Utilization of various honey, fruits, and vegetables to increase hemoglobin levels in pregnant women with anemia in Indonesia

The aims of the study was to analyze the student’s theses research data of Midwifery Study Program at Faculty of Health Sciences Universitas Nasional regarding the use of honey, fruit and vegetables to increase hemoglobin levels in pregnant women with anemia in Indonesia. The research was conducted by analyzing student theses for four semesters between 2020 and 2023. The variables analyzed included location of the research, types of honey, fruits and vegetables, form of serving, method of consumption, and the effect on hemoglobin levels. A total of 522 student’s theses from 2020 until 2023 were recorded. The results showed 40 theses research (7.66%) were according to the research objectives. The research locations were cover 11 provinces in Indonesia. There are two types of honey, namely acacia honey and mutiflora honey. There are 10 fruits consumed with or without a combination (guava, star fruit, dates, tomatoes, dragon fruit, watermelon, ambon banana, papaya, lime, avocado). There are also 10 vegetables consumed with or without a combination (beetroot, carrot, red spinach, green spinach, katuk, moringa, matel, green bean, broccoli, and caulerpa). The mean increase in the hemoglobin level ranged from 0.85 to 3.71 g/dl. Prevention of anemia in pregnancy should not only be done by providing blood-boosting tablets or iron supplement but also by providing varied and nutritionally balanced food to increase the hemoglobin level and prevent anemia in pregnancy.


Introduction
Anemia is a condition when the body experiences a decrease in red blood cells, or the number of red blood cells is below the normal range.This condition can occur in everyone [1].Anemia is stated as one of the most widespread diseases in the world [2].Anemia affects a quarter of the world's population and is concentrated in preschoolers and women [3].Anemia in pregnancy is a global public health problem [4], which mostly occurs in developing countries [1].
Based on the Basic Health Research in Indonesia in 2018, the percentage of pregnant women who experience anemia is 48.9%.This means that about 5 out of 10 pregnant women in Indonesia suffer from anemia [5].Anemia in pregnancy has a very high risk.Anemia in pregnancy increases the risk of maternal and perinatal morbidity and mortality, and is associated with preterm delivery and low birth weight [6,7,8].Negative health effects of anemia for the mother include fatigue, poor work capacity, impaired immune function and increased risk of heart disease [8].Meanwhile, negative health effects of anemia for the fetus in the womb include impaired fetal growth and development.Anemia can potentially cause pregnancy and childbirth complications [5].Furthermore, after the baby's born, their cognitive development can also be affected if the mother is iron deficient during her last trimester of pregnancy [9].1255 (2023) 012037 IOP Publishing doi:10.1088/1755-1315/1255/1/012037 2 An indicator of anemia is the concentration of hemoglobin, an oxygen-binding protein found in red blood cells.The main component of hemoglobin is iron in the Fe2+ or ferrous state [10].Iron is an essential element with important functions such as oxygen transport, DNA synthesis and muscle metabolism.Iron deficiency is the main cause of anemia, which is the most prevalent nutritional deficiency worldwide [9].
The World Health Organization (WHO) has defined anemia in pregnancy as a hemoglobin (Hb) concentration of less than 11 g/dl [11], and in more detail, it is defined as a hemoglobin concentration of less than 11.0 g/dl in the first trimester and less than 10.5 or 11.0 g/dl in the second or third trimester [12].Indeed, the need for iron in pregnant women increases by 25% compared to non-pregnant women [5].
To overcome the high incidence of anemia in pregnancy, the government of Indonesia has launched (a program encouraging) the consumption of blood-boosting tablets (In Bahasa Indonesia Tablet Tambah Darah / TTD) containing 60 mg of Ferrous Fumarate and 400 mcg of Folic Acid.Ferrous fumarate is a form of iron in the Fe2+ or ferrous state.A minimum of 90 tablets of iron tablets must be taken by pregnant women during pregnancy [13].The consumption of iron supplements every day during pregnancy can reduce the risk of maternal anemia by 70% and iron deficiency by 57% [14].However, this effort has not been successful enough, so the prevalence of anemia in pregnancy is still high.There is a possibility that the incidence of anemia is mainly caused by poor nutrition.Nutritional anemia is anemia that occurs due to insufficient intake of nutrients by cells.Among the most important nutrients that, if they are deficient, can cause anemia, are iron, folic acid, vitamin B12, vitamin B6, vitamin C and protein [15].These nutrients can be fulfilled by providing honey, fruit, vegetable and animal-based food.
The Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional has a scientific vision of herbal medicines and complementary midwifery care.With this scientific vision of herbal medicines, studies carried out by lecturers and students are directed at the use of various herbal medicines in Indonesia for care, treatment, recovery and healing in the life cycle of women.One of which is this study on the use of herbal medicines including a variety of honey, fruits and vegetables to increase the hemoglobin level of pregnant women with anemia.
The study aimed to analyze the undergraduate theses research data of students of the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional regarding the use of honey, fruit and vegetables to increase the hemoglobin level of pregnant women with anemia in Indonesia.

