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A review of adolescent nutrition in South Africa: transforming adolescent lives through nutrition initiative

Objective: In South Africa, urbanisation is associated with substantial burdens of adolescent overweight and obesity, making teenagers vulnerable to longer-term non-communicable diseases. In addition, as potential future parents, the nutritional status of adolescents is increasingly recognised as a key driver of health and well-being in the next generation. This review reported on the available literature examining nutritional status and dietary intakes and practices, as well as their determinants, in South African adolescents. Study design and methods: Medline (Pubmed), Web of Science and EMBASE were searched for relevant articles published between 1994 and May 2018. Applicable search terms and phrases were identified in study titles and/or abstracts and full-text articles were reviewed according to inclusion/exclusion criteria. Data were extracted according to specific review objectives. Results: A total of 67 relevant studies were identified. Only one study used a biochemical marker to describe adolescent nutritional status (vitamin D status; 25(OH)D). Overweight and obesity prevalence increased in South African adolescents over the reference period, with national increases of 6% in boys and 7% in girls between 2002 and 2008. Girls and urban-dwellers were particularly vulnerable to excess adiposity. Dietary intakes demonstrated a transition towards energy-dense, processed foods high in sugar and fat, but low in essential micronutrients. Food choices were driven by the adoption of obesogenic behaviours in the teenage years, including irregular breakfast consumption and fewer family meals, increased snacking and low levels of physical activity. Conclusion: South African adolescents — particularly girls — are increasingly burdened by obesity as a result of urbanisation-associated shifts in dietary intake and eating behaviours. However, the implications for micronutrient status and long-term nutritional health are not known. Additionally, more data on the clustering of diet, activity and sedentary behaviours in adolescent boys and girls is needed, as well as on behaviour patterns to facilitate healthy growth and reduced adiposity. individual-level body-image dissatisfaction, parental criticism of body size and endorsement of dieting behaviour by peer groups.


Introduction
Adolescence is a period of growth and development that is increasingly being recognised as a critical window for optimising the health and well-being of current and future generations. 1,2 While it is principally defined by the puberty-associated physiological changes that characterise a child's transition to adulthood, adolescence encompasses a range of developmental changes that form the foundation of one's ability to thrive physically, socially and emotionally as an adult. 1,3 In addition, the interplay between early life (prenatal, infant and childhood) growth and development and the physical and social environment experienced during adolescence may play a critical role in shaping the health trajectory of an individual, as well as of any future offspring. 2,3 It is widely accepted that optimising growth and development during the first 1 000 days of life can result in substantial benefits, namely: reductions in childhood morbidity and mortality risk; improvements in cognitive and motor development, school performance and economic productivity in adulthood; and reductions in the risk of becoming obese or developing non-communicable diseases (NCDs) in later life. 4 While the importance of maternal nutrition and lifestyle in programming early growth and development is well established, research and intervention strategies have focused largely on nutritional status, diet and physical activity during pregnancy when the maternal risk profile is already established and the scope for affecting both maternal and infant outcomes is limited. [5][6][7] In addition, there has been a lack of focus on the role that paternal nutritional status, attitudes and behaviour may have on the offspring both physiologically and at the level of partner and/or parental influence. 2,8,9 As shown recently by Patton et al., prioritising adolescent nutritional status in both females and males, as well as promoting healthy attitudes and behaviours around diet, physical activity, substance use and stress in this population, are critical to improving the intergenerational transmission of health and well-being. 2 In addition, it provides a window for intervention, during which investment is likely to yield substantial benefits for health, social development and economic growth and capacity. 2,10 Adolescents and youth (10-24 years of age) constitute almost one-quarter of the world's population, with more than 80% of this group living in low-and middle-income countries (LMICs). 11 While improvements in childhood nutrition and health, education and rapid technological advancements, as well as access to effective contraception and delayed timing of parenthood, provide a platform upon which adolescents should thrive, their health and well-being face substantial threats during this time. 1,3 As individuals progress through adolescence their exposure to social health determinants undergoes a considerable shift. This means that the parental/family-dominated determinants of lifestyle choices in childhood expand to include the influence of peers, the community, culture, education, the media and the economy. 10 Within this context, growing levels of independence make adolescents highly susceptible to the adoption of obesogenic behaviours that may persist into adulthood, thereby increasing the risk of obesity and NCDs in later life. 1,10,12,13 In LMICs rapid urbanisation exacerbates this by exposing young people to increasingly Westernised dietshigh in saturated fat, added sugar, salt, processed/convenience foods and edible oils-in environments characterised by low levels of physical activity. [14][15][16] This is particularly relevant in sub-Saharan Africa where overweight and inactivity rates are comparatively higher than in other LMIC regions. 17 In South Africa, where this nutrition transition has progressed considerably, approximately 27% of females and 9% of males are overweight or obese by 15-19 years of age, with those living in urban settings being particularly vulnerable. 18 Additionally, since the dawn of South Africa's democracy in 1994, policy changes around food production, composition and availability, as well as economic accessibility and education, have further reshaped the landscape of food consumption and activity patterns, predominantly in previously restricted black communities. [19][20][21] These policy changes are outlined in Table 1. Particularly since 1994 school feeding programmes have been implemented and expanded, and child support grants established, to improve food security at both individual and household levels. In 1995 a multi-sector policy aimed at addressing both clinical (leading to hospitalisation) and sub-clinical malnutrition was introduced and in 2003 a mandatory micronutrient fortification policy for maize and wheat was developed. More recently policies for salt reduction (2016) and sugarsweetened beverage taxation (2017) were introduced in response to the country's rising obesity and NCD burdens. While these government policies highlight that nutrition-based issues are on the national agenda, their coverage and effectiveness are widely debated and their impact on adolescent nutrition is less clear.
Although individual studies have explored nutritional status, dietary intake and physical activity, as well as perceptions and attitudes around healthy eating and body image in rural and/ or urban South Africa, relationships between these components and their determinants are not known. A comprehensive examination of nutritional health and well-being in the adolescent population is therefore critical to understanding the possible means of addressing the rapidly growing obesity epidemic in this-and future-generations.
In this review our aim was to report on the available literature examining nutritional status and dietary intake and practices, as well as their determinants, in South African adolescents. Data were therefore reviewed according to five specific Table 1: National policy changes that may impact adolescent nutritional status in South Africa  Policy area/programme Year Action (s) objectives that summarised the following variables in rural and/ or urban South African adolescents (10-20 years): (1) nutritional status (anthropometric, biochemical and dietary indicators of macro-and micronutrient intakes); (2) food consumption, dietary patterns and eating habits; (3) diet, eating habits and demographic and lifestyle factors (age, setting, socioeconomic status (SES) etc.) and their associations with adolescent adiposity (e.g. body mass index [BMI]/fat mass); (4) body image perceptions and eating attitudes; (5) qualitative perceptions of, and attitudes towards, healthy eating and physical activity.

Search strategy
Comprehensive literature searches were performed in March 2018 by a team of researchers. Searches identified all available studies describing adolescent nutritional status, and its determinants, since the establishment of democracy in 1994. Searches were conducted using the following databases: Medline (Pubmed), Web of Science and EMBASE. Searches included the following search terms and phrases, as well as any applicable variations: adolescent and anthropometry/(specific anthropometric measure of interest, e.g. body mass index)/nutrition/(specific nutrient of interest, e.g. protein or iron)/(specific micronutrient deficiency of interest, e.g. anaemia)/(specific nutritional biomarker of interest, e.g. ferritin)/ (specific dietary intake assessment method of interest, e.g. food frequency questionnaire) and Africa (full description of search terms is provided in Supplementary Appendix A). Search terms and phrases were used in various combinations for identification in study titles and/or abstracts. Full-text articles were obtained and reviewed to select those meeting the inclusion/exclusion criteria described below. Data were subsequently extracted from relevant publications into appropriate tables.

Selection criteria
Inclusion criteria 1. Studies conducted in South Africa.
2. Studies conducted in males and/or females aged 10-20 years.

Any study design.
For observational studies: . studies that described adolescent nutritional status (assessed using anthropometry and/or objectively measured body composition [weight and/or height and/ or BMI and/or waist circumference and/or body fat percentage] and/or biochemical indicators and/or reported dietary intakes) as an exposure and/or outcome; and . studies that used quantitative methods to assess attitudes and/or perceptions and/or degree of satisfaction towards nutritional status (body size, composition, diet) or behaviours.
For intervention studies: . nutritional intervention studies done in adolescents (with or without physical activity component(s) incorporated) with dietary values and/or where biochemical indicators from both the intervention and control group could be extracted.
For qualitative studies: . studies that explored thoughts on dietary behaviours and practices (with or without physical activity) and their determinants; . studies that explored perceptions and attitudes towards healthy dietary and lifestyle (e.g. physical activity) practices; . studies using any of the following qualitative research methods: observations, face-to-face interviews, focusgroup discussions; and . studies using any qualitative analytical methods.

Studies published in peer-reviewed journals and/or as academic dissertations
Exclusion criteria 1. Studies conducted in animals.
2. Studies conducted in languages other than English.
3. Studies published prior to 1994. 4. Studies which do not describe nutritional status (anthropometry and/or biochemical indicators and/or reported dietary intakes) using aggregate data summarised as mean (SD) and/or median (IQR or 95% confidence interval).
The results of the included scientific papers are structured and presented below according to the specific review objectives.
No weighting was applied across studies and therefore the data presented are actual findings per study.
Median energy intakes were similar in rural adolescents at 9-13 and 14-18 years of age (7 172  In the North West province, 10-15-year-old boys and girls had mean energy intakes of 8 014 kJ/d and 7 397 kJ/d respectively. 30 Mean fat intake was 56 g/d for boys and 53 g/d for girls, thereby contributing to 26.5% and 27.1% of daily energy intake in boys and girls respectively. 75 Energy, macro-and micronutrient intakes were similar in stunted compared with non-stunted 10-15-year-old black adolescents. 25 35 Daily intakes of all macro-and micronutrients similarly increased with age; however, increases in protein (56-59 g/d) and fibre (22-23 g/d) intake were small compared with those of carbohydrate (279-323 g/d), fat (51-70 g/d) and added sugar (68-102 g/d). 35 Intakes of calcium, iron, zinc, vitamin A, riboflavin and niacin were below the RDA at 10 and 13 years, while vitamin B6 and vitamin C intakes were below the RDA at 10 years only (data not shown). 35 Food intakes, diet patterns and eating practices ( The odds of higher 'Unhealthy Dietary Pattern (UDP)' scores were 2.77 times higher in the lowest vs. highest SES group (SES defined according to a combined scale of annual household income and highest level of parental education). 84 In addition, adolescents attending high SES schools had better knowledge of healthy vs. unhealthy foods (p < 0.01) and were more likely to bring a lunchbox to school (p < 0.001). 33 Lunchbox usage was associated with younger age and urban school attendance (p < 0.001), as well as higher standards of living (p < 0.001), dietary diversity scores (p = 0.012) and number of meals per day (p < 0.001). 43 In addition, adolescents who brought food to school had lower BMI percentiles (p = 0.002) and BMI-forage (p = 0.034) than those purchasing food at school. 43 Overall, 'unhealthy' food items were brought to school twice as often as 'healthy' foods and 70% of adolescents who purchased food at school reported purchasing no healthy items. 33 Many adolescents (47-61%) could not correctly identify less healthy food items (including sugar-sweetened beverages, samosas and pies). 33 In urban adolescents, the most commonly consumed food items were: rice, stiff maize-meal porridge, chicken, added sugar, sweets, tea, eggs, full-cream milk, carbonated beverages and oil. 36 Consumption of grains, dairy products and fruits and vegetables decreased and consumption of meat and meat substitutes (e.g. chicken, cheese and polony) and oil increased with age. 36 Between the ages of 13 and 17 years, regular breakfast consumption and lunchbox usage decreased, with adolescents purchasing more food at school. 46,57 Snacking while watching television increased with age (3.6 ± 4.6-6.7 ± 5.9 snacks/week), with girls consuming significantly more snacks than boys (p < 0.01). 46 Over two-thirds of adolescents consumed fast foods and sweetened beverages three or more times/week, with median intakes reaching 11 fast-food items per week in both sexes and 8 and 10 sweetened beverages per week in males and females respectively at 17 years. 57,61 Confectionery consumption was high across the five-year follow-up (9-10 items/ week) and reached 11 items per week in boys and 13 items per week in girls at 17 years. 46,61 Approximately three times the American Heart Association (AHA) recommended daily intake of added sugar was consumed via purchased food items (males: 561.6 g/week vs. females: 485.3 g/week; p = 0.02). 61,95 These items also contributed over half the AHA recommended daily intake of salt (males: 4 803 mg/week vs. females: 4 761 mg/week; p > 0.05) in adolescents. 96 The 'kota' (quarter-loaf of white bread filled with chips, a slice of cheese and delicatessen meats and sauces) was the least expensive and most regularly purchased fast food item at 17 years. 37 This item alone provided over half the estimated daily energy requirement (ER) containing, on average, 5 970 kJ of energy and 51 g of fat. 37,97 Compared with urban adolescents, rural girls and boys demonstrated significantly lower snack consumption while watching TV during early adolescence (EA; 11-13 years) and significantly lower fast food consumption during mid-adolescence (MA; 14-15 years). 87 Significantly more rural girls (EA: 51.02%; MA: 48.51%) than boys (EA: 33.33%; MA: 28.57%) consumed their main meal with the family almost every day. 87 Consumption of a dietary pattern driven by animal-derived nutrients was higher in rural girls vs. boys and in adolescents with higher SES (based on a Wealth Index) (P < 0.05). 73       A review of adolescent nutrition in South Africa week). 76 FVSs were highest for those with high scores on the nutrition knowledge questionnaire (NKQ). 76 Additionally, NKQ scores were inversely associated with carbohydrate, total fat and added sugar intakes and positively associated with protein intake. 76 Associations between diet and lifestyle factors and adolescent adiposity (Table 6) Thirteen studies met the inclusion criteria. 24,31,32,44,49,57,62,63,71,73,77,82,87 Exposure variables were largely questionnaire based and included assessment of demographics, SES and household food security, 44,71,77 dietary intake (FFQ), 31,73 dietary habits and eating practices, 57,87 physical activity and sedentary behaviour, 31 as well as body-image perceptions, satisfaction and dissatisfaction and eating attitudes. 24,31,32,62,63,82 Only one study used anthropometry (birth to two years of age) as the exposure. 49 Anthropometry was used to assess adolescent adiposity in all studies and measurements included weight, height and BMI. Additionally, two studies included DXA assessed fat mass. 49,57 Underweight and severe stunting prevalence rates were significantly higher in urban boys vs. girls across adolescence (13-19 years of age). Overweight/obesity prevalence was significantly higher in girls from both rural and urban settings (11-19 years). 71,77,82,87 A 1 SD increase in birthweight was associated with 0.22 higher BMI z-score and 1 051 g higher fat-free mass at 10 years of age (p ≤ 0.01). 49 Additionally, underweight at one year was associated with lower fat-free mass, and stunting at one and two years was associated with lower fat-free and fat mass at 10 years of age (p ≤ 0.01). A 1 SD increase in weight-for-age z-score (WAZ) between birth and two years of age was associated with adolescent adiposity (BMI and fat mass; p ≤ 0.01). 49 Urban black girls had higher BMIs than both their white and mixed ancestry counterparts (black: 24.1 ± 3.3, mixed ancestry: 22.1 ± 3.7, white 21.9 ± 3.0 kg/m 2 ; p < 0.05) between 15 and 18 years of age. 24 White girls were significantly taller (p < 0.001), had higher hip circumferences (p < 0.05) and participated in more formal, but less informal, physical activity (p < 0.05), than black girls. 31 In black girls only, sedentary time was positively associated with energy intake (p < 0.01) but not with body size. 31 Animal-driven nutrient pattern adherence was positively associated with adolescent BMI z-score in 11-15-year-olds (0.13 per + 1 SD; p = 0.02) and longitudinal sweetened beverage consumption was positively associated with BMI z-score and fat mass in boys at 17 years (p < 0.05). 57,73 For urban and rural adolescents, higher odds of overweight and obesity was associated with consumption of fewer family-based meals (i.e. eating the main meal with the family on some days or almost all days) and irregular breakfast consumption on weekdays. 87 Stunting prevalence (13-15 years) was lowest in adolescents with a high household SES (high SES: 18.1%; medium SES: 30.4%; low SES: 31.4%; tertiles based on occupation and highest education level of the household's 'breadwinner'). 71 Rural dwelling was associated with lower odds of overweight and obesity; however, this was seen only during early adolescence (11-13 years) (OR: 0.55 [0.32, 0.92]; p ≤ 0.02). 87 Odds of a high body fat percentage (%fat; > 85th percentile) at 17-19 years was higher in females who lived in neighbourhoods with a low social support index (OR: 1.59; 95% CI: 1.03, 2.44), as well as in males with higher household wealth index (OR: 0.28; 95% CI: 0.10, 0.78). 77 There was an inverse association between body image dissatisfaction and BMI in girls (p= 0.0001); however, overweight girls had a higher tendency towards a disordered body image than their normal-weight counterparts. 24,63 Across rural and urban settings, BMI was lowest in those who desired to be larger and highest in those desiring to be thinner (13-18 years). 32 A higher overall 26-item Eating Attitudes Test (EAT-26) score in girls (representing a greater tendency towards developing an eating disorder) was positively associated with BMI (white girls: p = 0.0001; black girls: p = 0.038) 63 and a higher dieting subscore was positively associated with weight, BMI and hip circumference in black girls specifically (p < 0.01). 31 Underweight girls had significantly lower EAT-26 scores than the other BMI groups. 24 For white boys, self-esteem was positively associated and dieting was inversely associated with BMI (p = 0.01 and p = 0.004 respectively), while in black boys lower bulimic and oral control scores were associated with higher BMIs. 62 Body image perceptions and eating attitudes (Table 7) Twelve studies met the inclusion criteria. 22,24,26,31,32,55,58,62,63,69,70,82 Data collection was questionnaire based and focused on the following: eating attitudes (26item Eating Attitudes Test; EAT-26), 22,24,26,31,58,62,63,69,82 58,62,63,82 National data showed that 84.5% of adolescents (15-18 years) had distorted body images (i.e. they either under-or overestimated their current body size) and 45.3% were dissatisfied with their body size. 70 Overweight and obese adolescents tended to underestimate their body size and desired to be thinner, while normal and underweight adolescents overestimated their body size and desired to be fatter. 55,70 Some 16.7% and 38.8% of urban white and black girls respectively had high body image dissatisfaction, with significantly more black vs. white girls being dissatisfied with their body image at 13 (p = 0.04), 15 (p = 0.001) and 17 (p = 0.0001) years. 63 In addition, significantly more black girls were at risk of developing an eating disorder (EAT-26 scores ≥ 20) than their white counterparts, with higher reported scores on the bulimia and/or oral control subscales. 22,26,63 In contrast, white girls idealised a smaller body size than their mixed-race or black counterparts. 24 Low self-esteem and a desire to be thinner was more common in white compared with black girls. 32,63 For rural girls, the desire to be thinner was higher in early puberty (Tanner stage ≤ 2) compared with mid-to postpuberty (Tanner stage > 2) (61.4% vs. 55.9%), while the desire to be fatter was lower in early vs. mid-to post-puberty (18.6% vs. 29.7%). 82 The majority of males and females in both pubertal groups perceived the underweight silhouettes to be 'unhappy' and 'weak'. In addition, the majority of females (early and mid-post-puberty) perceived the normal silhouette to be the 'best'. There were no differences in the risk of developing an eating disorder by sex or age; 10.5% and 10.6% of boys and girls respectively had an EAT-26 score ≥ 20 in early puberty, while in mid-puberty 7.1% of boys and 8.0% of girls scored ≥ 20.
For boys at 13, 15 and 17 years of age, body image dissatisfaction and risk of a disordered eating attitude were higher in Birthweight was associated with a 0.22 higher BMI z-score and 1 051 g higher fatfree mass at 10 years of age (per + 1SD; p ≤ 0.01) Stunting at one and two years was associated with lower fat mass and fat-free mass respectively at 10 years of age (p ≤ 0.01) Underweight at one year was associated with lower fat-free mass (p ≤ 0.01) 1 SD increase in WAZ between birth and two years was associated with fat mass and BMI at 10 years of age (p ≤ 0.01)      At 17 years, the normal weight silhouette was perceived as the 'best', as 'getting respect' and as the 'happiest' for boys and girls The obese silhouette was associated with being the 'worst' and 'unhappiest' The underweight silhouette was perceived as the 'weakest' Significantly more urban black vs. white adolescents (13, 15 and 17 years) perceived higher BMIs to be the 'best', the 'happiest' and to have 'more respect'. 62,63 However, in the BTT cohort at 17 years of age, both black and mixed-ancestry adolescents assigned these attributes to a normal weight silhouette. 58 Black and mixed-ancestry adolescents perceived the obese silhouette to be the 'worst' and to be 'unhappy' at 17 years of age. 58 However in 13-, 15-and 17-year-old black and white boys, this silhouette also symbolised 'strength'. 62 The underweight silhouette was perceived as the 'weakest' by black boys and girls and as getting the 'least respect' by black boys only. 58,62 Qualitative research: perceptions of, and attitudes towards, dietary and lifestyle behaviours (Table 8) Four qualitative studies met the inclusion criteria, all of which were conducted in girls. 51,52,68,83 Data were collected using semi-structured 'duo-interviews' (friend pairs) in three studies 51,52,68 and individual in-depth interviews in one study. 83 Breakfast consumption in the home was not prioritised and lunchboxes were not commonly used by urban girls. 52 Instead, girls preferred to purchase locally prepared convenience foods -commonly 'kotas', 'fat cakes' (deep-fried dough balls) and other snack foods-from vendors and the school tuck shop. 52 Food choices were driven by affordability, convenience and peer influence, as well as popularity of the food items. 51 In rural girls the importance of eating breakfast was acknowledged and locally grown, traditional foods-mainly fruits and vegetables-were perceived to be healthy. 68 Female caregivers and school meal programmes were viewed as facilitators to eating healthy diets. 68 Limited household food availability and accessibility to healthy foods acted as barriers to regular breakfast consumption, as well as drivers of 'convenient and less healthy food' consumption.
Active recreational activity was minimal in urban girls, largely due to a lack of facilities and safety concerns. 52 Physical activity was more common in rural girls, with various activities-including household chores, walking to school, traditional dancing and extramural activities (e.g. netball, soccer)-reported. 68 Many rural girls believed that engaging in these activities was beneficial to their health.
For girls in Limpopo, body dissatisfaction was common, with many desiring to be thinner than they were. 83 A variety of factors influenced girls to control their weight, including

Discussion
Using a systematic approach, this review aimed to report on the available data on nutritional status and dietary intake and practices, as well as their determinants, in South African adolescents (10-20 years).

Adolescent nutritional status Anthropometry and body composition
Using BMI, national data showed an overall increase in overweight and obesity prevalence in South African adolescents over time (2002)(2003)(2004)(2005)(2006)(2007)(2008), with approximately 14% of boys and 36.5% of girls between 13 and 18 years of age being overweight or obese in 2008. 38,39 However, this is coupled with persistently high stunting prevalence, affecting as many as a third of 13-15year-old boys and girls in the urban Free State. 71 Dual burdens of under-and overnutrition are widely documented in LMICs and have been linked to rapid urbanisation and a transition towards diets high in saturated fat, sugar, salt and processed foods and low in essential micronutrients, as well as decreased levels of physical activity. 4,15,16 In South Africa the coexistence of unyielding chronic undernutrition and increasingly prevalent obesity is well established and documented across the life course even at individual household levels, making tackling malnutrition in this context highly complex. 45,98 Sex differences in under-and overnutrition were evident across studies, with the majority showing higher overweight and obesity prevalence-as well as central adiposity (waist circumference), sum of skinfolds and %fat-in girls and higher stunting prevalence in boys. While the differences between girls and boys were shown across age categories, they became more pronounced as adolescents aged, with girls experiencing substantial increases in adiposity from mid-to late adolescence. The disproportionate burden of obesity in adult females is well documented in South Africa-as well as across most LMICs. 18,99 These data suggest that adolescence may be a critical period of divergence in risk profiles between sexes, triggering high levels of fat deposition in girls from around the onset of puberty.
Across South Africa, urban adolescents tended to exhibit higher overweight and obesity prevalence than those from rural settings. Such urban-rural differences have been identified across LMICs and are supported by diet and activity changes, which result as food environments and access, infrastructure, occupation and transport become increasingly urbanised. 99 However, as the degree of urbanisation becomes more extensive and rural communities are increasingly exposed to obesogenic environments and behaviours, this gap in nutritional profiles is rapidly reduced, with one study documenting higher mean BMI in rural compared with urban black girls from Gauteng province. 32 Studies from other LMICs have suggested that, in such cases, the rate of increase in overweight and obesity may be even higher in some rural compared with urban communities. 99

Biochemical markers
Only one article was retrieved that described nutritional status using any biochemical marker, highlighting the scarcity of data on adolescent micronutrient status in South Africa. Although this study showed low levels of vitamin D deficiency in both white and black urban adolescents-and adequate vitamin D status has been linked to a range of positive adolescent health outcomes-the levels required for optimal health are widely debated. 48,100 In addition, status of any single micronutrient in isolation is not reflective of highly interactive multi-nutrient profiles or dietary micronutrient adequacy, particularly for vitamin D, since diet is not typically the primary source. 73,100 This phenomenon is common across African populations, with available data being largely limited to single micronutrients or deficiencies and their associations with particular outcomes of interest in isolated target groups. 101 While such studies are useful, they do not take into account the complex nature of micronutrient deficiencies, which tend to occur in combination, particularly in populations of low socioeconomic status with low dietary diversity. More evidence is needed to understand the profiles of multi-micronutrient status and deficiencies in adolescents, as well as the diet and lifestyle determinants and health consequences of these in both the short and longer term.

Reported dietary intake and eating habits
Overall, in both rural and urban settings, energy intakes between 10 and 15 years either met or fell below the ER. 97 In rural adolescents, there was no change in energy intake between younger (9-13 years) and older (14-18 years) age groups. 75 This was surprising given the increase in adiposity during the later adolescent period, particularly in girls. However, these data were collected in a single rural population where food insecurity is common and almost 90% of adolescents consume diets of low food variety (i.e. < 30 food items per week). 76 This suggests that the monotonous diets of low dietary diversity, typically associated with poverty, persist in more isolated rural South African settings and intakes may not be comparable to those of the increasingly urbanised communities. 102 This is supported by the dietary habits demonstrated in rural adolescents who maintained more traditional eating behaviours than their urban counterparts, being more likely to partake in family meals and to consume fewer fast-food and snack-food items. 87 In addition, during qualitative interviews, rural girls reported household food availability to be a key driver of healthy eating behaviours such as regular breakfast consumption. 68 In urban adolescents, energy intake increased with age, predominantly driven by increased intakes of carbohydrate, fat and sugar. 35 This was reflected in the types of food consumed, with lower fruit, vegetable and dairy intakes and higher processed meat, oil, fast-food and sugar-sweetened beverage intakes reported at older ages. In addition to changes in patterns of food consumption, older adolescents were less likely to eat breakfast and carry a lunchbox to school and were more likely to purchase food at school and to snack while watching TV. Such dietary behaviours were associated with lower dietary diversity and meal frequency and higher adiposity, as well as increased consumption of convenience food products. 43 These purchased items contributed substantially to the total added sugar and salt intakes of adolescents. 61 This is supported by studies in both high-income and LMIC settings, which demonstrates the adoption of obesogenic behaviours as adolescents age and gain independence. 10,12,103 Poor dietary habits were reflected in the micronutrient intakes of adolescents, which were low across studies in both rural and urban settings.  23,35 However, the persistently low micronutrient intakes documented in later studies suggest that potential benefits of food fortification may be insufficient to allow for substantial changes in the proportion of adolescents meeting recommendations. 75,76 In addition, poor micronutrient intakes are documented across South African populations and have been, in part, linked to food insecurity and low accessibility to more expensive high-protein and micronutrient-rich foods. 106 This is supported by Manyanga et al., who showed higher odds of an unhealthy dietary pattern in adolescents from the lowest SES group. 84 In addition, those with low SES demonstrated lower knowledge around healthy foods, with higher knowledge being associated with increased food variety, as well as lower carbohydrate, fat and added sugar and higher protein intakes. However, South African adolescents demonstrated poor knowledge of unhealthy foods overall, being unable to classify high fat and sugar products such as pies, samosas and sugar-sweetened beverages as unhealthy items. Sugar-sweetened beverage consumption has been identified as one of the key drivers of obesity and was positively associated with adiposity in urban South Africa boys at 17 years. This suggests that interventions aimed at improving education around diet and health may be beneficial in shaping healthier food choices and improving dietary diversity in adolescents. However, this would require multi-sector involvement in prioritising nutrition and health within the education system-potentially at school level-as well as ensuring adequate access to healthy food at home, school and community levels. In addition, encouraging healthy-eating behaviours-such as eating breakfast, carrying lunch to school and eating meals as a familymay be beneficial in improving dietary intake and nutritional status in adolescents and their families.
Although the findings of this review support urbanisationassociated changes in the diets of South African adolescents, which become more pronounced with age, data fail to explain the substantial increases in adolescent adiposity, particularly in girls. While some differences in eating behaviour were identified between boys and girls-with girls consuming more snack and confectionery items than boys-energy, macro-and micronutrient intakes were largely similar. Understanding the interplay between diet and physical activity in adolescents as they age may therefore be an important component in explaining these differences. While studies exploring activity and sedentary behaviour patterns in South African adolescents are limited, available data suggest low activity levels in girls, particularly in urban settings and at older ages. 107,108 This is supported by data from high-income countries (HICs), which show that older, female adolescents demonstrate clusters of behaviour defined by low levels of physical activity. 12 In addition, data suggest differences in the types of sedentary behaviour adopted by girls and boys, as well as high clustering of unhealthy activity and dietary behaviours. 12 These may be important factors in targeting future interventions. