. To reduce their SSB consumption at
schools, it may be necessary to provide alternative drinks or to restrict the sale of SSBs at
schools.
Keywords: Drinking water; Sugar- sweetened beverages; Junior high school; Adolescent;Obesity
INTRODUCTION
Globally, there have been growing concerns aboutsugar-sweetened beverages (SSBs) as a risk factor forchild obesity ( 1- 3) . While overall sugar intake isepidemiologically and clinically proven to trigger
obesity and other metabolic adverse events such as
high blood pressure and insulin resistance, theinfluence of sugars from SSBs is greater than thosefrom solid foods because SSBs contain higher
concentration of fructose than solid foods ( 4) . SSBs
promotes energy intake efficiently because it isavailable in liquid form and easy to consume. Despite
such characteristics and potential health effects of SSB
consumption, SSBs are widely available andaccessible to children in any countries or regions
irrespective of their income levels.
In Indonesia where the prevalence of obesity( BMI > + 2 standard deviation above the median)among adolescents has largely increased in the recent
past (by eight-fold from 0.6% in 1996 to 4.9% in 2016),
the government has addressed the risk of excessive
sugar intake among children through their SSB
consumption at school ( 5- 7) . In schools, SSBs andbottled water are available at an affordable price forstudents. On the other hand, tap water available inschools is only for washing hands, since it is not safe
to drink unless properly boiled ( 8) . This situation
prompts students to drink SSBs. Yet, there isnoregulation to restrict the sale of SSBs at schools to
date. According to the Global school-based student*

health survey in 2015, 28% of Indonesian students
consume soft drink once or more daily (9).
Studies in the Western countries reported that theprovision of drinking water at schools was effective toincrease water consumption and to reduce overweight
among students (10-12). In Indonesia, a few schools or
food vendors in the schools voluntarily provide freedrinking water for students. If students in such schools
consume less SSBs at schools than those in the schools
without drinking water, the provision of free drinking
water at schools would be a sound approach to fightagainst child obesity in Indonesia as well. In thepresent study, we therefore tested this hypothesis
among junior high school students in the city of
Tomohon in North Sulawesi Province, Indonesia.
METHODS
Study Setting and ParticipantsThis study was conducted in Tomohon City,
North Sulawesi Province, Indonesia. The city has
105,000 residents in 2018, with 23% aged below 15
years (13). The majority of the population in the city isProtestant ( 73% ) , while the most of Indonesian
population is Moslem (87%) (14-15). In 2017 academic
year, there were 22 junior high schools with 5822
enrolled students in the city. Notably, the prevalenceof obesity among junior high school students in thecity is much higher than that of the whole country(10.4% vs. 2.5% in 2013) (16-17).
In Tomohon City, junior high schools start at 7
AM and finish around 1 PM with two recess timearound 9 AM and 11 AM. In the schools, school

Corresponding author: ishak.halim109@gmail.com

13

Drinking Water at School and Students’ SSBs Consumption

breakfast or lunch program is uncommon, and most of
schools provide foods and beverages through foodvendors, where students can purchase foods andbeverages freely during school recess time or after
school.
The study was designed to describe school foodenvironments in all 22 junior high schools in the city,and to investigate dietary intake and body mass index( BMI) among students ( 18) . The sample size wascalculated to estimate the proportion of students
consuming SSBs once per day or more in Tomohon
City to be 32. 3% , following the School- based oral
health survey guideline (19-20). Given 80% response
rate and design effect of two, the required sample size
turned to be 840. To achieve this sample size, we
selected eight schools, using systematic sampling by
urban/rural classification, district of the city, and thesize of school, and recruited all 9th graders in theselected schools. The study was approved by theinstitutional review board of Sam Ratulangi
University in Indonesia and the University of Tsukuba
in Japan.
In the present study, we used the cross-sectional
data from 813 participants in seven of eight selectedschools to investigate whether students in the schools
providing drinking water for free at canteen consumed
less SSBs at schools than those in the schools without
free drinking water. One school was excluded because
SSBs were not sold in the school.
Data Collection
Data collection was conducted by the first author
between July and October 2017 on typical school days
among students with a written informed consent ofboth students and their parents. We asked students tofill out self- administered questionnaires in theclassroom to provide information about theircharacteristics and dietary intake. At the same time, wemeasured their body weight and height. To obtain
information about schools and the food vendors, weinterviewed school principal (or designatedteacher/staff) and vendors who sell foods regularly at
school. We also observed the vendors to identify what
were sold. For data collection, we visited schools
twice, and students and vendors who were absent
during our visits were excluded from the study.
Measurements(1) School characteristics
School characteristics include type of school( public/ private) , number of students, availability ofwater server in the classroom, provision of freedrinking water at canteen, and the number of beverage
brands and varieties sold in school. Beverages wereclassified into SSBs and water. Some schools had
water servers in the classrooms, but they were not free,
and the installation of water servers depended on eachclass. Users have to pay for the water-refill fees to use.
(2) Student characteristics and SBB consumption
Student characteristics include sex, age, bodyheight, body weight, socioeconomic status, frequencyof and daily allowance for food purchase at school,and physical activity. Socioeconomic status wasmeasured with the Family Affluence Score III, which
has been validated in a previous study in Indonesia(21). The total score ranges from 1 to 13, where thehigher score indicates higher socioeconomic status.
Regarding physical activity, we asked the number ofdays per week students were engaged in moderate tovigorous- intensity physical activity for at least 60
minutes.