Materials and Methods
This study was carried out by recording all the undergraduate theses of students of the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional, for four semesters from 2020 to 2023.Data were obtained from the Academic Information System of Universitas Nasional, thesis soft files given to researchers and thesis soft files in the office secretariat of the Faculty of Health Sciences.The theses which were the object of this study were theses on the topic of the use of honey, fruits and vegetables to increase the hemoglobin level of pregnant women with anemia in Indonesia.
The variables in this study were the number of students researching the related topic; research locations; research design; respondents; hemoglobin measurement; analysis of results; types of honey, fruits, vegetables, or other forms that do not fall into the three categories mentioned; form and method of consumption; duration of consumption; and increase in hemoglobin.The results of this study were then analyzed qualitatively.

The number of students researching the related topic
The number of undergraduate theses of students who have graduated and the number of undergraduate theses with the related topic for 4 semesters from 2020 to 2023 are presented in Table 1.The total number of undergraduate theses of students of the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional, for four semesters is 522-and 40 theses or 7.66% use Honey, Fruits and Vegetables to increase the hemoglobin level of pregnant women with anemia.Apart of the related topic, studies carried out by students which take advantage of Indonesia's biodiversity are also aimed at increasing the hemoglobin level in young women with anemia, reducing blood pressure in hypertensive patients, reducing the pain level in dysmenorrhea, increasing breast milk, healing perineal wounds, overcoming breast milk dams and so on.
Honey, fruits and vegetables are natural products that can be used as health foods, dietary supplements and herbal medicines that have benefits for human health.The studies carried out by students of the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional are in line with the use of dietary supplements and herbal medicines derived from natural substances to improve quality of life in which their purported benefits have increased worldwide.The use of many dietary supplements and herbal medicines could be based on knowledge from traditional medical practices [16].

Student research locations
The results of data collection on student research locations by province, regency/municipality and island are presented in table 2. The locations of the student studies on the topic of the use of honey, fruit and vegetables to increase the hemoglobin level of pregnant women with anemia in Indonesia, were found in 11 provinces, located in 22 regencies/municipalities and 8 islands.Most of the studies were carried out in the provinces of West Java with 18 studies, Banten with 10 studies, Maluku with 3 studies, Lampung with 2 studies and others-namely Special Capital Region of Jakarta, Central Java, East Java, South Sumatra, Central Sulawesi, North Maluku and East Nusa Tenggara with 1 study each.
The islands where the studies were carried out apart from Java, Sumatra and Sulawesi, are islands that are rarely mentioned, namely Ambon, Seram, Dullah, Bacan and Timor.Regarding the provinces and islands where the studies were carried out, it shows that students come from various places in Indonesia.This confirms that the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional is sought after by students from all over Indonesia.
The results of previous studies regarding the provinces of origin of students studying at the Study Program of Midwifery, Faculty of Health Sciences, Universitas Nasional, showed that they were from 29 out of 34 provinces in Indonesia from 2016 to 2018, covering the provinces of Aceh, North Sumatra, West Sumatra, South Sumatra, Jambi, Bengkulu, Bangka-Belitung, Banten, Special Capital Region of Jakarta, West Java, Central Java, East Java, Special Region of Yogyakarta, Bali, West Nusa Tenggara, East Nusa Tenggara, West Kalimantan, East Kalimantan, South Kalimantan, North Kalimantan, Central Sulawesi, South Sulawesi, Southeast Sulawesi, North Maluku, Maluku, Papua and West Papua [17].

