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Haemoglobin status to determine nutritional anaemia and its association with breakfast skipping and BMI among nursing undergraduates of Farasan Island, KSA

Published online by Cambridge University Press:  24 May 2022

Shabihul Fatma Sayed*
Affiliation:
College of Nursing, Farasan Province, Jazan University, Jazan, Kingdom of Saudi Arabia
Sumathi Nagarajan
Affiliation:
College of Nursing, Farasan Province, Jazan University, Jazan, Kingdom of Saudi Arabia
*
*Corresponding author: Shabihul Fatma Sayed, email Ssaid@jazanu.edu.sa

Abstract

The present study was conducted to determine nutritional anaemia using haemoglobin levels of female nursing undergraduates studying at Farasan Island with the purpose to intervene at a point, before the potential problems become serious later in life. In total, 130 apparently healthy, female students of Department of Nursing were recruited by a random sampling method to collect information on socio-demographic, lifestyle and anthropogenic characteristics, and dietary habits including breakfast skipping. Haemoglobin content was estimated using Sahli's Haemoglobinometer and observations were interpreted as per WHO's criteria for anaemia. Body mass index (BMI) was recorded using a digital weighing machine. Correlation between haemoglobin concentration, breakfast skipping and body mass index of study participants was assessed by Pearson's correlation. Data analyses were done using Origin software. Overall, 51⋅6 % (n = 67) students were all together anaemic with 28⋅5 % (n = 37) had mild anaemia, 15⋅4 % (n = 20) moderate and 7⋅69 % (n = 10) had severe anaemia. Of these, 20⋅8 % (n = 27) were underweight, 63⋅8 % (n = 83) normal weight and 15⋅4 % (n = 20) were above normal weight (over weight and obese). The Hb content showed a positive correlation with the BMI and exhibited an increasing trend with increase in the BMI among study participants (P < 0⋅05). Questionnaire analyses revealed that the majority (96⋅9 %, n = 126) of students were taking junk food as bulk of their meal. A strong negative correlation was recorded between Hb contents and breakfast skipping tendencies (r = −0⋅987, P < 0⋅05). Findings of the present study are of high significance for public health professionals and educators to prioritise actions that could motivate these future nurses to adapt healthy lifestyles to strategically combat nutritional anaemia.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

Introduction

Anaemia is a public health issue that affects low-, middle- and high-income countries and has adverse impacts on socio-economic development. Low oxygenation of brain tissues due to anaemia may lead to impaired cognitive functions and psychomotor development, especially among children and teens. It adversely affects learning, cognitive function, behaviour, attention and regular activities of young students(Reference Haas and Brownlie1Reference Krämer, Kumar and Vollmer3) and may also results in college absenteeism. Anaemia has multifactorial aetiology such as nutrition, age, sex, social class, lifestyle characteristics, anthropogenic factors which are reflection of obesity such as BMI, dietary habits and infections. Nutritional anaemia is one of the most important global health issues and is the most common morbidity among micronutrients and affects health, education, economy and productivity of the entire nation(Reference Kotecha4). It is categorised as one of the ten most serious health problems by the World Health Organization(5) and is defined by the WHO as Hb<13⋅0 g/dl in male adults and <12⋅0 g/dl in female adults(Reference Chopra and Anker6). In 2016, the global prevalence of anaemia among women of reproductive age was 32⋅8 % (compared with 30⋅3 % in 2012). The rates of anaemia were highest in South-East Asia (45⋅8 %), Eastern Mediterranean (39⋅8 %) and African (39⋅0 %) regions(7).

The term ‘nutritional anaemia’ encompasses all pathological conditions in which the blood haemoglobin concentration drops to an abnormally low level, due to a deficiency in one or several nutrients. Its adverse health consequences affect people of all age-groups(Reference Haidar8). Complete and balanced nutrition is essential to maintain normal health and avoid health risks throughout the entire life. Moreover, during the development stage and, particularly, during early adolescence, good nutrition is essential as it influences brain maturation and has impact on future health indicators(Reference Prado and Dewey9,Reference Khan, Awan and Misu10) . Increased activity, social life and the busy academic schedules of university undergraduates may affect their eating habits. Females in their teenage have higher nutrient requirements due to their rapid growth, expansion of red blood cells, dramatic psychological changes, loss of blood during menstruation, increased physical activities which are the characteristics of adolescence, and therefore are at higher risks of anaemia incidence if their nutritional needs are not met. If this happens for a long time, it will cause Hb levels continue to decrease and cause anaemia(Reference Brown, Isaacs and Krinke11).

Breakfast is the most essential meal of the day(Reference Musaiger12). Many previous studies have exhibited the proven positive impact of breakfast in appetite regulation(Reference Adolphus13). Although the variety of factors affect a person's nutritional status, irregular food consumption pattern mainly the breakfast skipping tendencies are the most dominant factor that makes young university females vulnerable to the development of anaemia because continued breakfast skipping makes the body unable to meet the diversity of nutrients needed for the synthesis of haemoglobin (Hb). Despite all these facts, breakfast is frequently skipped, especially among the young generation, with almost 74 % of female students in Saudi Arabia either skip or irregularly consume their breakfast(Reference Musaiger12,Reference Spence14) .

Furthermore, high overweight and obesity prevalence has been observed in developed and developing countries, and obesity is considered as an important public health problem worldwide(15,Reference Wang and Lobstein16) , mainly due to its close relationship between inadequate nutritional status leading to various serious health issues including nutritional anaemia. Overweight is multifactorial in origin, with important genetic(Reference Frisancho17) and environmental factors such as inadequate eating habits, the preference for quick meals, consisting mostly the high-calorie foods like snacks and soft drinks(Reference Neymotin and Sen18). It may be considered that anaemia holds a close association with body type and various anthropometric parameters(Reference Micozzi, Albanes and Stevens19Reference El-Shafie, Kasemy and Omar27). Thus, anthropometric parameters can serve as alternative predictors of anaemia, which are simple, non-invasive and rapid yet accurate. The most studied anthropometric parameters that find an association with haemoglobin levels include body mass index(Reference Lee and Kim28Reference Al Sabbah30) which gives significant information on the nutritional and health status of individuals. For this reason, BMI has been considered as one of the parameters to determine nutritional status of the study participants and hence nutritional anaemia. The majority of studies have associated anaemia with low BMI(Reference Alrubaie, Majid and Alrubaie31Reference Dutta, Karkada and Sengupta34). Although various studies have been conducted in the past on Hb content anaemia and the associated risk factors at the national(Reference Abalkhail and Sherine35Reference Shaban, Rahman and Al-Sabah41) and international levels(Reference Al Sabbah30,Reference Dutta, Karkada and Sengupta34,Reference Khan, Khan and Kochhar42Reference Abro, Saleem and Parveen45) , information of anaemia and its association with breakfast skipping, and BMI is not available. To the best of our knowledge, based on PubMed, Scopus and Google scholar database search, this is the first study that reports anaemia and its association with breakfast skipping, and BMI.