Body weight and height were measured using abody weight scale and a stadiometer with graduationof 0. 1 kg and 0. 1 cm, respectively. Students were
wearing school uniform during weight measurement,so the approximate weight of school uniform wasdeducted from the measured weight. We calculated
body mass index (BMI) by dividing the square of bodyweight (kg) by body height (m). Obesity, overweight,
and thin are defined as z-score > 2 standard deviation(SD), 1SD < z-score ≤ 2SD, and z-score < -2SD frommedian, respectively, according to the WHO child
growth standard for boys and girls (WHO, 2007) (2223).
SSB consumption was evaluated using a foodfrequency questionnaire ( FFQ) separately for
consumption at school and outside school. FFQ
assesses the consumption of beverages during
previous 30 days with 9 levels of frequencies: ( 1)almost never; (2) one to three times per month; (3) once
per week; (4) two to four times per week; (5) five to six
times per week; (6) once per day; (7) two to three times
per day; (8) four to six times per day; (9) more than six
times per day, which was converted to the frequencyof daily consumption (i.e., 0, 0.07, 0.1, 0.4, 0.8, 1.0, 2.5,
5.0, and 6.0, respectively) (24). For the present study,
we developed the FFQ among 43 junior high schoolers
in Tomohon City through three- day inconsecutive
food records (two school days and a weekend day).
Analyses
First, we compared school and student
characteristics between schools with and without freedrinking water at canteen (as shown in Table 1 andTable 2, respectively) . Then, we compared SSB
consumption among students in schools with andwithout free drinking water at canteen (as shown in
Table 3). Specifically, we compared the proportion of
students who consumed SSBs at least once a day atschool and outside school and among those who
consume SSBs every day, we compared the dailyfrequency of SSB consumption at school and outsideschool.
For the comparisons between students in theschool with and without drinking water, we performed
Mann Whitney U test, t test, or chi square test,
depending on the type of the variables to be compared.
We showed effect size of Spearman’s rho (ρ), Pearson’sr, and phi ( φ) or Cramer’ s V for these tests,
respectively. Effect size of 0.2 for ρ, r, φ, and Cramer's
V indicates a practically significant effect (25).
RESULTS
1. School characteristics
Table 1 compares the school characteristics
between two schools with free drinking water atcanteen and five schools without it. One of the twoschools and one of the five schools were publicschools. The median number of students in schools
with and without free drinking water was 376 and 229,
respectively. The number of SSB brands and varieties
sold was much higher in schools with free drinking
water than in schools without it. Such clear difference
between the schools with and without free drinking
water at canteen was not seen in the brands andvarieties of water.
2. Student characteristics
In the schools with and without free drinking
water at canteen, 251 and 562 students in the 9th grade
completedthequestionnaire
surveyandanthropometric measurements. Table 2 compares theircharacteristics. The proportion of male students was
14

Asian Journal of Dietetics, 2021

higher in the schools with free drinking water (58%)
than in the schools without it (45%). Mean body weight,
height and BMI of the students were similar between
the schools, though the proportion of overweight andobese students was higher in the schools without freedrinking water (29%) than in the other schools (23%).
Based on the effect size, there was no difference
between the schools in students’ characteristics
including their family affluence, daily food allowance,
food purchase at school, and physical activity.

Table 1. Characteristics of schools with and without free drinking water at canteen

Number of public schools

Free drinking water at canteen
Available
Not available(2 schools)(5 schools)
11

Number of students per school (median [range b])

376

Total number of students across schools
Number of schools providing water server insome classrooms
Number of beverage brands/varieties sold inschool (median [range b])
SSBs

751

2011

1

2

22

[19, 25]

2[1, 8]

Water
Number of beverages sold per day per 100
students (median [range b])
SSBs

1[1, 1]

1[1, 2]

61[55, 67]

15[6, 57]

Water
22
Daily sale of beverages per student (USD a)(median [range b])
SSBs
0.21
Water
0.01
a
USD 1 = IDR 13,574.00 (as of October 1st, 2017)b
Range shows minimum and maximum value of a variable[18, 26]

19[4, 47][0.18, 0.24][0.01, 0.01]

0.04
0.01

[0.02, 0.04][0.00, 0.11][374, 377]

229

[134, 1188]

Table 2. Student characteristics of schools with and without free drinking water at canteen
Free drinking water at canteen
Available
Not available
Effect(251 students)(562 students)
size a
Φ
n
%
n
%
Male
146
58.2%
254
45.2%
-0.120Female
105
41.8%
308
54.8%
Cramer’s
Child growth standard b
V
Normal
187
74.5%
392
69.8%
0.068
Overweight
31
12.4%
98
17.4%
Obese
26
10.4%
60
11.7%
Thin
7
2.8%
12
2.1%
Mean
(SD c)
Mean(SD c)
R
Height (cm)
156.9
(7.1)
156.3
(7.2)
0.038
Weight (kg)50.9
(11.1)
51.2(12.6)-0.012
BMI c (kg/m2)
20.6
(4.0)
20.9
(4.3)
0.026
Median[IQR c]Median[IQR c]Ρd
Family affluence score
5.0[4.0, 7.0]
6.0
[4.0, 8.0]
-0.149Daily food allowance (USD e)
0.88[0.74, 0.88]
0.88[0.74, 1.47]
0.040
Food purchase at school (days/5 school days)
4[3, 5]
4[3, 5]-0.01960 mins or more PA (days/week)3[2, 5]
3[2, 5]-0.034aEffect size of 0.2 indicates a practically significant effect; b Based on the WHO child growth standard, thin,
normal, overweight, and obese are defined as z-score < -2SD, -2SD ≤ z-score ≤ 1SD, 1SD < z-score ≤ 2SD, z-score> 2SD from median, respectively; c SD: standard deviation, IQR: interquartile rage, BMI: body mass indexdFamily affluence score ranges from 1 to 13; e USD 1 = IDR 13,574.00 (as of October 1st, 2017)15

Drinking Water at School and Students’ SSBs Consumption
school with and without drinking water ( 57% and
55% , respectively) . Among those who drink SSBs
every day, the daily frequency of SSB consumption
at school and outside school was also similar
between the schools with and without drinking water.
Based on the effect size, there was no difference
between the schools in students’ SBB consumption.