Research design; respondents; hemoglobin measurement; and analysis of results
The research design carried out by students was entirely quasy experimental, with or without using a control group.The number of respondents used in the studies ranged from 15 to 60 pregnant women.The determination of respondents was carried out using purposive sampling.The inclusion criteria include mildly to moderately anemic pregnant women with a hemoglobin level of <11mg/dl, willing to take iron tablets according to the provisions, and not having acute or chronic diseases.Most of the students' theses stated that ethical clearences had been carried out at universities outside Universitas National, Jakarta, Indonesia.
Hemoglobin measurement was carried out using a digital hemoglobinometer with an accuracy of two decimal places.The blood used was from peripheral blood taken from the mother's middle or ring finger using a sterile lancet.The hemoglobin level measurement was carried out before and after providing the honey, fruit, or vegetable.
Analysis of the results obtained was carried out using univariate analysis and bivariate analysis.Univariate analysis was carried out to determine the mean value, minimum value, maximum value and frequency distribution.Bivariate analysis was carried out based on the results of the homogeneity test and whether there was a control group.If the data were normally distributed, parametric tests, namely the paired sample t-test and the independent t-test were used, whereas if the data were not normally distributed, non-parametric tests, namely the Wilcoxon test and the Mann-Whitney test were used.This is following the statistical theories that apply in the health sector [18].