Farasan is a beautiful Island located about 40 km offshore from the city of Jazan. It is close to being registered under UNESCO's Man and Biosphere Program(Reference Egal46,Reference Al-Zayad47) . It has a vast educational institute, as Farasan University College with well-established Department of Nursing, affiliated to Jazan University. Despite all its beauty and natural wealth, scientifically it has been less studied. Farasan is famous for its coral reefs, pristine beaches, crystal clear waters and, rich land and underwater wildlife, and for its Parrot-fish locally called as ‘hareed’. Considering the increasing trend of breakfast skipping(Reference Musaiger12,Reference Spence14,Reference Al Tamimi, Alshwaiyat and Alkhalidy48) , obesity/overweight in KSA(49) and the higher prevalence and public health outcomes of anaemia(Reference Aedh, Elfaki and Sounni50), the study on the association of anaemia with breakfast skipping and BMI could help meet the challenges of anaemia and complications related to breakfast skipping due to malfunction in dietary intake. Since young girls of age 18–25 years are more prone to get nutritional anaemia as this age group is vulnerable to dietary deficiencies because of their increased physiological needs of micronutrients, it is crucial to expand our understanding on nutritional anaemia and its association with breakfast skipping, and BMI. The outcomes would be of high significance for public health professionals and educators to prioritise actions that could motivate these future nurses to adapt healthy lifestyles to combat nutritional anaemia.

Materials and methods

Study design

A cross-sectional study was conducted to determine nutritional anaemia among the nursing undergraduates. The study was conducted from the beginning of November 2020 to April 2021. Anaemia was determined by analysing blood samples to measure the concentration of haemoglobin (Hb g/dL). The correlation of Hb contents with breakfast skipping and body mass index (BMI) was assessed. Dietary habits for breakfast skipping of study participants were evaluated by questionnaire analyses.

Study subjects

The study included 130 eligible nursing undergraduates (18–25 years) from Department of Nursing at Farasan University College, Jazan University, Kingdom of Saudi Arabia. Study participants were randomly selected.

Ethical statement

This study was conducted according to the ethical guidelines of Jazan University and was approved by the College Ethics Committee (Farasan/2020-1). The study protocol strictly followed the Declaration of Helsinki. Participants were informed about the study objectives and enrolled after getting their voluntary consent, researchers conducted a face-to-face interview with each student during their scheduled intervals. Informed consent forms, along with a self-administered questionnaire, were sent to the WhatsApp group of students. Each student was given the complete unconditional choice to participate without any incentives/bonus or penalty and was assured that confidentiality of data throughout the study would be maintained and that the data would be used exclusively for research.

Inclusion criteria

Apparently healthy participants who gave their voluntary consent and were full-time students enrolled with Jazan University during the academic year 2020/2021 were included. Information pertaining to this has been summarised in Table 1.

Table 1. Demographic, lifestyle and anthropogenic characteristics, and the dietary habits of study participants (N = 130)

* P < 0⋅05 is statistically significant.

Exclusion criteria

Students on routine medications due to any type of medical conditions were not included in the study. Those who were having their menstruation during sampling were also not included. Students with bleeding disorders or with the history of haematological disorders and those who had undergone minor or major surgery in recent past were also excluded from the study.

Data collection

A self-structured questionnaire was developed after a comprehensive review of relevant literatures published in peer-reviewed journals only(Reference Al-Sharbatti, Al-Ward and Al-Timimi51Reference Al-Jamea, Woodman and Elnagi57). The questionnaire had three domains: Section A was dedicated to general Demographic information which included twelve items on age, gender, educational background, nationality, marital status, and study year. Section B had eleven items related to lifestyles and anthropometric characteristics and Section C had thirteen items which were exclusively focused on dietary habits of the study participants which included intake of regular breakfast, frequency of junk food intake, multivitamins and the questions on intake of iron/iron-rich foods (Table 1).

Data collection took nearly 4 months. All sampling and data collections were done under strict guidelines of COVID-19 safety protocol which may be the reasons that data collection took more time.

Estimation of Hb content

To collect data on Hb content of the participants, blood samples were drawn by Sahli's pipette and added to the haemoglobin tube where haemoglobin (Hb) was converted to acid haematin by the addition of 0⋅1 N HCl. The resulting brown colour was diluted by distilled water to finally match with the standard brown glass reference blocks of Sahli's haemoglobinometer(Reference Anand, Mir and Saxena58). Results were noted as g/dl. The measured values were tabulated and compared to the standard values of grading anaemia according to the WHO guidelines with <12 g/dL of haemoglobin considered as anaemic(5), while values of haemoglobin of 10⋅0–11⋅9 g/dL, 7⋅0–9⋅9 g/dL and <7 g/dL were noted as Grade 1 (mild) anaemia, Grade 2 (moderate) anaemia and Grade 3 (severe) anaemia, respectively. Good laboratory practice and quality control were maintained while blood sampling.

Anthropometric measurements

Anthropometric measurements related to weight and heights were taken by the researcher. Body weight and BMI were measured by a self-calibrating digital weighing machine in standardised manner with the students standing bare feet and wearing light clothes (Seca, Digital, Germany). Height measurements were reassured by using a stadiometer (Detecto, Patriot, USA) measured to the nearest 0⋅1 cm. Anthropometric measurements were used to get BMI data.

A value of BMI <18⋅5 kg/m2 was considered as underweight, 18⋅5–24⋅9 kg/m2 as normal weight, 25⋅0–29⋅9 kg/m2 as pre-obese (overweight) and BMI 30 kg/m2 was considered as obese(Reference Wang and Lobstein16,Reference Abarca-Gómez, Abdeen and Hamid59) .

Breakfast skipping

Breakfast skipping was calculated by the evaluation of questionnaire response. Breakfast is generally considered as the foremost meal taken after waking up in the morning between 5:00 am and 11:00 am(Reference O'Neil, Byrd-Bredbenner and Hayes60,Reference Kahleova, Lloren and Mashchak61) . Breakfast skipping is defined as not taking breakfast one day or more per week(Reference Lazzeri, Giacchi and Spinelli62,Reference Nilsen, Yngve and Monteagudo63) . The breakfast skipping was measured by asking the participants about the number of days per week they usually did not take the breakfast. The responses for reasons of skipping the breakfast were also calculated as frequencies and percentages.

Statistical analysis

Data were collected and analysed using Origin (version 8⋅1, Originlab.com, USA). Descriptive statistics were conducted where quantitative data was shown as mean and standard deviation (sd). The qualitative data were expressed as frequency and percentage. Inferential statistics was performed as χ 2 test to measure association between qualitative variables, while independent Student's t test was used to compare mean and sd of two sets of quantitative normally distributed data. Pearson's correlation was used to determine the type of correlation between Hb content (g/dL), breakfast skipping and BMI of the study participants. P-value was considered statistically significant at P < 0⋅05.

Results

Socio-demographic and health characteristic data on study participants are presented in Tables 1 and 2. The questionnaire analyses revealed that all the participants belonged to upper-middle class or affluent class (Table 1). Family's educational background and the study year of the participants had no significant relation to anaemia (P > 0⋅05, Table 1). Regarding lifestyle characteristics data, 96⋅2 % of the study participants reported that they have an active lifestyle and follow a scheduled evening walk and exercising activities in college gym during their free lecture timings.

Table 2. Descriptive statistics of study population

* Continuous variables were analysed using an independent samples t test and are expressed as means and standard deviations.

Hb contents of study participants

The mean Hb g/dL of the study population was 11⋅5 g/dL (Table 2).

Anaemia characteristics of study participants

Anaemia was present in 51⋅6 % (n = 67) of the study participants with 28⋅5 % (n = 37) had mild, 15⋅4 % (n = 20) moderate and 7⋅69 % (n = 10) had severe anaemia (Table 3).

Table 3. Distribution of the study sample according to the grade of anaemia

* Statistically significant at P < 0⋅05. Categorical variables were analysed using χ 2 test and expressed as numbers and percentages. Continuous variables were analysed using an independent samples t test and are expressed as means and standard deviations.

Breakfast skipping

Breakfast skipping was calculated by the evaluation of questionnaire response. Based on questionnaire analyses, it was found that only 23⋅1 % (n = 30) participants had daily breakfast habits, while 76⋅9 % (n = 100 students) skip breakfast regularly (Table 4).

Table 4. Reasons of breakfast skipping

* Categorical variables were analysed using χ 2 test. Statistically significant at P < 0⋅05.

The study participants who regularly skip breakfast had significantly lower mean haemoglobin status (11⋅5 g/dL, r = −0⋅983, P < 0⋅05) and hence were more likely to get anaemic compared to those who were regular in their breakfast (12⋅4 g/dL), although the number of such students were quite less. This clearly indicates that nutrients responsible to tackle anaemia were not taken in sufficient amount by the participants who were skipping breakfast and hence were anaemic. Those who regularly skip the breakfast cited the reasons as lack of time.

Anthropogenic measurements as BMI assessments

As exhibited by data of BMI, 20⋅8 % (n = 27) study participants were found to be under weight. Irrespective of their anaemic status, the majority of study subjects regularly skip breakfast and frequently consume junk foods as their diet and hence were at risk of developing anaemia.

Data pertaining to BMI of study participants exhibited that the frequency of anaemia was more among those who were underweight and was significantly less (P < 0⋅05) among overweight participants compared to the other study groups (Table 5). Furthermore, Hb content and BMI of the study participants exhibited a significant positive correlation (r = 0⋅187, P < 0⋅05, Table 6). It was noted that underweight students had the lowest mean haemoglobin content (6⋅2, sd 0⋅8 g/dL) and were severely anaemic. Moreover, overweight and obese students had highest mean haemoglobin concentration (12⋅5, sd 0⋅6 g/dl).

Table 5. Distribution of the study sample according to body mass index (BMI)

* Categorical variables were analysed using χ 2 test. Statistically significant at P < 0⋅05.

Table 6. Association of breakfast skipping and body mass index (BMI) with Hb content

r = Pearson's correlation.

P = Statistical significance at P < 0⋅05.

Discussion

Anaemia remains a major public health problem, affecting one third of all adults and almost two billion people worldwide(Reference Kassebaum, Jasrasaria and Naghavi64). Defined broadly as a condition associated with lower than normal haemoglobin concentration, anaemia impairs the circulation of oxygen in the blood, which in turn has detrimental effects on maternal and birth outcomes, suboptimal child growth, impaired learning, reduced work productivity and income earning during adulthood(65).

Despite the fact that the participants of the present study belonged to upper-middle class or affluent class, significant percentages of participants (51⋅6 %, n = 67) were found to be anaemic indicating that the incidence of nutritional anaemia is not exclusively related to poverty alone. Various other studies have also reported insignificant association between the prevalence of anaemia and socio-economic class(Reference Sultan36,Reference Manjula, Parameshwari and Pothen66) . The majority of study participants of the present study had mild anaemia which is also seen in other studies(Reference Subramaniyan, George and Seshadri67). Despite being well educated and well oriented about nutrition and its ill effect on health, anaemia is prevalent among nursing undergraduate students. BMI exhibits a higher prevalence of anaemia among underweight followed by normal weight and overweight participants. The prevalence of anaemia among 51⋅6 % study participants is a serious health issue as per WHO's classification(5). Findings of the present study are similar to various other studies, done on university students both inside the Kingdom and various international studies(Reference Al Hassan38,Reference Subramaniyan, George and Seshadri67,Reference Khan, Sohail and Ali68) .

Though we did not encounter more cases of severe anaemia in the present study, however, 15⋅4 % (n = 20) and 28⋅5 % (n = 27) of moderate and mild anaemia cases in the present study are worrisome findings. This study population is ideally supposed to have a better awareness and access to anaemia diagnosis and treatment compared to general population as all are the future healthcare professionals. These findings are similar to the study conducted by Pandey and Singh(Reference Pandey and Singh69) among the medical students, where they found that there was mild anaemia among twenty students (20⋅83 %) followed by moderate anaemia among nine students (9⋅37 %), however in another study by Keller(Reference Keller70) severe cases of anaemia was not found among the study participants. The findings are also comparable to a study conducted by Chaudhary et al. (Reference Chaudhary, Gupta and Verma71), where out of 104 subjects, 72 subjects (69⋅2 %) had mild anaemia while 32 subjects (30⋅8 %) had moderate anaemia and none of their study subjects had severe anaemia(Reference Haas and Brownlie1).

Although many factors affect a person's nutritional status, adequate nutrition is the most dominant factor for normal nutritional status(72). This is consistent with research conducted by Shariff and Akbar(Reference Shariff and Akbar73) which states that there is an influence between the levels of nutritional consumption on anaemic status of female students. Various other factors that trigger the occurrence of nutritional anaemia among adolescence are the wrong eating habits, wrong understanding of nutrition to attain a slim body, and also excessive preference for certain foods is prevalent among teenagers hindering their nutritional needs.

Anaemia is directly affected by the consumption of daily foods(Reference Shariff and Akbar73). Despite the documented benefits of breakfast consumption, skipping breakfast was found to be more common and the percentage of participants skipping regular breakfast was 76⋅9 %. It has also been reported in various other studies that the frequency of skipping breakfast is higher in girls(Reference Monzani, Ricotti and Caputo74,Reference Peña-Jorquera, Campos-Núñez and Sadarangani75) , and breakfast skippers tend to consume more fast food, leading to increased weight gain from adolescence to adulthood. These unhealthy dietary habits are also seen in various other such studies done in the past(Reference Chalise, Aryal and Mehta76Reference Cooper, Greene-Finestone and Lowell78). Evidence suggests that regular breakfast intake improves the cognitive function and have positive impact on the health of the children and young adults(Reference da Silva, Fawzi and Cardoso79,Reference Chandrakumari, Sinha and Singaravelu80) . Since breakfast is the first meal of the day which sets the metabolic rate, if breakfast is skipped, brain interprets it as starving setting a lower metabolic rate leading to weight gain when one eats later. The habit of breakfast skipping is also a risk factor for the incidence of anaemia among educated youth(Reference Gajre, Fernandez-Rao and Balakrishna81,Reference Funsu82) . Research conducted by Ansar et al. (Reference Ansar, Taslim and Jafar83) found that young women who did not eat breakfast showed lower mean haemoglobin (12⋅03 g/dl) compared to those who were regular in their breakfast (12⋅63 g/dl). Based on the results of the study, it can be concluded that breakfast habits have significant influence on the incidence of anaemia.

