Inadequate intake of vitamins and minerals among high-school pupils in the Moroccan Rif region

1 Introduction

Adolescence is a time of rapid growth, body changes, and development of behaviors, such as eating habits. During this period, vitamin, mineral and trace element requirements increase substantially. These micronutrients are essential for growth and development, maintenance of adequate defenses against infection, utilisation of macronutrients and many other metabolic and physiological functions. Several previous studies have looked at the nutritional status of adolescents both in Morocco [1, 2] and internationally [3]. Nevertheless, nutrient intake, dietary practices and nutritional deficiencies among adolescents have generally received little attention. According to nutritional profiles published by the Morocco Health Ministry and validated by the World Health Organization (WHO), data on food consumption in Moroccan adolescents are limited.

Micronutrient deficiency is a public health concern [4]. Inadequate intake can delay somatic growth and sexual development [5]. Cognitive development is also dependent on micronutrients. For instance, B complex vitamins play an important role in neural communication, and depression may result from their absence [6]. Deficiencies in vitamin B12, folate, and thiamine may impair episodic memory and cause language problems [6]. A deficiency of iron, essential for oligodendrocyte growth and neurotransmitter production, may affect cognition, memory, and sensory and motor development [7]. Iodine is involved in regulating cellular metabolism and is essential in the early growth and development of most organs, the brain in particular; iodine deficiency causes mental retardation [8]. Attention deficits, learning difficulties, impaired memory, and possibly certain neuropsychological diseases are linked to zinc deficiency [9]. Zinc plays an important role in adolescence in growth and sexual maturation [10].

To learn about the nutritional status of adolescents, for guiding public policies to prevent deficiency diseases and chronic non-communicable diseases, it is necessary to carry out a dietary assessment in this age group. Information on food intake and dietary habits, and estimates of the adequacy of the nutrient intake can be provided by dietary surveys. Unfortunately, few studies of the prevalence of inadequate nutrient intakes among Moroccan adolescents [11] have been conducted, especially in the Rif region, where no known studies had been carried out previously. The main objective of this study was to estimate the daily intake of selected micronutrients by adolescents in the Rif region, and the prevalence of inadequate intake of these micronutrients.

2 Materials and methods

3 Results

Regardless of sex and age group, our subjects were found to be particularly at risk of inadequate intakes of vitamins E and D, calcium and potassium. Our older adolescents (14–18 years) also showed a risk of inadequate intake of folate, biotin, magnesium, iodine and zinc (among boys). This may be because our older adolescents have more freedom to choose what they eat, especially if they live with parents who do not impose their own dietary practices. A previous Moroccan study found that the degree of inadequacy in adolescents in general was partly dependent on the environment (availability of food groups), family structure (size and composition of the household), household economic conditions, and the social roles that mothers play in food access (home-prepared food) [25]. The daily intakes of vitamin A, C, B12, B6, pantothenic acid, thiamine, riboflavin, phosphorus and iron, were close to meeting the requirements in all subjects.

In our sample, most adolescents had a body mass index within the normal range. These results concord with recent studies of Moroccan adolescents [26], although we must emphasise the coexistence of underweight with overweight and obesity, a situation typical of the nutritional transition occurring in other North African countries [27].

The mean energy intake observed among adolescent boys is higher than in girls. Sex-specific quantitative and qualitative differences in their daily diets may partly explain this discrepancy, for example, the increased consumption of high energy density food groups such as cereals, oils and fats by boys [28]. In addition, the traditions and social norms still dominant in the Rif region may lead to unequal gender roles, inside and outside the home, which are associated with differences in food consumption. These include male privilege, where men eat before and more than women [29]. The average percentage contribution of total energy intake for carbohydrates, proteins and lipids estimated in this study fell within the limits set by WHO [30].

Girls aged 14 to 18 years had more nutrient-dense diets, with values significantly higher than those of boys, especially for vitamin E, thiamine, riboflavin, pantothenic acid, vitamin C and potassium. For 12 to 13-year-olds, girls had higher values only for vitamin C. No significant differences were observed for daily mean nutrient densities of other vitamins and minerals. A study carried out between 2007 and 2008 of adolescents in the region of Ouarzazate in southern Morocco gave similar results, with differences between boys and girls in usual intakes and nutritional densities of certain vitamins and minerals [11]. However, few studies have focussed on age differences in diet quality within the adolescent population. Our results are consistent with those of the National Diet and Nutrition Survey in the United Kingdom, which found no significant age differences in diet quality score in boys, but girls aged 19–21 years had a better diet quality score than girls aged 13–15 years [31]. Our finding of a more nutrient-dense diet among older girls reflects their higher consumption of fresh and dried fruits, milk and dairy products, and confectionery, documented in a previous study of the same sample [28]. The lack of local higher education institutions means that to continue their education, girls must be sent to neighbouring areas, which involves additional expense and raises social and cultural fears. Often, the easiest solution to securing a future for girls is marriage [32], and since overweight is considered by many a sign of good health and prosperity, girls will be encouraged to eat a nutrient-dense diet [33]. It has been suggested that greater variation with age is to be expected in females than males if these variations reflect lifestyle changes, [34] and that the home environment has a stronger influence on diet in females than in males [35].

As part of a healthy diet, and without exceeding energy needs, increasing intakes of vitamin D, calcium and potassium from nutrient-dense foods like vegetables, fruits, whole grains, and milk and milk products is recommended [36]. In view of the low consumption of these three nutrients in the present study, the authors have identified them as “nutrients of concern” worthy of special public health attention.

The prevalence of vitamin D insufficiency was high in all age groups and both sexes. This deficiency is widespread in the world, and can affect all population groups irrespective of sex, age or ethnicity [37]. Sebbar et al. reported a high prevalence of inadequate vitamin D intake based on reported food consumption among adolescents in the city of Oujda, in north eastern Morocco [38]. The fact that vitamin D is found naturally in only a few foods, such as fish, egg yolk, and offal may explain the high prevalence of inadequate intakes. Benjeddou et al. measured serum 25(OH)D concentration in fasting blood samples from 191 Moroccan school children aged 7–9 years, and found a high prevalence of vitamin D deficiency along with diets very poor in foods rich in vitamin D [39]. Given that the main source of vitamin D is the conversion of 7-dehydrocholesterol to vitamin D3 mediated by the action of ultraviolet B radiation from the sun on the skin, Morocco’s high levels of sunshine are probably sufficient to compensate for low dietary intake. However, Benjeddou et al. subsequently studied children living in mountainous rural areas [40]. As they have an active outdoor life and greater sun exposure opportunities throughout the year, especially during the highly sunny seasons of summer and autumn, one would expect a high vitamin D status. Yet this was not the case, even after providing the equivalent of a large glass of vitamin D fortified or non-fortified milk for daily consumption. In addition, fortification of cooking oil and milk in Morocco with vitamins A and D3 has not improved vitamin D levels, mainly due to the low consumption of dairy products [41].

The daily intake of calcium was below the EAR level. Several national and international studies have reported similar findings [42–46]. Bouziani et al. assessed by 24-hour dietary recall the calcium intake of 131 children and adolescents, finding a mean calcium intake of 522.0±297.0 mg/day, and 85.5% of subjects with inadequate calcium intakes, in boys and girls alike [46]. Contrary to our results, calcium intake differed significantly between age groups, subjects aged 14–18 years having the highest intakes. The low consumption of dairy products among our adolescents may explain the insufficient calcium intake observed [47]. The Moroccan diet, essentially Mediterranean, favours a high consumption of cereals, fruits and vegetables, with a limited consumption of dairy products. The majority of our sample came from disadvantaged groups, who prefer Moroccan mint tea to milk-based drinks. In addition, some components such as oxalates in spinach and phytates in cereals highly consumed by our sample reduce the bioavailability of calcium [28]. Particular attention must be paid to these adolescents, whose calcium needs are not being met, with a view to improving their current consumption patterns.

In our study, potassium consumption is below the recommended intake level for almost all adolescents. These results are in agreement with those obtained with 24-hour urinary potassium excretion analysis in a descriptive cross-sectional study of 131 children and adolescents attending public schools in Rabat and the surrounding area [48]. This study recorded a mean daily urinary potassium excretion of 1431±636.5 mg/day, with an inadequate intake in 75% of children. This highlighted an unusually low consumption of foods that are good sources of potassium, especially fruits, vegetables, legumes, potatoes, meats, poultry, fish, milk, yogurt, and nuts.

Adolescents in our study are particularly at risk of inadequate intake of iodine, the risk being highest in the 14–18 year age group. In 1995, Morocco adopted WHO recommendations for universal salt iodisation to combat iodine deficiency disorders by fortifying salt with iodine, passing legislation and establishing standards to ensure the programme’s sustainability. Twenty years later, a 2016 study showed that iodised salt use is still far from widespread, with only 25% of Moroccan households using iodised salt, and only 4.5% of iodised salt meeting the regulatory standard median iodine concentration of 17.8 mg/kg [49]. Our results are somewhat unexpected since our study was conducted in a coastal area. Studies in the Moroccan capital Rabat [48] and Larache in the north [49], both coastal cities, found similar levels of inadequate iodine intake. It would appear that iodine deficiency is not influenced by the proximity of the sea, although higher iodine levels in populations living in coastal regions and a higher prevalence of iodine deficiency in the interior have previously been observed [2]. More emphasis must be placed on the importance of dairy products, eggs and seafood in maintaining an adequate iodine status in the nutrition education of adolescents.

Except for boys aged 12-13 years, adolescents in our study are particularly at risk of inadequate intake of vitamin E. This deficiency can be attributed to a diet very low in plant-based oils, nuts, seeds, fruits, and vegetables. Although exclusively obtained from the diet, vitamin E deficiency is extremely rare in humans, except children [50]. Similar results have been reported in a Brazilian study on the intake of macro- and micronutrients in adolescents [44] and in the National Dietary Survey on the Child and Adolescent Population in Spain [45].

In our sample, a high proportion of adolescents aged 14–18 years reported an inadequate folate intake. Other adolescent studies have found similar results [11, 51]. This low folate status is likely attributable to a low intake of vegetables and fruit. Folate-rich food sources include leafy vegetables, legumes, nuts, fruits and berries. A significant amount of folate is lost during food preparation and cooking, and Moroccans prefer well-cooked vegetables. The effect of socioeconomic conditions must not be overlooked, as some studies have indicated that poor and rural populations may be at greater risk of folate deficiency than more affluent and urban populations [52], despite the fact that flour in Morocco is fortified with folate. The low folate intake among study participants suggests that alternative solutions need to be found, such as the fortification of foods other than flour.

Biotin is widely present in small amounts in natural foodstuffs. Our results show a deficiency of this vitamin in adolescents aged 14–18 years of both sexes. The same result was recorded in the survey conducted with adolescents in Ouarzazate which found 83.1% of boys and 79.4% of girls with inadequate biotin [11].

The daily magnesium intake was insufficient in the majority of boys and girls aged 14–18 years. A Spanish study found inadequate magnesium intake in 63.5 % of boys and 81.8 % of girls aged 14 years and over [45]. Conversely, adolescents in Ouarzazate in southern Morocco met their magnesium requirements [11]. Our result may be explained by dietary differences between northern and southeast Morocco especially in the consumption of magnesium-rich foods, as well as the greater availability on the North Moroccan market of refined and processed foods with low magnesium contents [53].