Types of honey, fruits, vegetables; form and method of providing
To increase the hemoglobin level of pregnant women with anemia, besides consuming blood-boosting tablets every day, they be done by consuming honey or fruits, or vegetables, either singly or in combination, local and scientific name, form of serving of honey, fruits and vegetables as presented int table 3.There are two types of honey, namely acacia honey and mutiflora honey.There are 8 fruits consumed without a combination (guava, star fruit, dates, tomatoes, dragon fruit, watermelon, Ambon banana, papaya) and two types of fruit, lime and avocado, consumed in combination.There are two types of tubers (beetroot and carrot), five types of leaves (red spinach, green spinach, katuk, moringa and matel), one type of pea-namely green bean, one seaweed-namely caulerpa, one flower-namely broccoli.The providing fruits and vegetables most often used to increase the hemoglobin level are red guava with seven studies and moringa leaves and green spinach with four studies each.
The ways of serving of honey, fruits and vegetables were by consuming directly such as eating dates and ambon bananas or eating by cutting into pieces the fruits-such as dragon fruit and papaya.Then by making fruit and vegetable juices, such as juices from red guava, watermelon, star fruit, tomato, dragon fruit or juices from a combination of date and coconut water or a combination of vegetable, fruit and honey (spinach, lime and honey).Another way is by making tea like moringa leaves tea.For consumptions, honey was consumed as much as 10 ml twice daily-in the morning and evening.Then juice and tea were consumed between 200 -250 ml between once to twice daily.The average consumption of fruits and vegetables is 200 grams twice daily.The duration of the providing food consumption minimal was between 12-15 days.
Even though the government has provided and obliges pregnant women to consume blood-boosting tablets, almost 50% of pregnant women still suffer from anemia [5].Reference tracing results suggest that iron absorption is not simple.Dietary iron absorbed by the intestinal mucosa consists of two types, namely iron heme and iron non-heme.Iron heme, derived from animal hemoglobin and myoglobin, is well absorbed and relatively little influenced by other foods eaten in the same meal.On the other hand, the absorption of iron non-heme, derived from the main food, is greatly influenced by the composition of other foods [19].Heme iron is present only in animal products such as meat, fish and poultry, while iron non-heme is found in fruits, vegetables, dried beans, nuts and grain products [20].Iron non-heme contributes up to 90% of iron levels consumed through food in the form of Fe3+ but its absorption is influenced by dietary factors and iron status in the human body.On the other hand, iron heme in the form of Fe2+ contributes 10% of dietary iron and its absorption is not influenced by dietary factors that are taken/consumed with it [21].
In the absorption of iron, there are enhancer factors, namely ascorbic acid and meat, fish and poultry.The inhibitors are plant components in vegetables, tea and coffee (eg., polyphenols, phytates), and calcium [22].Ferrous (Fe2+) is the only iron that can be absorbed through iron transporters of intestinal enterocyte cells [23].For this reason, iron non-heme ferric (Fe3+) must first be converted to ferrous (Fe2+).At a low pH, gastric acid in the proximal duodenum allows a ferric reductase enzyme, duodenal cytochrome B (Dcytb)-on the brush border of the enterocytes to convert the insoluble ferric (Fe3+) to absorbable ferrous (Fe2+) ions.Enhancers of iron absorption are dominated by the effects of vitamin C or ascorbic acid, which can overcome the effects of all dietary inhibitors when it is included in a diet with high iron non-heme availability (usually a meal heavy in vegetables) [24].Vitamin C forms a chelate with ferric (Fe3+) iron in the low pH of the stomach, which persists and remains soluble in the alkaline environment of the duodenum where iron is absorbed [19,24].
Based on the explanation above, it is important to have vitamin C in various foods given to pregnant women with anemia.Vitamin C helps in the absorption of iron by converting Fe3+ to Fe2+ so that it is more easily absorbed by the body [25].Other studies also state that iron and vitamin C supplementation has a greater impact on the changes of the hemoglobin level compared to iron supplementation only [26].
Based on the results of student studies, the food given is food that contains vitamin C. For every 100 grams of food given to pregnant women, there is an amount of vitamin C based on the USDA (United States Department of Agriculture) and several other references, namely 0.5 mg honey; 0.4 mg dates; 4 mg dragon fruit; 4.9 mg beetroot; 6 mg carrot; 8.1 mg watermelon; 8.7 mg banana; 8.8 mg avocado; 14 mg tomatoes; 30 mg spinach; 60 mg papaya; 90 mg cauliflower; and 228 mg guava.Moringa leaves contain 200 mg of vitamin C per 100 grams of leaves [27].Katuk leaves contain 239 mg of vitamin C per 100 grams of leaves [28].Thus the addition of various types of fruits and vegetables to pregnant women is mostly vitamin C supplementation which can convert non-heme iron Fe3+ to Fe2+ which facilitates absorption by the duodenum.
Apart from iron deficiency, anemia can also be caused by nutrient deficiency, namely vitamin A, riboflavin (vitamin B2) and vitamin B12 [29].Studies have shown that vitamin A supplementation has a significant impact on iron status indices and iron deficiency anemia [30].Anemia can be prevented with riboflavin.Studies have shown that increasing the amount of riboflavin in the body can increase the circulating hemoglobin level and increase red blood cell production.The advantage of riboflavin is that it is a heat-stable, water-soluble vitamin [31].A study of parenteral administration of vitamin B12 and iron shows gradual improvement in anemia [32].
Based on USDA data and several other references, the presence of vitamin A and riboflavin is found in 100 g of bananas, respectively 64 IU and 0.073 mg; beetroot 33 IU and 0.04 mg; spinach 9,377 IU and 0,189 mg; guava 624 IU and 0.04 m; dates 10 IU and 0.066 mg; carrot 16,706 IU and 0,058 mg; tomatoes 833 IU and 0.019 mg; dragon fruit 59 IU and 0.1 mg; moringa leaves 7560 IU 0.66 mg; cauliflower 623 IU and 0.117 mg.Katuk leaves contain vitamin A of 10370 IU while honey contains 0.038 mg of riboflavin.
In fruits and vegetables, vitamin B12 is rarely found.When there is vitamin B12 in foods of plant origin, the levels are very small.Sources of vitamin B12 are foods of animal origin [33].As for macroalgae, vitamins C and B12 with antioxidant properties are present [34].Thus vitamin A and riboflavin found in fruits and vegetables are used to increase the hemoglobin level in pregnant women not in iron absorption, but together with iron that has entered the body-they will help increase the hemoglobin level.
Based on USDA reference, honey does not contain much vitamin C, vitamin A and riboflavin.However honey can influence the absorption process, pharmacological activity and bioavailability of the phytochemical compounds dissolved in it [35].Thus to increase the hemoglobin level, it should not only focus on iron consumption but also on nutrient consumption that should be varied and balanced.

Increase in hemoglobin
The mean hemoglobin level in pregnant women during the examination before the consumed the food was 9.10 to 10.20 g/dl.Meanwhile, the mean hemoglobin level after consumed the food was 10.80 to 12.75 g/dl.The mean increase in the hemoglobin level ranged from 0.85 to 3.71 g/dl.All study results showed a significant increase in the hemoglobin level before and after the intervention with consumed the food.There was a significant difference in the increase hemoglobin level in the group consumed the food and the control group.Most of the studies showed changes in the anemia group, namely from mild anemia to normal and from moderate anemia to mild or normal anemia.
Hemoglobin is a component of red blood cells that is responsible for the delivery of oxygen to the tissues [36].In arterial circulation, hemoglobin has a high affinity for oxygen and a low affinity for carbon dioxide [37].Oxygen is needed for the formation of energy in the body.Lack of hemoglobin level will result in reduced red blood cells, while lack of red blood cells in the body will cause less oxygen to be sent throughout the body so that the formation of energy in the form of ATP in the mitochondria decreases.
An indirect result of anemia is reduced energy in the body, causing people to feel lethargic, weak, tired, fatigued and inattentive as well as having headaches and making them more susceptible to infectious diseases.Pregnant women who suffer from anemia are at risk of having a miscarriage, premature birth, low birth weight babies, and bleeding before, during and after giving birth.In moderate and severe anemia, bleeding can become more severe, thus risking maternal and infant death.Babies born to mothers with anemia have very little iron supply in their bodies so they are at risk of developing anemia at an early age.If this happens, it can result in disruption/barriers to their growth and development.
Thus, babies born to mothers with anemia can become stunted.This must continue to be suppressed/found a solution for the golden generation of Indonesia.For this reason, it is necessary to intervene in pregnant women not only by giving blood-boosting tablets but also by providing honey, fruits and vegetables as well as animal food sources containing iron heme that is easily absorbed by the human body.Most importantly, the variety of food needs to be improved.

Conclusion
There are two types of honey, namely acacia honey and mutiflora honey.There are 10 fruits consumed with or without a combination (guava, star fruit, dates, tomatoes, dragon fruit, watermelon, ambon banana, papaya, lime, avocado).There are also 10 vegetables consumed with or without a combination (beetroot, carrot, red spinach, green spinach, katuk, moringa, matel, green bean, broccoli, and caulerpa.
Increased hemoglobin levels can occur if pregnant women consume iron supplement tablets and consume honey or fruits or vegetables according to the provisions given Vitamin C in the food given in the studies can increase iron absorption.As for vitamin A, riboflavin and vitamin B12 can increase the formation of hemoglobin.
Prevention of anemia in pregnancy should not only be done by providing blood-boosting tablets or iron supplement but also by providing varied and nutritionally balanced food on an ongoing basis to increase the hemoglobin level which can ultimately prevent anemia.

Table 1 .
Percentage of undergraduate theses related to the topic for four semesters

Table 2 .
Research locations based on province, regency/municipality and island

Table 3 .
Local and scientific name, form of serving of honey, fruits and vegetables