3. SSB consumption
Table 3 compares students’ SSB consumption
between the schools with and without free drinking
water at canteen. The proportion of the students whoreported to drink SSBs at least once a day in theschool was higher in the schools with free drinking
water (40%) than in the other schools (34%), while this
proportion outside school was similar between the

Table 3. SSB consumption among students in schools with and without drinking water at canteen
Drinking water at canteen
Available
Not available
Effect size a(251 students)(562 students)
n
%
n
%
φ
Once or more daily SSB consumption
184
73.3%
390
69.4%
0.040
At school
100
39.8%
193
34.3%
0.053
Outside school
142
56.6%
308
54.8%
0.016
Median[IQR]Median[IQR]ρFrequency of daily SSB consumption of
2.5[2.5, 5.0]
2.5
[2.5, 2.5]
0.033
those who consume SSBs every day
At school
1.0[1.0, 2.5]
1.0
[1.0, 1.0]
0.141
Outside school
1.0[1.0, 2.5]
1.0
[1.0, 2.5]
0.094
aEffect size of 0.2 indicates a practically significant effect.
DISCUSSION
We found no discernable difference in SSB
consumption among students regardless of freedrinking water provision at their schools. This is
somewhat contradictory to the findings in the Westerncountries that the provision of drinking water atschools would increase water consumption among
students (10-12). In our study setting, it is possible that
SSB consumption was not replaced by free drinking
water because the sale of SSBs at schools was not
restricted. In fact, previous studies reported that when
SSBs and drinking water are both available, students
tend to choose visually colorful SSBs because it isthought to be more thirst quenching than plain drinking
water (26-27).
The impact of free drinking water provision on
SSB consumption, if any, might have been cancelled
due to the variety of SSBs sold. In fact, SSBs sold inthe schools with free drinking water were more various
than their counterparts. Previous studies show thathaving more varieties of SSBs in vending machine
results in a higher number of SSBs sold (28-29).
However, our study did not find such a relationshipthat more various SSBs sold in schools, more SSB
consumption among students. This finding implies thatstudents would consume SSBs irrespective of thevariety of SBBs sold as long as SBBs are sold at
schools.
To reduce sugar consumption from SSBs among
students, it may be necessary to offer a healthier drinks
at schools or totally ban the SBB sale. One option is toprovide school feeding with low-fat milk or drinking
water. Reportedly, school feeding can reduce students’purchase of snacks and SSBs (30). Besides, low-fat milk
without added sugar has the same thirst-quenchingeffect as SSBs, and it will be a good calcium source(31). Another option is to allow SSBs with less sugar
content to be sold at school. It might not reduce theconsumption of SSBs, but it might potentially reducesugar intake from SSBs while having the same thirstquenching effect as regular SSBs (27). Ultimately, theban of selling SSBs at school will prevent students to
consume SSBs at school, but further investigation of
its impact toward SSB consumption outside school
should be kept in mind.

We acknowledge several limitations of this study.
First, there is a lack of information on the amount andcalorie content of SSBs students consume at school.
We asked students to report only the frequency of SSB
consumption based on a food frequency questionnaire.
With this information, however, we could estimate theproportion of students who daily consume SSBs at
school. Moreover, SSBs are sold in PET bottles (350 to
500 ml) or sealed cups (200 to 500 ml) at school, so thisrange of the amount is roughly consumed for one
purchase. Second, we could not validate FFQ
developed in this study. Still, self-report dietary survey
tool like FFQ is useful to rank the tendency of
predefined food (or food group) consumptions (32-33).
In this study, FFQ was used to measure theconsumption frequency of SSBs, which thencategorized into more frequent and less frequent SSB
consumption by cut-off of once per day consumption.
Also, we chose this self-reporting method over foodobservation or other methods because it was the mostfeasible to obtain data of a long-term SSB consumption
from a large sample (34).
The findings of this study may not be
generalizable to other regions of Indonesia, and in thiscross-sectional study, we are uncertain whether theprovision of free drinking water at schools has any
impact on SSB consumption among students. Yet, thelessons learned from this study should be still relevant
to other regions or even beyond the country, because
SSB consumption among children is highly prevalentglobally.
In conclusion, there was no difference in SSB
consumption among junior high school students
between schools with and without free drinking water
available at school canteen. To reduce their sugar
intake through SSB consumption at schools, it isnecessary to investigate the impact of providing
alternative drinks or restricting the sale of SSBs at
schools.
ACKNOWLEDGEMENTS
We would like to thank Mr. Jimmy Eman, Mayorof Tomohon City, dr. Deesje Liuw, Head of Tomohon
City Health Office, Dr. Juliana Karwur, Head of
Tomohon City Education Office, Dr. Makiko
16

Asian Journal of Dietetics, 2021

Sekiyama of the National Institute of Environmental
Studies (Japan), and Mr. Daichi Suzuki of Josai
International
University(Japan)for
theiradministrative and technical support.

13) Health Office of Tomohon City. Tomohon City
Health Profile 2018 (in Indonesian).
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2017(inIndonesian).
<https://tomohonkota.bps.go.id/statictable/2019/01/11/389/ju
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09/07/2019).
15) BPS - Statistics Indonesia. Nationality, ethnicity,religion, and daily language of Indonesia Citizen ( in Indonesian) . https: / / www. bps. go. id/ publication/ 2012/ 05/ 23/ 55eca38b7fe08
30834605b35/ kewarganegaraan- suku- bangsaagama- dan- bahasa- sehari- hari- penduduk- indonesia> (accessed 18/03/2020).
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Dietary Intake Among Junior High SchoolStudents in Tomohon City, Indonesia. J Acad
Nutr Diet 118(10): A164. 2018.
19) Ministry of Health Republic of Indonesia,
Ministry of Education, World HealthOrganization, U.S. Centers for Disease Control
and Prevention. Global school-based student
health survey: Indonesia, outside Java andSumatra 2015 fact sheet.
20) Association of State & Territorial Dental
Directors. Guidance on selecting a sample for aschool-based oral health survey. <https://www.
astdd.org/docs/school-survey-sampling-guidancejuly-2017.pdf> (accessed 07/02/2019).
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Jakarta, Indonesia: The roles of gender andfamily income. Public Health Nutr 19(15):27602768. 2016.
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to 19 years (z-scores).
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Double burden of malnutrition in rural West
Java: Household-level analysis for father-childand mother-child pairs and the association withdietary intake. Nutrients 7(10):8376-8391. 2015.
25) Ferguson CJ. An effect size primer: A guide forclinicians and researchers. Washington, DC, US:
American Psychological Association 301-310.
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26) Clydesdale FM, Gover R, Fugardi C. The effectof color on thirst quenching, sweetness,
acceptability and flavor intensity in fruit punch
flavored beverages. J Food Qual 15(1):19-38. 1992.
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Peterson KE. School vending machine use andfast-food restaurant use are associated with sugarsweetened beverage intake in youth. J Am Diet
Assoc 106(10):1624-1630. 2006.

FUNDING AND CONFLICT OF INTEREST
There is no financial support and conflict ofinterest regarding this study.
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Multi-National Study. Nutrients 8(12):770. 2016.
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18

Asian Journal of Dietetics, 2021

Research Note
Investigation of Oral Lesion Outbreak among Two Boarding School Students in Thimphu
Pratap Singh Tamang1, Guru Prasad Dhakal1, Gyan Prasad Bajgai1, Vishal Chhetri2,
Laigden Dzed3, Hari Prasad Pokhrel4*

Jigme Dorji Wangchuck National Referral Hospital, Thimphu, Bhutan
Royal Center for Disease Control, Thimphu, Bhutan
3
Nutrition Program, Ministry of Health, Thimphu, Bhutan
4
Gidakom Hospital, Ministry of Health, Thimphu, Bhutan
12

ABSTRACT Background: The objective of the study is to determine the cause of oral lesion
outbreaks among boarding school students and provide proper clinical diagnosis and treatment.
Methods: This was a retrospective descriptive study. Data was collected from the affectedstudents during our visit to the schools. Participants were students who had reported of various
oral lesions including glossitis in two schools of Thimphu district. A total of 105 students who
had oral lesions and glossitis were screened and provided symptomatic treatment. Around 20
students who had severe lesions were sent for blood investigation inclusive of C-reactive
protein and micronutrient assays for serum iron, ferritin, folate and cobalamin. Oral swabs werecollected and cultured to rule out any fungal growth. All the students were treated
symptomatically with B-Complex multi-vitamin, analgesics and with amoxicillin in suspectedbacterial super imposed infection. The students were followed up after 2 weeks and 4 weeksof the first visit. Results: Over two-third (70%) of the severely affected students were female
and all blood investigation parameters were normal except for one student who had serum
micro-nutrients level below the normal range. Microbial culture of oral swab did not isolate
any pathogenic organism. All students reported improvement during the first visit and most
students had recovered during the second visit with symptomatic treatment. Conclusion: Allstudents reported improvement during the first visit and most students had recovered during
the second visit with B-Complex multi-vitamin supplementation. Although the investigation
was inconclusive, it strongly points towards riboflavin deficiency which is supported byglossitis outbreak investigation literature from various settings. The investigation recommends
conducting a prospective study taking account of all the important micro-nutrients to establish
the exact cause of deficiency.
Keywords: Oral lesions, glossitis, schools, students
on the dorsal surface of the tongue most commonly
which keeps changing in its color, size and position(5, 6). BMG has variable presentation and isasymptomatic in most cases . Very rarely it isassociated with systemic diseases and psoriasis (7).
Atrophic glossitis (AG) is characterized by the partial
or complete absence of filiform papillae on thedorsum of the tongue. It is caused by nutritional
deficiencies for a prolonged duration like riboflavin,niacin, pyridoxine, vitamin B12, folic acid, iron, zinc,and vitamin E. Helicobacter pylori (H. Pylori)
infection, fungal infections, dry mouth and othermetabolic diseases can also cause atrophic glossitis(8-11). Studies have also reported the association ofglossitis as heredity, allergy, hormonal factors, andsmoking and in association with syndromic diseases(7, 11, 12).
In the present study, students of two boarding
schools in Thimphu district of Bhutan had been
suffering from different types of oral lesions andglossitis for some time. Interestingly, lesions occurred
within a few months after they come to school (AprilMay and September-October every year). This has
been happening for past 2 years and got more severein 2019 with some students requiring treatment andeven hospitalization. Reports from school authorities
and Ministry of Education indicate that it affected

INTRODUCTION
Oral health is an integral part of general health. It
d o es n o t p o se a m ajo r m o r tality th r eat b u t it
substantially influences the general health and wellbeing of an individual (1). Mouth is the only gateway
to the body and everything we eat or drink has to passthrough it (2). Oral diseases are highly influenced byindividual’s belief, attitude, knowledge, skills, dietary
habits, nutritional status, environment and day to day
living practices (3). Oral hygiene is not perceived as
an important procedure in most parts of the world
including Bhutan and it is made worse by the inability
to carry out normal daily procedures such as
performing proper oral hygiene practices like toothbrushing or cleaning teeth and tongue due to various
oral lesions and glossitis (4).
Oral lesions can be anything in the mouth that is
not normal, an ulcer or breach on the mucosa etc.
Glossitis is inflammation of the tongue generally
characterized by redness and swelling. There are two
major types; Benign Migratory Glossitis (BMG) andAtrophic Glossitis (AG) (5, 6). BMG or erythemamigrans is an inflammatory condition characterized
by focal areas of depapillation of filiform papilla. It
is usually surrounded by an area of erythema or
hyperkeratosis, resulting in a ‘‘map-like’’ appearance*

Corresponding author: hari88pokhrel@gmail.com
19

Glossitis Outbreak Investigation among Boarding School Students in Thimphu
only boarding students and they improved during
school vacations (13, 14). Over the years, it has
become a concern for both the Health and Education
Ministries (15). However, there is limited knowledge
on the topic in the country. This study aimed todetermine the cause of oral lesion outbreaks amongboarding school students and provide proper clinicaldiagnosis and treatment.

bacterial super imposed infection. The students were
followed up after 2 weeks and 4 weeks of the first visit.
Ethical clearance was granted by the Research Ethics
Board of Health (REBH), Ministry of Health, Bhutan.
Data Management and Analysis
Data collected was double entered and validated
using Epi- Data version 3. 1 and analyzed using
Microsoft Excel.
The characteristics of theparticipants are presented as frequencies, percent,mean and standard deviation (SD).

METHODSThis is a retrospective descriptive study. Data
were collected from the students during visit to theschools. Participants were students who reported ofvarious oral lesions including glossitis in two schoolsof Thimphu district in Bhutan. A total of 105 students
who complained of different oral lesions and glossitis
in these two schools were screened by Oral Medicine
Specialist. Twenty students presenting with severe
oral lesions were sent for various blood tests inclusiveof C-reactive protein (CRP), and micronutrient assays
for serum iron, ferritin, folate and cobalamin. Oralswab samples were collected and cultured to rule out
any fungal growth. All the students were treated
symptomatically with vitamin B- Complex multivitamin, analgesics and with amoxicillin in suspected

RESULTS
The mean age of students was 15. 8 years ( SD:
1. 8) and 70% of the severely affected students werefemale. Microbial culture of oral swab did not isolate
any pathogenic organism (Table 1).
Blood investigation findings are being presented
in table 2. All the parameters were normal except for
one female student who had serum micro- nutrients
level below the normal range ( Ferritin; 8. 9 and Iron
8. 6) . All students ( 100% ) reported improvement
during the first visit while most ( 88. 6% ) of thestudents had recovered during the second visit withsymptomatic treatment (Figure 1) which indicates thatthe outbreak was caused by micro-nutrient deficiency.

Table 1: Descriptive (n=20)
Category

Variables
Age

Frequency

Percent

≤ 15
11
55
≥ 16
9
45
Mean: 15.8, SD: 1.8, Minimum 13, Maximum 20
GenderMale
Female

6
14

30
70

Oral Swab Culture: Pathogenic organism not isolated
SD: Standard Deviation
Table 2: Blood Serum Parameters (n=20)
Parameter
Normal Range
MeanSD
CRP (mg/dl)
<0.6
0.2
0.5
B12 (pg/ml)
130-700
498.8
218.3
Folate (ng/ml)
5.0-20
16.3
4.7
Ferritin (ng/ml)
F:13-150; M 30-400
40.9
26.8
Iron (mg/dl)
F:39-149; M;40-168
93.0
45.3
CRP: C-reactive protein, SD: Standard Deviation, F: Female, M: Male

Number of Students

120

Minimum
0.0
246.5
11.3
8.9
8.6

105
93

100
80
Improvement
Recovery

60
40
20

12
0

0
1st Follow up

2nd Follow up

Figure 1: Improvement and recovery during follow up visits (n=105)

20

Maximum
2.0
988.4
20.0
107.3
212.9

Asian Journal of Dietetics, 2021

4)
DISCUSSION
Students responding to B-Complex multi-vitaminsupplementation indicates that the outbreaks could
possibly be linked to micro-nutrient deficiencies. Past
studies conducted in boarding schools have reported
that that over 90% of the boarding school students
were deficient in thiamine (16) and around 64% had
deficiency of cobalamin (17). An investigation ofmeals provided in feeding schools across Bhutan
found that meals had inadequate amount of proteinsand micro-nutrients (18).
To address the huge burden of micronutrient
deficiencies, fortified rice was introduced in feeding
schools towards end of 2017. The rice was fortified
with eight micronutrients (Vitamin A, vitamin B1, B3,
B6, B9 and B12, iron and zinc) (19). Since the oral
lesion / glossitis symptoms improved/reduced with
Vitamin B complex supplementation, vitamin B2(riboflavin) was suspected as the most likely cause ofoutbreaks as fortified rice lacked riboflavin but ispresent in vitamin B complex. Glossitis outbreak
investigations conducted in different countries
indicated that the outbreaks could be linked toriboflavin deficiency (20-22) Riboflavin deficiency is
associated with glossitis, oral ulceration, hyperemia
and swelling of mouth and throat, angular stomatitis
and cheilitis. The main sources of riboflavin are meatand dairy products. Smaller amounts are also present
in different cereals, food grains, seeds and green leafy
vegetables (23).

5)
6)
7)

8)

9)

10)

LIMITATIONS
Due to urgency of the work, the investigation
could not wait for resource mobilization thus, small
sample size was a big limitation. The investigation
also could not conduct serum assays of important
micro-nutrients such as thiamine and riboflavin.

11)

12)
CONCLUSION
All students reported improvement during the first
visit and most students had recovered during thesecond visit with B-Complex multi-vitaminsupplementation. Although the investigation wasinconclusive, it strongly points towards riboflavindeficiency which is supported by glossitis outbreak
investigation literature from various settings. The
investigation recommends conducting a prospective
study taking account of all the important micronutrients to establish the exact cause of deficiency.

13)
14)
15)

1)

2)

3)

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Madraa E, Chandia AB, et al. (2013) Suspected
Outbreak of Riboflavin Deficiency among
Populations Reliant on Food Assistance: A Case
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2009– 2010. PLoS ONE 8( 5) : e62976. https: / /doi.org/10.1371/journal.pone.0062976.
23) Malnutrition EtPHSoM. Evaluating the Public
HealthSignificanceofMicronutrient
Malnutrition, 2018.

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Asian Journal of Dietetics, 2021
Research Note
Medical Nutritional Therapy for COVID-19 Inpatients

Basmawati B, Fadhlina AS, Nurul Farahanie Izzaty R, Siti Sarah Zakirah J, Norazizah M,
Noor Zarirah J, Lydianis B and Sarah Khalilah K
Dietetic & Food Service Department, Hospital Tuanku Ja’afar, Ministry of Health
Malaysia, Seremban, Negeri Sembilan
ABSTRACT Introduction: COVID-19 pandemic is a challenging period, which requires
fast adaptation of the healthcare system. It is crucial for each of the patients to get accessto medical nutrition therapy from dietitian due to disease progress itself will affect patient
nutritional status. The study aims to identify nutritional status and diet intake of COVID19 inpatients and to determine efficacy of method in delivering Medical Nutrition
Therapy (MNT) and intervention done by dietitian. Method: An observational
retrospective study which using convenience sampling for study population, which
includes all records of the patients that fulfill the criteria. 30 Nutrition Care Process(NCP) records of COVID-19 patients warded in HTJS during COVID-19 pandemic from
April 2020 to May 2020 were included. Results: Among 30 of COVID-19 subjects, there
were 16 (53.3%) subjects given with Full COVID High Protein Diet, 3.3% (1) subject
indented with Full COVID High Protein Diabetic Diet as well as Full 30 Normal Dietand Soft 30 Normal Diet each. About 36.7% (11) paediatric subjects given with Full
COVID Paediatric Diet. Out of three assessment methods used, only 10% of subjects
answered the questionnaire and another 90% via direct phone call due to subjects did not
answered the questionnaire through google form after 48 hours of admission.
Conclusion: Dietitian approach in delivering MNT should incorporate and adapt with thecurrent new norms as align with advance technology in providing remote or virtual MNT.
This study also showed that MNT still needed due to NCD factors that can elevate therisk of mortality among COVID-19 patients.
Key words: Medical nutrition therapy, pandemic, COVID -19, dietitian
INTRODUCTION
The breaking of a COVID-19 pandemic is
posing unprecedented challenges and threats topatients and healthcare systems worldwide (2). The
initial clinical sign of the SARS-CoV-2 relateddisease COVID-19 which allowed case detection
was pneumonia (5). The disease primarily involves
the respiratory tract but it may deteriorate to multiorgan failure and be fatal (12). In addition, death
statistic reported by Crisis Preparedness andResponse Centre (CPRC), Ministry of Health andDepartment of Statistic, Malaysia (DOSM) (20),shows that total death percentage among COVID-19
patients is 1.47% which most of them involved deathamong older population and person with underlying
non-communicable disease (NCD). Mortality
appears to be highest among older people and thosewith comorbidities, who are also often the most at
risk of under-nutrition in society (18). Dietitian canplay an important role in managing cases of NCD
and under-nutrition. Identification and correction ofunder-nutrition is practical steps to COVID-19
patients to improve outcomes cost-effectively (20).
During this pandemic period, there are number ofservices that were affected including dietetic
profession. Based on the recent online opinion polls
done among Malaysian dietitians, 57.4% to 60.7% of
dietitian stated that most of the implementation of
Medical Nutrition Therapy (MNT) among patientswere done in appropriate steps accordingly withsome constraint arising from the current situation(3). The same opinion poll also reported that 46.3%

from 298 respondents among Malaysian dietitians
think that dietitian could contribute towards careamong infected COVID-19 patients.
There are only few guidelines available fordietitians regarding their roles during pandemic or
outbreak to help them to overcome this issue.
Screening is designed to be quick way of identifying
those who are at significant risk of nutritional
problems so that further detailed nutritional
assessment can be undertaken and action can be put
in place including dietary intervention via
therapeutic diet alone or with oral nutrition
supplement. weight and height measurements is themost crucial screening process usually carry out
physically, however due to pandemic, reliable,
reported values from patient need to be gained. Thus,
there are a series of subjective criteria that can beused to help form an overall clinical impression of
an individual’s malnutrition risk category.
Subjective criteria including clinical impression on
body size and side effects of disease that affectedoral intake. This study aims to provide baseline dataon nutritional status and diet intake among COVID19 inpatients and method in delivering MNT during
pandemic.
METHODSThis is an observational retrospective study
with convenience sampling. The study includes all
the COVID-19 inpatients who able to tolerate orally
and exclude critically ill COVID-19 patients onventilator and were on Ryle’s tube feeding. 30 out of
37 COVID-19 inpatients received Nutrition Care________________________________________________________________________*To whom correspondence should be addressed:

fadhlinasamad@gmail.com
23

Medical Nutritional Therapy for COVID-19 Inpatients
Process (NCP) by dietitians in HTJS during
pandemic from April 2020 to May 2020. The data
extracted from Dietetic Care Note (DCN) andPatient Management System (SPP) including age,
comorbidity, class/category of Covid-19, medicationprescribe for COVID-19 treatment, sign andsymptoms related with COVID-19, biochemical
data, estimated food plate waste, type of special
therapeutic diet prescribed by dietitians for thepatient, oral nutrition supplement regime (ifavailable) and method of delivering MNT.
The data analysis done using the IBM SPSS
Statistics Version 21. Descriptive data expressed asmean. standard deviation (SD) unless otherwise
stated. One Way ANOVA used for normally
distributed data. Kruskal-Wallis ANOVA used for
non-normally distributed data. A value of P< 0.05
Variable
Age Group, years
≤19
20-39
≥40
Comorbidities
Hypertension
Cardiovascular
AsthmaRhinitis
Combination
NKMIClass Covid
Class 1
Class 2A
Class 3A
Class 3B
Class 4B

considered as statistically significant. The datacollected analyzed using an intention-to-treat basis.
RESULTS
Socio-demographic characteristics of thesubjects involved in this study were presented inTable 1, 37% (n=11) of the subjects were pediatricand 63% (n=19) were adult subjects. There were
43.3% male (n= 13) and 56.7% female (n= 17). Mostof the subjects were age below 19 years old (n=12).
The minimum age was 2 years old and maximum age
was 67 years old. There were six subjects (20%) had
comorbidities
compriseofhypertension,
cardiovascular disease, asthma, rhinitis, diabetes or
combinations. 50% (n= 15) of subjects werecategorized under COVID-19 Class 2A and 7 out of
15 subjects were pediatrics case.

Table 1: Social-demographic characteristics of the subjects
Male (n=13)

Out of 30 subjects, only 20 subjects measured
for potassium level, (n=1) was pediatric subject who
was on antiviral medication and balance (n=19) were
adult subjects. Another (n=10) pediatric subjects
were not any medications therefore blood potassium
level not available. Majority of the subjects showed
an improving trend in potassium level except for(n=4) subjects no further blood investigation prior todischarge. Other than that, no significance blood
result parameter correlates with nutritional status.
According to COVID-19 Case Category by
Infectious Disease Unit, Penang General Hospital,
the categories were based on classification orpresentation of symptoms (cough/SOB), fever, andpneumonia, oxygen dependent and critically ill withshock/MOF/ARDS. While based on ClinicalManagement of SARI when COVID-19 disease issuspected (interim guidance) by WHO, listed
clinical syndromes in mild illness category whichinterfere with oral intake such as fever, fatigue,
cough (with or without sputum), anorexia, malaise,muscle pain, sore throat, dyspnea, nasal congestionor headache. Rarely patients may also present withdiarrhea, nausea and vomiting.
Table 2 shows that all subjects except fromCOVID-19 Class 1 were presented with runny nose,
cough, fever and sore throat. Five subjects wereaccompanied with loose stool and another two had
arthralgia and myalgia. Most of the subjects

Female (n=17)5(41.7)4(44.4)4(44.4)7(58.3)5(55.6)5(55.6)0(0.0)
1(100.0)
1 (100.0)
1 (100.0)1(50.0)9(37.5)1(100.0)0(0.0)
0(0.0)
0 (0.0)1(50.0)15(62.5)2(50.0)5(33.3)4(66.7)1(25.0)1(100)

2(50.0)10(66.7)2(33.3)3(75.0)0(0.0)

presented with clinical symptoms were treated with
Hydroxychloroquine (HCQ) and different COVID19 anti-viral medication known as Favipiravir except
pediatric subjects, no medication was prescribed.
There were 14 specialized COVID-19 Diet
developed during pandemic focusing on high protein
diet with oral nutrition supplement (ONS) and highpotassium fruit. The menu plans providing averageenergy 1600 Kcal – 1700 calorie and 70g – 75g
protein per day. High protein diet category mainly
consists of 15% ONS providing 220-300 calorie; 1014g protein. If patient could not finish their meals
whereby intake only quarter or half of meal served,
they will be supplemented with ONS. Another two
categories which are Full 30 / Soft 30 and Full 50 /Soft 50 each indicate patient require with 30% ONS(480-560 calorie; 20-24g protein) and 50% ONS(577-657 calorie; 40-44g protein). Product given
either standard flavor formula with low GI plus
protein concentrated or combination with peptide
formula. High potassium fruit providing 131.2262.4mg (2.5-6.7mmol) of potassium intake withadditional 340mg (8.7mmol) potassium consumed if
given 30% ONS or 50% ONS. All of the pediatricsubjects were prescribed with Full Covid pediatricdiet. Most of the adult subjects were indented with
Full COVID High Protein Diet (n=16). Besides that,
7% (n=2) of the subjects were at risk of malnutritionand prescribed with Full 30 normal diet and Soft 30

24

Asian Journal of Dietetics, 2021
normal diet. For individuals having difficulty
coordinating breathing and chewing, beverages

Variable
Clinical Symptoms
Runny Nose
Cough
Fever
Combination
Asymptomatic
Medications
Hydroxychloroquine
Other Antibiotic
Combinations
No Medication
Commorbidities
Hypertension
Cardiovascular
AsthmaRhinitis
Combinations
NKMI

might be a better option to efficiently increaseenergy intake compared to solid food.

Table 2: Clinical data according to Class of COVID-19
Class 1
Class 2A
Class 3A
Class 3B
n (%)
n (%)
n (%)
n (%)
0(0.0)
0(0.0)
0(0.0)Class 4Bn (%)

4(66.7)1(100.0)3(100.0)3(60.0)8(53.3)0(0.0)

0(0.0)
0(0.0)
1(20.0)3(20.0)2(33.3)0(0.0)
0(0.0)
1(20.0)3(20.0)0(0.0)

0(0.0)
0(0.0)
0(0.0)
1(6.7)
0(0.0)

0(0.0)
0(0.0)
0(0.0)
4 (33.3)7(43.8)0(0.0)
0(0.0)
8(66.7)5(31.3)1(100.0)0(0.0)
0(0.0)

4(25.0)0(0.0)
0(0.0)
0(0.0)

0(0.0)
0(0.0)
1(100.0)0(0.0)

0(19.5)0(0.0)
1(100.0)0(0.0)
0(0.0)
3(12.5)0(0.0)
0(0.0)
0(0.0)
1(100.0)1(50.0)13(54.2)

1(100.0)0(0.0)
0(0.0)
0(0.0)
0(0.0)
6(25.0)0(0.0)
0(0.0)
0(0.0)
0(0.0)
3(50.0)2(8.3)

0(0.0)
1(100.0)0(0.0)
0(0.0)
0(0.0)
0(0.0)

Table 3: Specialized COVID-19 Diet
Special Diet
Number of Subjects (n)Full Covi COVID High Protein Diet
16
Full COVID High Protein Diabetic Diet
1
Full COVID Pediatric Diet
11
Full 30 Normal Diet
1
Soft 30 Normal Diet
1
1600-1700 calorie; 70-75 gram protein
HIGH PROTEIN DIETSUPPLEMENT ONS 30%
SUPPLEMENT ONS 50%(additional commercial soybean/ full(additional low GI flavored(additional low GI flavored milk
cream milk 2 pack/day + dates 20-40
milk + protein concentrated+ protein concentrated 6g/day +g/day)
6g/day+ dates 20-40 g/day)
1 bottle 50 ml of peptide drink+dates 20-40 g/day)Full COVID High Protein Diet
Full 30 Normal Diet
Full 50 Normal Diet
Full COVID High Protein Diabetic Diet
Full 30 Diabetic Diet
Full 50 Diabetic Diet
Full COVID Pediatric Diet
Soft 30 Normal Diet
Soft 50 Normal Diet
Soft COVID High Protein Diet
Soft 30 Diabetic Diet
Soft 50 Diabetic Diet
Soft COVID High Protein Diabetic Diet
Soft COVID Pediatric DietDISCUSSION
With the increasing burden of liver diseases on
the world’ s and Currently, there is no nutrition
guidelines specifically for patients with or at risk for
COVID-19 infection, yet guidelines from Evidence
Analysis Library is still applicable and can be used
to provide guidance when working with COVID-19
infected patients. However, some adjustments might
be required to meet the increased metabolic andfunctional needs caused by the COVID-19 infection
and treatments.
Hence COVID-19 patient should have accessto nutritional care as a part of healthcare services.
This study used virtual assessment approaches
through three main methods including selfanswering questionnaire from google form, direct

phone call to patient and or via call to ward staff.
Self-answering questionnaire can be reachedthrough link or QR Code stamped on patient’s diettray. For IT illiterate patients, the approaches weredone through phone call or ward staff assistance. Outof these three methods, only 10% of subjects
answered the questionnaire and another 90% via
direct phone call due to subjects did not answered thequestionnaire through google form after 48 hours ofadmission. The assessment included anthropometry,sign and symptoms, which may affect food intake
and estimated current intake in ward. These
approaches in line with Greenhalgh T et al (9), whichstate that every protocol made to avoid in-person
assessment of patients with COVID-19. According
to Deepa H et,al (11), due to limited resources and25Medical Nutritional Therapy for COVID-19 Inpatientsstaff during the COVID-19 pandemic, somenutrition screening procedures require flexibility tobetter meet the safety and operational needs of anorganization. Special coordination such as
conducting nutrition screening using patient-room
telephones can be considered to minimize staff
exposure.
Nutritional intervention should be tailoredaccording to subject’s needs by changing to specificdiet for COVID-19 and it can be met by oral
nutritional supplements (ONS). ESPEN in Expert
Statements and Practical Guidance for Nutritional
Management of Individuals with Sars-Cov-2
Infection stated that COVID-19 patients need moreenergy than normal. The patients require highcalorie, high protein meals and snack for each
mealtime to help prevent weight loss or further
weight loss, and maintain lean muscle mass while
helping the body to build better immune system tofight the infection. A study showed that therequirement for Covid-19 patients likely to be higher
than normal due to the pathology of COVID-19
infection. According to MNT for COVID-19 Quick
Guide energy and protein requirement for prevention
and treatment of malnutrition in individuals at risk or
infected with COVID-19 are as follows: Energy
needs for polymorbid patients aged >65 years is 27
kcal/kgBW/day while for severely underweight
polymorbid patients is 30 kcal/kgBW/day, this value
also as guidance for energy intake in older persons.
Protein needs in older person is 1g/kgBW/day
meanwhile in polymorbid medical inpatients in orderto prevent body weight loss, reduce the risk ofcomplications and hospital readmission and improvefunctional outcome requirement should be more than
> 1g/kgBW/day.
Luigia B et.al (15) stated that duringhospitalization, oral nutrition supplement (ONS) areuseful in case of malnutrition or for those cases
which intake only 50-60% and as for dysphagia
cases, it is mandatory to modify diet consistency inaddition to ONS. Nutrient-dense food and beverages,
including oral nutrition supplements are good
methods to increase calorie and protein intake thus
can help prevent weight loss and maintain leanmuscle mass (11). The menu included full COVID
high protein diet, full COVID high protein diabetic
diet, soft COVID high protein diet, soft COVID highprotein diabetic diet, full 30 normal diet, full 30
diabetic diet, full 50 normal diet, full 50 diabetic diet,soft 30 normal diet, soft 30 diabetic diet, soft 50
normal diet, soft 50 diabetic diet, soft COVID
pediatric diet, and full Covid pediatric diet.
Basically, all COVID -19 adult subjects were auto
indented with full COVID high protein diet while
COVID -19 pediatric subjects were auto indented
with full COVID pediatric diet upon admission but
subsequently changed to another type of diet dependon their needs after seen and intervened by dietitians.
COVID -19 subjects who received full 30 and soft
30 were also received additional oral nutrition
supplements (ONS) to increase their energy andprotein intake. Since they unable to finish their mealon account of their health condition/symptoms
which interfere with their oral intake. As part ofdietary intervention, pediatric cases (n=4, 1-6years
old), who were still bottle feeding were given withgrowing up formula and (n=3, ≥7years old) were
given commercial full cream milk during supper
which provided average energy and protein

supplemented 338.6kcal; 11.5g and 150kcal; 8g
respectively. All COVID -19 diet specially designed
as high protein diet category providing up to 75 g
protein per day. Another two categories which are
Full 30 / Soft 30 and Full 50 / Soft 50 each indicate
patient require with 30% ONS (480-560 calorie; 2024g protein) and 50% ONS (577-657 calorie; 40-44g
protein). Product given either in form of powder orready to drink. This in line with the intervention
done by Riccardo Caccialanza M.D et.al (4), whichstated that if nutritional risk is detected after
screening procedure, it is encouraged to prescribe thepatient with oral nutrition supplement; two to threebottles (125/200 mL/d) of protein-calorie ONS(600/900 kcal/d; 3555 g/d of proteins) provided topatients, to be consumed between or immediately
after meals.
There were few subjects developed
hypokalemia during the stay. Hypokalemia is anelectrolyte characterized by low serum potassium
concentrations (normal range: 3.5 – 5.0 mEq/L).
Hypokalemia is classified into stages of mild (3.03.4 mEq/L), moderate (2.5-2.9mEq/L) and severe(<2.5 mEq/L). Pathophysiology of COVID-19
infection itself might be the cause of hypokalemia in
COVID -19 patients. COVID-19 infection develop
when Sars-CoV-2 invades human cells via binding
angiotensin I converting enzyme 2 (CE2) on the cell
membrane (16). The final effect increases
reabsorption of sodium and water, and thereafter
increases blood pressure and excretion of potassium(K+) (21). So, the dietitians provide dietaryintervention for hypokalemia by providing high andmoderate potassium food such as banana, milk,
green leafy vegetables, dates and other potassiumcontaining food to the hypokalemic patients withaverage 131.2 – 262.4mg (2.5-6.7mmol) potassium.
According to contemporary review by Cohn
J.N et.al (6), national council on potassium inclinical practice, for prevention of hypokalemia, adosage of 20 mmol/d potassium in oral form isgenerally sufficient, and 40 to 100 mmol/d sufficientfor its treatment A study by Aboujamous.H et.al (1)reveals that every 10 mEq of potassium administered
increase serum potassium levels by a mean value of0.13 mEq/L. The result of the study also further
reveals that intravenous potassium appears to impact
serum potassium levels similarly to the impact oforal potassium. After intervention done by dietitians
and medical practitioners, there were improvementin subjects blood potassium level prior theirdischarge.
In conclusion, Medical Nutritional Therapy (MNT)
is a fundamental aspect in managing malnutrition
regardless of pandemic. Dietitians play a significant
role and should proactively implement appropriate
nutrition care plans (NCP) to assess, prevent andtreat malnutrition among COVID -19 patient. The
management and guidance provided in this study can
assist dietitian in assessing and intervening patients
infected with COVID -19 who are hospitalized.
Although it has been created and done in responseto the COVID -19 pandemic crisis, it could besuitable for every situation in the future that might
limit the availability of healthcare system and adopt
to the new norms and align with IR4.0 revolution.

26

Asian Journal of Dietetics, 2021
COMPLIANCE WITH ETHICALSTANDARDS
This study approved by MREC with reference
number KKM/NIHSEC/P20-1591 (4). No potential
conflict of interest was reported by the authors.
ACKNOWLEDGMENTS
We would like to thank Director and Deputy
Director of Hospital Tuanku Ja’afar, Seremban for
permission and approval in conducting this study.
We also would like to thank the Director General of
Health Malaysia for his permission to publish thisresearch.

11)

12)

13)

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