Infrequent consumption of Laban is associated with anemia in adults aged >50 years in Saudi Arabia

Introduction: Limited information is available on the prevalence of anemia in adults and elderly. Contradictory results are available regarding the association between drinking Laban and anemia in children and adults. No study has explored this association in the adults/elderly population. The aim of this study was to measure the prevalence and association between anemia and food items among adults aged >50 years in Riyadh, Saudi Arabia. Material & Methods: 266 Saudi adults aged >50 years were invited to participate in a cross-sectional study in Riyadh. Anthropometric measurements were taken and blood samples were collected. Blood hemoglobin was measured with a Coulter Cellular Analysis System using the light scattering method. Multiple logistic regression analyses were performed to identify the food items significantly associated with anemia. Results: The mean (±SD) hemoglobin was 13.8 (±1.6) mg/dL. Anemia was prevalent among 19.9% (n = 53) of the participants. Infrequent intake of red meat [adjusted Odds Ratio ORa 3.4; 95% confidence interval CI 1.2, 9.7] and Laban (fermented yogurt drink) ORa 2.7, 95% CI 1.1, 6.7 were significantly associated with anemia, whereas obesity (BMI >30) was protective aOR 0.4, 95% CI 0.2, 0.9 from anemia. Conclusion: Anemia is prevalent among Saudi males and females aged >50 years. The association between drinking Laban and anemia support the emerging evidence on the role of probiotics in preventing anemia among adults and elderly. It is recommended that people aged >50 years should get regularly screened for anemia.

high as 45% [1]. Studies from Middle-East found that the prevalence of anemia in the elderly ranged between 6.3% to 16.3% [3,4]. Alhamdan from Saudi Arabia reported the prevalence of anemia as 38% in adults (24 to < 60 years) and 55% in those aged > 60 years [5]. Few other studies found that the prevalence among Saudi adult males ranged between 2.3% to 6.3%, whereas in females it ranged between 18% to 21.0% [6][7].
Anemia may lead to multiple negative health consequences, such as poor physical performance, decrease in body strength, increased risk of falls, exacerbation of associated disease conditions, impaired cognition and, in severe cases, even death [8 -10].
Anemia due to lack of appropriate and inadequate nutrition is considered as one of the most common types present among the older adults [11]. Nutritional anemia can be prevented by several food items, especially green vegetables, fruits, meat, liver, eggs are [12]. In majority cases, multiple factors act together and can lead to anemia in the elderly [12].
The world population ageing report, 1950 -2050, reports a worldwide shift in the youngold age balance [13]. Similar to elsewhere in the world, Saudi Arabia is expected to observe an increase from 5.4% (1.6 million), to 25% in the population aged >50 years by 2050 [14]. Generally, it is believed that people aged >50 years will suffer from chronic diseases like hypertension, diabetes, or cardiovascular problems and anemia is not considered important [15]. A significant proportion of the population accepts it as a normal aging process being unaware of the long term consequences of anemia [15]. This study is part of a larger project on the prevalence and associated factors of anemia among different age groups in Riyadh, Saudi Arabia. Research publications (from the same project) focusing on children, adolescents and the child-bearing aged women have been published elsewhere The results related to middle-aged and elderly are being presented here. The objective of this study was to measure the prevalence and association between anemia and common food items among adults aged >50 years in Riyadh, Saudi Arabia.

Study participants
This study was part of a large community-based, two-staged household cross-sectional survey, and hence does not need to be registered. According to 2010 -2011 census report, Riyadh has a total population of 3,151, 209 individuals [16]. In the first stage, one primary health care centers (PHCC) was randomly selected from each of the five administrative regions (East, West, North, South and Central) of Riyadh city. In the second stage, households situated in the catchment area of respective PHCC were approached and invited to participate. Assuming the prevalence of anemia at 50% in elderly and with 5% width of confidence interval, and significance level of 0.05, we needed to interview 368 women. For risk factors of anemia, assuming a type-I error of 0.05, type-II error of 0.20 (power of 0.80) and 30% difference of prevalence of risk factors in anemic and nonanemic participants, we need to have 300 adults aged > 50 years. However due to missing data and selection criteria, 266 participants were included in the final analysis.

Data collection procedure and tools
Trained data collectors conducted the interviews to collection information about sociodemographic characteristics, medical history, smoking and reproductive history (from females only). Food frequency questionnaire inquired about the frequency of intake for red meat, vegetables, eggs, tea or coffee, fruit juices, beverages and laban (diluted yogurt) during the last one week. Medical history included past or current diseases such as peptic ulcer, hemorrhoids, parasitic infections, cancers and Bilharzias. Females were inquired about menopause and number of children. Anthropometric measurements included weight and height. Weight was measured in kilograms using an electronic scale (Secca 220 -Hamburg Germany 2009), whereas height was measured in cms using the stadiometer. The body mass index (BMI) was calculated by using the formula weight in kg / [height in m] 2 for each participant [17].

Statistical analysis
Data were analyzed using the Statistical Package for the Social Sciences computer software package (IBM SPSS statistics version 21.0). The outcome variable (anemia) was defined according to the cut-off values recommended by World Health Organization (WHO) (males Hg <13 g/dl and females Hg <12 g/dl) [18]. Descriptive statistics with mean and standard deviations (SD) and percentages were calculated for continuous and categorical variables. Intake of dietary items was reported as frequently (5 -7 days/week), infrequently (2 -4 days/week) or 0 or 1 as never taken during the last week. The level of statistical significance was kept at p < 0.05. Pearson correlation coefficient was calculated to measure the correlation between continuous variables. Bivariate analysis was conducted to identify biologically plausible and statistically significant variables associated with anemia. Variables causing a change of 10% in the estimates were retained in the final model. Multivariable logistic regression was performed to identify important dietary items associated with anemia. Hosmer and Lemeshow goodness-of-fit test was used to assess the model-fit. Plausible interactions were checked before developing the final model.
Majority of the participants were currently married and had education till primary level or less ( Table 1). The mean reported number of children was five (±3) and ranged from 2 to 14. The mean (±SD) BMI of males and females was 29.0 (±5.2) and 31.2 (±6.4) [p = 0.004], respectively. No statistically significant difference was observed in mean BMI levels between anemic and normal Saudi males (p = 0.5) or females (p=0.4). A small percentage (ranging from 2% to 6%) of participants reported problems like peptic ulcers, hemorrhoids, cancers or Bilharzias diseases (results not shown). Three females and two males were diagnosed as cases with cancer (results not shown). None of the participants had current or past history of intestinal parasitic infection. A significant difference was observed in the numbers of males and females using iron supplements in the past (1% of males vs. 4% of females). About 10.4% (n = 27) of males were ever smokers; however, only 5.8% (n = 15) were currently smoking cigarettes. None of the female participants was a smoker.
The food frequency questionnaire found that the most frequently consumed food items were red meat (60%), green vegetables (60%), followed by Laban (55%), eggs (47%), tea (30%), cola drinks (20%) and fresh juices (19%). Amongst these red meat and eggs were consumed on frequently basis, whereas green vegetables and Laban were infrequently consumed. Majority reported that food items like tea and cola drinks were consumed only 0 -1 times per week ( Table 2). No significant difference was observed in the dietary patterns between males and females (results not shown).