A significantly low BMI in women indicates disorder and malnutrition. Overall, a BMI level at 18⋅5 kg/m2 was more common among the study participants. Although in the present study, the relatively low frequency of overweight and obesity was recorded, and hence, BMI above 30 kg/m2 was least common. Analysis by BMI categories in the present study showed that the percentage of anaemia was found to be high among underweight students (88⋅9 %) as compared to normal (45⋅8 %), overweight (27⋅3 %) and obese participants (11⋅1 %). Studies conducted by various other scientists have also documented almost similar findings(Reference Khan, Awan and Misu10,Reference Chakraborty and Mandal32Reference Dutta, Karkada and Sengupta34,Reference Chandrakumari, Sinha and Singaravelu80) . These findings suggest that good nutritional status reduces the risk of anaemia. A large prevalence of anaemia is attributed to nutritionally inadequate diet among the females(Reference Chandrakumari, Sinha and Singaravelu80). Pandey and Singh(Reference Pandey and Singh69) found the prevalence of anaemia among underweight, normal weight and overweight was 60, 27⋅5 and 12⋅5 %, respectively. Gupta et al. (Reference Gupta, Maria and Kumar84) found the higher prevalence of anaemia among underweight 91⋅4 % followed by normal weight 83⋅6 % and in overweight participants 73⋅3 %. Similarly, Pal et al. (Reference Pal, De and Sengupta85) found the higher prevalence of anaemia among underweight males and females as 62⋅5 and 80⋅65 %, respectively, among normal weight males and females 45⋅98 and 62⋅67 %, and among overweight/obese males and females 19⋅05 and 25⋅0 %, respectively. Waseem et al. (Reference Waseem, Bano and Ahmad86) found 44⋅9 % anaemia among underweight participants, 23⋅67 % among normal weight while 10 % anaemia was recorded among overweight participants. Furthermore, Sinha et al. (Reference Sinha and Haldar24) reported the prevalence of anaemia among undernourished women at 76⋅06 % compared to those with normal weight and overweight women, where the prevalence was at 75⋅28 and 66⋅67 % indicating a positive correlation between anaemia and BMI. Furthermore, Gargade and Patil(Reference Gardage and Patil87) found similar findings of the higher prevalence of anaemia among normal weight 55⋅2 %, underweight 27⋅6 %, overweight 13⋅6 % and obese 3⋅4 %. Metha(Reference Metha88) also found that anaemia is more prevalent 63⋅33 % among underweight student and overweight students have the less prevalence of anaemia (0⋅83 %), while the prevalence of anaemia was 6⋅67 % in normal weight students. High Hb content recorded for overweight participants may probably be due to the nutritional status of these groups such as intake of high iron foods and also due to over-nutrition. The study done by Khan et al. (Reference Khan, Khan and Kochhar42,Reference Khan, Khan and Bhardwaj43) also showed a statistically significant positive correlation of BMI with haemoglobin. Contrary to this, Abro et al. (Reference Abro, Saleem and Parveen45) also found a negative correlation between Hb content and BMI among adolescents.

Despite the fact that overweight or obesity has been reported to induce inflammatory problems through release of hepcidine, an inhibitor of dietary iron absorption which may cause anaemia among overweight or obese individuals(Reference Al Sabbah30,Reference Abro, Saleem and Parveen45,Reference Pagani, Nai and Silvestri89) , the percentages of anaemia among participants with high BMI were quite less. This may probably be due to the reasons majority of the overweight participants were having active lifestyles in an attempt to shed their extra weight and were on dietary intake of camel milk which contains greater iron concentration (1⋅35–2⋅5 mg/l v. 0⋅3–0⋅8 mg/l)(Reference Wernery90). Since the majority of iron in camel's milk is associated with the lower molecular fraction of casein suggesting better bioavailability to increase iron store and haemoglobin synthesis(Reference Al-Awadi and Srikumar91), this might probably be the reason that the majority of overweight and obese participants could not develop anaemia. Furthermore, vitamin C concentration is also higher in camel milk(Reference Yadav, Kumar and Priyadarshini92,Reference Abdurahman and Gashu93) which enhances iron absorption from non-heme sources by reducing ferric iron into the readily bioavailable form – ferrous iron. These characteristics might have been beneficial for better haemoglobin synthesis.

Another reason may be that the participants were non-vegetarian in their food preferences and prefer camel meat, traditional seafood and organ meats which are rich in the bioavailable form of iron. In addition, these animal foods are good source of high-quality proteins with the capacity to enhance iron absorption from non-heme sources consequently increasing blood haemoglobin concentrations(Reference Neumann, Harris and Rogers94Reference Hurrell and Egli96) thus diluting the adverse effects of overweight on Hb synthesis.

Moreover, the percentage of anaemia in the present study was 51⋅6 % which is lower than that reported from several low-income countries, such as India(Reference Chandrakumari, Sinha and Singaravelu80), Ethiopia(Reference Gonete, Tariku and Wami97Reference Mengistu and Azage99), Nepal(Reference Timilsina, Yadav and Bhusal100), Brazil(Reference Morais, Alves and Fagundes-Neto101) and Latin America(Reference Vazquez, Valera and Villalobos77) however, is almost similar to that reported from high-income countries like Canada(Reference Hartfield102) and the United States of America(Reference Le103).

The percentages of moderate and severe anaemia in the present study were comparatively low at around 15⋅4 and 7⋅69 %, respectively. Such lesser prevalence of severe anaemia seems logical and could be justified by several factors. First, citizens have a high standard of living, which includes free education and medical care in addition to subsidised foods, such as iron-fortified bread and iron-fortified food whereas these factors remain strong predictors for anaemia in various other low- and middle-income countries(Reference Balarajan, Ramakrishnan and Ozaltin104). Second, the study participants had high hygienic practices which completely rules out the chances and occurrence of anaemia due to parasites or infections. Percentages of mild anaemia recorded in the present study are much lesser than that recorded for the female students of Faculty of Applied Medical Sciences in Jazan University (67⋅35 %)(Reference Hamali, Mobarki and Saboor44).

In the present study, there was no significant relation between anaemia and family education as analyses of questionnaire revealed that family members mainly parents of all the study participants were educated with some were being bilingual as Arabic and English (Table 1). The present study shows a statistically insignificant association of anaemia and socio-economic status (P > 0⋅05). Similar results are found in a study done by Ugwuja et al. (Reference Ugwuja, Ogbonnaya and Obuna53), which has also depicted that educational status and occupation had no effect on anaemia prevalence.

Though the incidence of moderate and severe anaemia is only 15⋅4 and 7⋅69 %, respectively, in the present study, it is still disheartening, as these students have better knowledge about anaemia and its consequences, compared to general population. The contributing factors could be the stress of the professional course which demands comparatively longer study hours, night shifts in hospitals during field trainings and changes in the dietary habits in most of the students, as they enter university.

Conclusion

To sum up, we may say that the percentage of mild anaemia are high among female nursing undergraduates of Farasan which in long term may affect cognitive, learning and work efficiencies of these future nurses. It is a matter of concern as this may probably be due to negligence of healthy food habits as majorities were found to skip their daily breakfast which is very important for a normal kick of the metabolism and, also due to more preference to junk foods.

The present study is a significant contribution in highlighting the problem of anaemia, and its association with breakfast skipping and BMI among educated youth. The outcomes of the study would also be useful in healthcare planning and to make policies to strategically reduce the incidence of anaemia.

Recommendations

Young girls of age 18–25 years are more prone to get nutritional anaemia. Routine checkup and haemoglobin estimation should be done frequently for the screening of anaemia as the majority of the participants were not even aware of that they are anaemic. Preventive programmes and policies should be made to combat this health issue.

Haemoglobin estimation of students at the time of students’ registration should be done. Iron and folic acid tablets in therapeutic doses should be provided to anaemic students by college clinic and expert general physician should be appointed in college clinic so that they could have appropriate medications. Also, a dietician should be appointed in the clinic so that the students specifically those who are staying far from their families could be motivated and educated to take balanced diet with a regular and healthy breakfast because nutritional anaemia is totally preventable.

Acknowledgements

The authors are highly grateful to the Dean of the College, Dr. Afaf Mohammad Babeeir, for providing necessary facilities and highly conducive work environment for successful accomplishment of the research. Thanks are also due to Dr. Sarah Almalki, Vice Dean of Research & Academic Development for her continued interest in research and development activities. The authors are also grateful to the Dean of Main Campus, College of Nursing, Dr. Muhammed Yahya Arishi and the Vice-Dean of Scientific Research Unit Dr. Hamad bin Ghalib Al Daleh for promoting research and development activities for Nursing Program. Thanks are also due to the members of laboratory committee from Main Campus, College of Nursing, Mr. Mohamed Ali Hamzi, Mr. Mohsen Ali Wad'ani and Mr. Ali Yahya Al-Hakami, for their keen interest in laboratory affairs during their routine lab visits of Department of Nursing, Farasan Campus. The authors also extend their sincere thanks to the participants who willingly participated in the study.

Funding Sources: The study is not funded from any government or private sources.

Authors' Contribution: Dr. Shabihul Fatma Sayed has designed the study, performed blood sampling and analyses, anthropological measurements, statistical analyses of the data and manuscript writing. Dr. Sumathi Nagarajan has done sampling and data entries. Finally, the manuscript was critically reviewed by Dr. Shabihul Fatma Sayed. Both the authors have given final approval of the manuscript.

Conflict of Interest: There is no conflict of interest between the authors.

References

Haas, JD & Brownlie, T (2001) Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr 131, 676S690S. doi:10.1093/jn/131.2.676SCrossRefGoogle ScholarPubMed
Halterman, JS, Kaczorowski, JM, Aligne, CA, et al. (2001) Iron deficiency and cognitive achievement among school aged children and adolescents in the United States. Pediatrics 107, 13811386. doi:10.1542/peds.107.6.1381CrossRefGoogle ScholarPubMed
Krämer, M, Kumar, S & Vollmer, S (2021) Anemia, diet, and cognitive development: impact of health information on diet quality and child nutrition in rural India. J Econ Behav Organ 190, 495523. doi:10.1016/j.jebo.2021.06.043CrossRefGoogle Scholar
Kotecha, PV (2011) Nutritional anemia in young children with focus on Asia and India. Indian J Community Med 36, 816. doi:10.4103/0970-0218.80786.CrossRefGoogle ScholarPubMed
World Health Organization (2015) The Global Prevalence of Anemia in 2011. Geneva: WHO.Google Scholar
Chopra, VK & Anker, SD (2020) Anaemia, iron deficiency and heart failure in 2020: facts and numbers. ESC Heart Fail 7, 20072011. doi:10.1002/ehf2.12797CrossRefGoogle ScholarPubMed
World Health Organization (2017) Trends in Anaemia in Women and Children: 1995 to 2016. Geneva: World Health OrganizationGoogle Scholar
Haidar, J (2010) Prevalence of anaemia, deficiencies of iron and folic acid and their determinants in Ethiopian women. J Health Popul Nutr 28, 359368. doi:10.3329/jhpn.v28i4.6042CrossRefGoogle ScholarPubMed
Prado, EL & Dewey, KG (2014) Nutrition and brain development in early life. Nutr Rev 72, 267284. doi:10.1111/nure.12102.CrossRefGoogle ScholarPubMed
Khan, JR, Awan, N & Misu, F (2016) Determinants of anemia among 6-59 months aged children in Bangladesh: evidence from nationally representative data. BMC Pediatr 16, 3. doi:10.1186/s12887-015-0536-zCrossRefGoogle ScholarPubMed
Brown, J, Isaacs, J, Krinke, U, et al. (2004) Nutrition Through the Life Cycle, 2nd ed. Belmont, CA: Thomson Wadsworth.Google Scholar
Musaiger, A (2007) Overweight and obesity in the Arab countries: the need for action. Arab Center for Nutrition (January).Google Scholar
Adolphus, K, et al. (2017) Methodological challenges in studies examining the effects of breakfast on cognitive performance and appetite in children and adolescents. Adv Nutr 8, 184S196S. doi:10.3945/an.116.012831.CrossRefGoogle ScholarPubMed
Spence, C (2017) Breakfast: the most important meal of the day? Intl J Gastronomy Food Sci 8, 16. doi:10.1016/j.ijgfs.2017.01.003.CrossRefGoogle Scholar
WHO (2006) BMI Classification. Global Database on Body Mass Index. Geneva: World Health Organization.Google Scholar
Wang, Y & Lobstein, T (2006) Worldwide trends in childhood overweight and obesity. Int J Pediatr Obes 1, 1125. doi:10.1080/17477160600586747CrossRefGoogle ScholarPubMed
Frisancho, AR (2000) Prenatal compared with parental origins of adolescent fatness. Am J Clin Nutr 72, 11861190. doi:10.1093/ajcn/72.5.1186CrossRefGoogle ScholarPubMed
Neymotin, F & Sen, U (2011) Iron and obesity in females in the United States. Obesity 19, 191199. doi:10.1038/oby.2010.112.CrossRefGoogle ScholarPubMed
Micozzi, MS, Albanes, D & Stevens, RG (1989) Relation of body size and composition to clinical biochemical and hematologic indices in US men and women. Am J Clin Nutr 50, 12761281. doi:10.1093/ajcn/50.6.1276.CrossRefGoogle ScholarPubMed
Smith, BB, Reed, P, Pearson, E, et al. (1991) Erythrocyte dyscrasia, anemia, and hypothyroidism in chronically underweight llamas. J Am Vet Med Assoc 198, 8188.Google ScholarPubMed
Collett-Solberg, PF, Fleenor, D, Schultz, WH, et al. (2007) Short stature in children with sickle cell anemia correlates with alterations in the IGF-I axis. J Pediat Endocrinol Metab 20, 211218. doi:10.1515/JPEM.2007.20.2.211.CrossRefGoogle ScholarPubMed
Saxena, Y, Shrivastava, A & Saxena, V (2011) Effect of gender on correlation of anaemia with body mass index in medical students. Ind J Physiol Pharmacol 55, 364369.Google ScholarPubMed
Chang, J-S, Chen, Y-C, Owaga, E, et al. (2014) Interactive effects of dietary fat/carbohydrate ratio and body mass index on iron deficiency anemia among Taiwanese women. Nutrients 6, 39293941. doi:10.3390/nu6093929CrossRefGoogle ScholarPubMed
Sinha, NK & Haldar, JP (2015) Correlation between haemoglobin level and anthropometric variables: a study on women of reproductive age group, West Bengal. Anthropologist 19, 185192. doi:10.1080/09720073.2015.11891653.CrossRefGoogle Scholar
Virginia, DM & Fenty, F (2017) Correlation between anthropometric measurements and risk of anemia among rural community in Cangkringan, Sleman. J Pharm Sci Comm 14, 112119. doi:10.24071/jpsc.142712.CrossRefGoogle Scholar
Sumami, S, Puspitaari, N, Handajani, R, et al. (2016) Underweight as a risk factor for iron depletion and iron-deficient erythropoiesis among young women in rural areas of east Java, Indonesia. Mal J Nutr 22, 219232.Google Scholar
El-Shafie, AM, Kasemy, ZA, Omar, ZA, et al. (2020) Prevalence of short stature and malnutrition among Egyptian primary school children and their coexistence with anemia. Ital J Pediatr 46, 19. doi:10.1186/s13052-020-00855-y.CrossRefGoogle ScholarPubMed
Lee, BJ & Kim, JY (2016) Identification of hemoglobin levels based on anthropometric indices in elderly Koreans. PLoS ONE 11, e0165622. doi:10.1371/journal.pone.0165622.CrossRefGoogle ScholarPubMed
Vuong, J, Qiu, Y, La, M, et al. (2014) Reference intervals of complete blood count constituents are highly correlated to waist circumference: should obese patients have their own “normal values?”. Am J Hematol 89, 671677. doi:10.1002/ajh.23713.CrossRefGoogle ScholarPubMed
Al Sabbah, H (2020) Prevalence of overweight/obesity, anaemia and their associations among female university students in Dubai, United Arab Emirates: a cross-sectional study. J Nutr Sci 9, 16. doi:10.1017/jns.2019.41CrossRefGoogle ScholarPubMed
Alrubaie, A, Majid, S, Alrubaie, R, et al. (2019) Effects of body mass index (BMI) on complete blood count parameters. Pren Med Argent 105, 164171.Google Scholar
Chakraborty, A & Mandal, GC (2019) A cross sectional study of association between hemoglobin levels and the BMI indices among the adolescents Sunni Muslim population in Lucknow city, India. Asian J Life Sci 1 (104), 1-6. doi:10.29011/2577-0241.100004Google Scholar
Kamruzzaman, MD (2021) Is BMI associated with anemia and hemoglobin level of women and children in Bangladesh: a study with multiple statistical approaches. PLoS ONE 16, e0259116.CrossRefGoogle ScholarPubMed
Dutta, S, Karkada, IR, Sengupta, P, et al. (2021) Anthropometric markers with specific cut-offs can predict anemia occurrence among Malaysian young adults. Front Physiol 12, 731416. doi:10.3389/fphys.2021.731416.CrossRefGoogle ScholarPubMed
Abalkhail, B & Sherine, S (2002) Prevalence of daily breakfast intake, iron deficiency anaemia and awareness of being anaemic among Saudi school students. Int J Food Sci Nutr 53, 519528. doi:10.1080/09637480220164370CrossRefGoogle ScholarPubMed
Sultan, AH (2007) Anemia among female college students attending the University of Sharjah, UAE: prevalence and classification. J Egypt Public Health Assoc 82, 261271.Google ScholarPubMed
Mohamed, S & Sweilem, S (2014) Prevalence of anemia levels in a sample of University female students. Int J Sci Res 3, 805809.Google Scholar
Al Hassan, NN (2015) The prevalence of iron deficiency anemia in a Saudi University female students. J Microsc Ultrastruct 3, 2528. doi:10.1016/j.jmau.2014.11.003CrossRefGoogle Scholar
Elfakki, FAM & AlBarrak, NSM (2016) Counseling strategies for nutritional anemia by family physicians in Saudi Arabia: implication for training. Family Med Community Health 5, 259265. doi:10.15212/FMCH.2017.0124.CrossRefGoogle Scholar
Al Afeef, SA, Albridi, AI, Alherz, IH, et al. (2020) Review of nutritional anemia in low and middle income regions. EC Microbiol 16, 0107.Google Scholar
Shaban, A-TA, Rahman, A, Al-Sabah, R, et al. (2020) Anemia and its associated factors among adolescents in Kuwait. Sci Rep 10, 5857. doi:10.1038/s41598-020-60816-7.CrossRefGoogle ScholarPubMed
Khan, T, Khan, ZA, Kochhar, S, et al. (2018) Unfeasible body mass index and its association with low haemoglobin concentration: a correlation study among undergraduate medical students. Int J Res Med Sci 6, 40024007. doi:10.18203/2320-6012.ijrms20184898CrossRefGoogle Scholar
Khan, ZA, Khan, T, Bhardwaj, A, et al. (2018) Underweight as a risk factor for nutritional anaemia - a cross-sectional study among undergraduate students of a medical college of Haryana. Indian J Comm Health 30, 6369.Google Scholar
Hamali, HA, Mobarki, AA, Saboor, M, et al. (2020) Prevalence of anemia among Jazan University students. Int J Gen Med 5, 765770. doi:10.2147/IJGM.S275702.CrossRefGoogle Scholar
Abro, S, Saleem, Q, Parveen, SA, et al. (2021) Association of body mass index with hemoglobin level, erythrocyte indices and red cell distribution width. Professional Med J 28, 311317. doi:10.29309/TPMJ/2021.28.03.5334CrossRefGoogle Scholar
Egal, F (2004) The jewel of the Red Sea (author, with inputs from Villeneuve François). Une inscription latinesur Farasân, Arabie Séoudite, sud de la mer Rouge (note d'information). Comtesrendus des séances de l'Académie des inscriptions et belles-lettres 148, 419429.Google Scholar
Al-Zayad, S (2020) Saudi Farasan Islands close to being registered in UNESCO's MAB.Google Scholar
Al Tamimi, JZ, Alshwaiyat, NM, Alkhalidy, H, et al. (2022) Breakfast skipping among a multi-ethnic population of young men and relationship with sociodemographic determinants and weight status. Int J Environ Res Public Health 19, 2903. doi:10.3390/irjerph19052903.CrossRefGoogle Scholar
World-Health-Survey-Saudi-Arabia (2019) Kingdom of Saudi Arabia World Health Survey. https://www.moh.gov.sa/en/Ministry/Statistics/Population-Health Indicators/Documents/World-Health-Survey-Saudi-Arabia.pdf (accessed November 2021).Google Scholar
Aedh, A, Elfaki, NK & Sounni, EM (2019) Iron deficiency anemia and associated risk factors among teenagers in Najran, Saudi Arabia. Int J Med Res Health Sci 8, 108114.Google Scholar
Al-Sharbatti, SS, Al-Ward, NJ & Al-Timimi, DJ (2003) Anemia among adolescents. Saudi Med J 24, 189194.Google ScholarPubMed
Soleimani, N & Abbaszadeh, N (2011) Relationship between anaemia, caused from the iron deficiency, and academic achievement among third grade high school female students. Procedia Soc Behav Sci 29, 18771884. doi:10.1016/j.sbspro.2011.11.437.CrossRefGoogle Scholar
Ugwuja, EI, Ogbonnaya, LU, Obuna, AJ, et al. (2015) Anaemia in relation to body mass index (BMI) and sociodemographic characteristics in adult Nigerians in Ebonyi state. J Clin Diagnost Res 9, LC04LC07.Google ScholarPubMed
Alzaheb, RA & Al-Amer, O (2017) The prevalence of iron deficiency anemia and its associated risk factors among a sample of female university students in Tabuk, Saudi Arabia. Clin Med Insights Womens Health 10, 1179562X17745088.Google ScholarPubMed
AlSheikh, M (2018) Prevalence and risk factors of iron-deficiency anemia in Saudi female medical students. Saudi J Health Sci 7, 148152. doi:10.4103/sjhs.sjhs_79_18.CrossRefGoogle Scholar
Alswailem, A, Alahmed, S & Alshehri, M (2018) The prevalence of iron deficiency anemia and its associated risk factors among a sample of females in Riyadh, Saudi Arabia. Egypt J Hosp Med 72, 462.Google Scholar
Al-Jamea, L, Woodman, A, Elnagi, EA, et al. (2019) Prevalence of iron-deficiency anemia and its associated risk factors in female under-graduate students at prince sultan military college of health sciences. J Appl Hematol 10, 126133. doi:10.4103/joah.joah_44_19.CrossRefGoogle Scholar
Anand, H, Mir, R & Saxena, R (2009) Hemoglobin color scale a diagnostic dilemma. Indian J Pathol Microbiol 52, 360362. doi:10.4103/0377-4929.54994Google ScholarPubMed
Abarca-Gómez, L, Abdeen, ZA, Hamid, ZA, et al. (2017) Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128⋅9 million children, adolescents, and adults. Lancet 390, 26272642. doi:10.1016/S0140-6736(17)32129-3CrossRefGoogle Scholar
O'Neil, CE, Byrd-Bredbenner, C, Hayes, D, et al. (2014) The role of breakfast in health: definition and criteria for a quality breakfast. J Acad Nutr Diet 114, S8S26. doi:10.1016/j.jand.2014.08.022CrossRefGoogle ScholarPubMed
Kahleova, H, Lloren, JI, Mashchak, A, et al. (2017) Meal frequency and timing are associated with changes in body mass index in Adventist Health Study. J Nutr 147, 17221728.Google ScholarPubMed
Lazzeri, G, Giacchi, MV, Spinelli, A, et al. (2014) Overweight among students aged 11-15 years and its relationship with breakfast, are of residence and parents’ education: results from the Italian HBSC 2010 cross-sectional study. Nutr J 13, 110. doi:10.1186/1475-2891-13-69CrossRefGoogle ScholarPubMed
Nilsen, BB, Yngve, A, Monteagudo, C, et al. (2017) Reported habitual intake of breakfast and selected foods in relation to overweight status among seven-to nine-year-old Swedish children. Scand J Public Health 45, 886894. doi:10.1177/1403494817724951CrossRefGoogle ScholarPubMed
Kassebaum, NJ, Jasrasaria, R, Naghavi, M, et al. (2014) A systematic analysis of global anemia burden from 1990 to 2010. Blood 123, 615624. doi:10.1182/blood-2013-06-508325CrossRefGoogle ScholarPubMed
International Food Policy Research Institute (2016) Global Nutrition Report 2016: From Promise to Impact: Ending Malnutrition by 2030. Washington, DC: International Food Policy Research Institute (IFPRI).Google Scholar
Manjula, VD, Parameshwari, P, Pothen, L, et al. (2014) Prevalence of anemia among female undergraduate students of Government Medical College Kottayam, Kerala. Int J Med Health Sci 3, 133138.Google Scholar
Subramaniyan, K, George, M, Seshadri, D, et al. (2016) Prevalence of anemia among health science students of a University in South India. Int J Res Med Sci 4, 45984601.Google Scholar
Khan, HM, Sohail, M, Ali, A, et al. (2014) Symptoms based evaluation of iron deficiency anemia in students of Bahawalpur correlated with their eating habits. Trop J Pharm Res 13, 769772. doi:10.4314/tjpr.v13i5.17CrossRefGoogle Scholar
Pandey, S & Singh, A (2013) A cross sectional study of nutritional anaemia among medical students in a Medical College at Bilaspur Chhattisgarh. Natl J Medical Res 3, 143146.Google Scholar
Keller, H (2006) The burden of anemia in rural Bangladesh: the need for urgent action. Nutr Surveill Proj Bull 16, 14.Google Scholar
Chaudhary, P, Gupta, R & Verma, R (2019) Improvement in physical fitness index, VO2 max score and hemoglobin level with diet and nutrition intervention. Appl Biol Res 21, 4148. doi:10.5958/0974-4517.2019.00006.5.CrossRefGoogle Scholar
Supariasa (2014) Penilaian Status Gizi. Jakarta: EGC.Google Scholar
Shariff, SA & Akbar, N (2018) Hubunganantara status Gizidan Pola Menstruasidengan Kejadian Anemia pada Mahasiswi Prodi DIII Kebidanan Universitas Muslim Indonesia. J Window Health 1, 3439.Google Scholar
Monzani, A, Ricotti, R, Caputo, M, et al. (2019) Systematic review of the association of skipping breakfast with weight and cardiometabolic risk factors in children and adolescents. What should we better investigate in the future? Nutrients 11, 387. doi:10.3390/nu11020387CrossRefGoogle ScholarPubMed
Peña-Jorquera, H, Campos-Núñez, V & Sadarangani, KP (2021) Breakfast: a crucial meal for adolescents’ cognitive performance according to their nutritional status. The cogni-action project. Nutrients 13, 1320. doi:10.3390/nu13041320.CrossRefGoogle ScholarPubMed
Chalise, B, Aryal, KK, Mehta, RK, et al. (2018) Prevalence and correlates of anemia among adolescents in Nepal: findings from a nationally representative cross-sectional survey. PLoS ONE 13, e0208878. doi:10.1371/journal.pone.0208878.CrossRefGoogle ScholarPubMed
Vazquez, I, Valera, L, Villalobos, E, et al. (2019) Prevalence of anemia in children from Latin America and the Caribbean and effectiveness of nutritional interventions: systematic review and meta (−) analysis. Nutrients 11. doi:10.3390/nu11010183.Google Scholar
Cooper, M, Greene-Finestone, L, Lowell, H, et al. (2012) Iron sufficiency of Canadians. Health Rep 23, 4148.Google ScholarPubMed
da Silva, LL, Fawzi, S, Cardoso, WW, et al. (2018) Factors associated with anemia in young children in Brazil. PLoS ONE 13, e0204504. doi:10.1371/journal.pone.0204504.CrossRefGoogle ScholarPubMed
Chandrakumari, AS, Sinha, P, Singaravelu, S, et al. (2019) Prevalence of anemia among adolescent girls in a rural area of Tamil Nadu, India. J Family Med Primary Care 8, 14141417. doi:10.4103/jfmpc.jfmpc_140_19.CrossRefGoogle Scholar
Gajre, NS, Fernandez-Rao, S, Balakrishna, N, et al. (2008) Breakfast eating habit and its influence on attention-concentration, immediate memory and school. Achievement Ind Pediatr 45, 824828.Google ScholarPubMed
Funsu, A (2018) Analysis of Breakfast Habits on The Incidence of Anemia International Conference on Sustainable Health Promotion. Faculty of Psychology and Health, UIN Sunan Ampel Surabaya, October 9–11, pp. 25–29.Google Scholar
Ansar, Taslim, NA & Jafar, N (2014) Anemia padaRemaja putri dalam kaitannya dengan malaria, pola konsumsi pangan dan status Sosial Ekonomidi Daerah Endemik Malaria. J MKMI 10, 8589.Google Scholar
Gupta, VK, Maria, AK, Kumar, R, et al. (2011) To study the prevalence of anaemia in young males and females with respect to age, body mass index (BMI), activity profile and the socioeconomic status in rural Punjab. J Clin Diagnos Res 5, 10201026.Google Scholar
Pal, A, De, S, Sengupta, P, et al. (2014) An investigation on prevalence of anaemia in relation to BMI and nutrient intake among adult rural population of West Bengal, India. Epidemiol Biostat Public Health 11, e8915-1e8915-109.Google Scholar
Waseem, SM, Bano, R, Ahmad, N, et al. (2015) Study of haematological profile and body mass index in undergraduate medical students in Lucknow, Uttar Pradesh. IJHSR 5, 257262.Google Scholar
Gardage, CB & Patil, SN (2016) Prevalence of anaemia in first MBBS students in a Rural Medical College. J Evolution Med Dent Sci 5, 13291331. doi:10.14260/jemds/2016/312Google Scholar
Metha, K (2015) Prevalence of nutritional anemia among college students and its correlation with their body mass index. Int J Sci Res 4, 18821886.Google Scholar
Pagani, A, Nai, A, Silvestri, L, et al. (2019) Hepcidin and anemia: a tight relationship. Front Physiol 9, 1294. doi:10.3389/fphys.2019.01294.CrossRefGoogle Scholar
Wernery, U (2006) Camel milk, the white gold of the desert. J Camel Pract Res 13, 1526.Google Scholar
Al-Awadi, FM & Srikumar, TS (2001) Trace elements and their distribution in protein fractions of camel milk in comparison to other commonly consumed milks. J Dairy Res 68, 463469. doi:10.1017/S0022029901005003CrossRefGoogle ScholarPubMed
Yadav, AK, Kumar, R, Priyadarshini, L, et al. (2015) Composition and medicinal properties of camel milk: a review. Asian J Dairy Food Res 34, 8391. doi:10.5958/0976-0563.2015.00018.4CrossRefGoogle Scholar
Abdurahman, A & Gashu, D (2021) Level of hemoglobin among cow milk and camel milk consuming young children: a comparative study. PLoS ONE 16, e0247572. doi:10.1371/journal.pone.0247572.CrossRefGoogle ScholarPubMed
Neumann, C, Harris, DM & Rogers, LM (2002) Contribution of animal source foods in improving diet quality and function in children in the developing world. Nutr Res 22, 193220. doi:10.1016/S0271-5317(01)00374-8CrossRefGoogle Scholar
Reddy, MB, Hurrell, RF & Cook, JD (2006) Meat consumption in a varied diet marginally influences non heme iron absorption in normal individuals. Nutr J 136, 576581. doi:10.1093/jn/136.3.576CrossRefGoogle Scholar
Hurrell, R & Egli, I (2010) Iron bioavailability and dietary reference values. Am J Clin Nutr 91, S1461S1467. doi:10.3945/ajcn.2010.28674FCrossRefGoogle ScholarPubMed
Gonete, KA, Tariku, A, Wami, SD, et al. (2017) Prevalence and associated factors of anemia among adolescent girls attending high schools in Dembia District, Northwest Ethiopia, 2017. Arch Public Health 76, 79. doi:10.1186/s13690-018-0324-y.CrossRefGoogle Scholar
Tariku, EZ, Abebe, GA, Melketsedik, ZA, et al. (2019) Anemia and its associated factors among school-age children living in different climatic zones of Arba Minch Zuria District, Southern Ethiopia. BMC Hematol 19, 6. doi:10.1186/s12878-019-0137-4.CrossRefGoogle ScholarPubMed
Mengistu, G & Azage, M (2019) Iron deficiency anemia among in-school adolescent girls in rural area of Bahir Dar City Administration. North West Ethiopia 2019, 1097547. doi:10.1155/2019/1097547.Google ScholarPubMed
Timilsina, A, Yadav, RM, Bhusal, P, et al. (2020) Status of Anemia among Undergraduate Students of a Medical College of Central Nepal. J College Medical Sci-Nepal 16, 103106. doi:10.3126/jcmsn.v16i2.25652.CrossRefGoogle Scholar
Morais, MB, Alves, GM & Fagundes-Neto, U (2005) Nutritional status of Terena indian children from Mato Grosso do Sul, Brazil: Follow up of weight and height and current prevalence of anemia. J Pediatr 81, 383389. doi:10.2223/JPED.1389.CrossRefGoogle Scholar
Hartfield, W (2010) Iron deficiency is a public health problem in Canadian infants and children. Paediatr Child Health 15, 347350. doi: 10.1093/pch/15.6.34.CrossRefGoogle ScholarPubMed
Le, CH (2012) The prevalence of anemia and moderate-severe anemia in the US population (NHANES 2003-2012). PLoS ONE 11, e0166635. doi:10.1371/journal.pone.0166635.CrossRefGoogle Scholar
Balarajan, Y, Ramakrishnan, U, Ozaltin, E, et al. (2011) Anaemia in low-income and middle-income countries. Lancet 378, 21232135. doi:10.1016/s0140-6736(10)62304-5.CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Demographic, lifestyle and anthropogenic characteristics, and the dietary habits of study participants (N = 130)

Figure 1

Table 2. Descriptive statistics of study population

Figure 2

Table 3. Distribution of the study sample according to the grade of anaemia

Figure 3

Table 4. Reasons of breakfast skipping

Figure 4

Table 5. Distribution of the study sample according to body mass index (BMI)

Figure 5

Table 6. Association of breakfast skipping and body mass index (BMI) with Hb content