Daily zinc intake was low in boys aged 14–18 years, similar findings having been observed in several studies, in Ethiopia, Nigeria, South Africa and India [54, 55]. Dietary habits and the poor bioavailability of zinc in cereal-based diets with a high phytate content may put adolescents from developing countries like Morocco at a high risk of zinc deficiency [56].

Concerning the contribution of different food groups to the intakes of the three micronutrients studied, cereals and cereal products are still a major component of the Moroccan consumption model [57]. Flour, which is consumed mainly in the form of soft wheat flour, dominates cereal products with a share of 67.5% of the total [58]. Milk and milk products were the main contributors to calcium intake for our adolescents. The micronutrient contribution from spices and condiments group differed from one element to another, but it occupies the first place for sodium. In our study area, spices are omnipresent in typical Rif region dishes. The main spices are paprika, cumin, turmeric, aniseed, cinnamon, saffron and coriander, which is one of the main ingredients of Rif cuisine. Sources of vitamins and minerals, spices are important for a healthy diet [59, 60].

Fish, eggs and meat contribute significantly to calcium and sodium intakes. Fish is an important source of vitamins and minerals, such as vitamin D, selenium, phosphorus, and calcium, as well as valuable lipids and proteins. Chicken eggs are considered a good source of phosphorus, sulfur, potassium, sodium, chloride, calcium, and magnesium, and of most vitamins, except vitamin C, such as vitamins A, D, E, choline, folic acid, pantothenic acid, and niacin. Meat is a good source of zinc, iron, selenium and phosphorus, as well as vitamin A and B-complex vitamins, However, meat is consumed less by households due to its price. Occupying an important place in the Moroccan diet, fruit and vegetables contribute an important portion of vitamins and minerals, especially folate.

This study has some limitations and strengths. Excluding adolescents who do not go to school, our sample of high school students may not be representative of all adolescents living in the region. There is a risk of selection bias due to the self-selection of participating pupils, but this was unavoidable as recruitment was voluntary. The randomised selection of classes helps to reduce selection bias.

Despite the calculation of an appropriate sample size based on statistical parameters prior to conducting the study, the desired sample size was not achieved (302 instead of 325). However, the quality of the results was enhanced through the exclusion from the analyses of participants who showed insufficient understanding of the study, judged by the inconsistency of their answers.

The food composition tables used may not represent accurately the nutrient composition of the Moroccan diet, which is likely to vary with the seasons, or in variety. Precise measurements of the amount of food consumed are difficult to obtain, a common problem in studies of populations where meals are eaten from a shared plate. Misreporting is likely for meals such as fast food taken outside the house, and in the estimation of their portion sizes. The assessment period in our study covered a specific period of the year, so seasonal variations in diet cannot be taken into account. Among the main strong points of the present study is the use of a 3-day food consumption record which provides numerous details about the types and quantities of food consumed and is less prone to recall bias than other methods.

5 Conclusion

Our study provides data on the dietary intake of vitamins and minerals in food and beverages of a sample of Riffian adolescents. Regardless of gender and age group, our subjects were found to be particularly at risk of inadequate intakes of vitamins E and D, calcium and potassium. Older adolescents (14–18 years) also showed a risk of inadequate intake of folate, biotin, magnesium, iodine and zinc (among boys). While the authors support the policy of fortifying foods with micronutrients such as folate, iodine, and calcium, fortification has not proved sufficiently effective, for example, in improving vitamin D status. Because an adequate nutrient intake in adolescence is of crucial importance for health later in life, nutrition education programs are necessary to promote healthy eating habits and encourage children and adolescents to maintain the diverse traditional Moroccan diet rich in cereals, vegetables, and fruit, which are essential sources of micronutrients. Interventions such as nutrition education for adolescents may be more effective than fortifying foods.

To deepen our knowledge of micronutrient deficiencies in Moroccan adolescents and their effect on their future health as adults, further studies are desirable, which include the clinical and biological assessment of nutritional status, as well as the regular collection of quality and nationally representative micronutrient data.