Discussion
The prevalence of 19.9% is significantly higher than reported by previous studies amongst the same age group in Saudi Arabia [5 -7]. In our study both males and females showed almost equal prevalence of anemia (19.3% vs 21.2%), which is in contradiction with previous studies that have reported significantly higher prevalence amongst the females [5 -7, 19]. The International review study on anemia reported a prevalence of 10% among people aged >65 years, that increased to 40% among elderly aged >80 years [20]. We observed an overall increase of 6% in anemia among >60 years with respect to <60 years.
Our sample had very few people aged > 80 years (n=4), hence, we are limited in commenting on the increase in this specific group.
The findings related to majority of anemic males in the older age category (> 60 years) can be explained through various mechanisms. It is proven that age leads to increase in pro-inflammatory cytokines, especially IL-6, which in turn inhibits the synthesis of erythropoietin, which may impair the erythroid progenitor cell proliferation, and interferes with iron metabolism [21,22]. In addition, age-related inflammatory conditions lead to increased cytokine production, which stimulate the liver to release hepcidin, which in turn decreases intestinal absorpstion of iron and decreases the release of iron from macrophages [21]. There is also reason decreased responsiveness of the bone marrow erythroid precursors to stimulatory growth factors with advancing age that may contribute to higher prevalence of anemia among elderly males [22].
Diluted yogurt, Laban, is one of the most ancient, widely consumed, drink in the Arab world [23]. It belongs to the group of fermented food products, containing probiotics [24,25]. Studies from Middles East, including Saudi Arabia have confirmed the presence of probiotics in yogurt and dairy drinks, including Laban [26,27]. Probiotics, containing the Lactic Acid Bacteria (LAB) are known to have various beneficial effects including controlling and preventing gastrointestinal problems, allergies, cholesterol and regulating the immune functions [24 -28].
One of the bacilli, the Lactobacillus plantarum is found to assist in the iron absorption from the gut by maintaining acidic environment, acting as an anti-inflammatory agent [29] or by producing iron chelating ligands or by degrading the mineral complexing phytic acid from the food consumed, thus defining its role in preventing iron deficiency anemia [30]. It is a general understanding that obesity is negatively associated with health. However, our findings are in support of a large-scale study conducted on Columbian reproductive age group women [37], that found overweight and obese women had lower prevalence of anemia as compared to normal weight. It is recommended that elderly people should consume high caloric diet as they are at risk of malnutrition [38]. In the older people, the daily recommended daily allowance (RDA) of proteins is same as for the younger 0.80 g/kg/day [39]. One explanation may be that despite being obese, they tend to consume diet, which is healthy, and rich in micronutrients, and hence they are at less risk of developing anemia.
Anemia can be both a diagnosis as well as a complication due to other diseases; hence, the earlier it is detected, the better the outcome [12,13]. Fortunately, the majority of anemics in our study had mild anemia (Hb 11.0 -12.9 mg/dL). Mild anemia, due to its trivial presentation, is usually ignored; however, complications are associated even with This is one of the first community-based surveys reporting the association between Laban intake and anemia in adults aged >50 years in Riyadh, Saudi Arabia. The number of participants in this age category was less compared to other; however, this distribution supports the actual age pyramid of Saudi Arabia, where a large population consist of children, adolescents and young adults compared to elderly. The findings of this study can be generalized to other urban/semi-urban areas of Saudi Arabia, as Riyadh is the capital and home to different social and ethical groups. Our study also had some limitations. We cannot comment on the type of anemia, as we failed to measure serum ferritin, vitamin B12 or Folate levels. The food frequency questionnaire was not validated hence lack of comparability of the results to those from other studies that have used standard instruments. The design was cross-sectional so that the temporal relation of Laban to anemia cannot be determined.
With increased aging in the Saudi population, the prevalence of anemia will is most likely to increase, causing a burden on the health system and the society. Hence, it is recommended that health education and early screening at the primary health care level should be made mandatory. Future prospective and interventional studies should explore the effect of Laban intake on improving the iron stores and hence hemoglobin among adults and elderly.

Ethics approval and consent to participate
The study protocol was approved by the Institutional Review Board, King Saud University. Informed and signed consent was received from each participant

Consent for publication
Consent for publication for research purpose was taken from the participant.

Availability of data and material
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests"

Funding
The study was funded by the Vice Deanship of Research, King Saud University, Riyadh, Saudi Arabia and the Ministry of Health, Riyadh, Saudi Arabia. The funding was provided to cover the data collection, blood sample collection and the laboratory tests.

Author contributions
AMA conceptualized the study, wrote the proposal, and reviewed the manuscript; AK conducted the analysis and contributed towards manuscript writing and reviewing, TAK and AS contributed towards proposal writing, analysis and reviewing the manuscript; HA and AA supervised the data collection, manuscript writing and reviewing. SAS assisted in analysis, and manuscript writing. All authors read and approved the final manuscript.

Acknowledgement
We shall like to thank all the participants for their time and cooperation. We shall like to      Percentage of anemic males and females by the age categories in Riyadh, Saudi Arabia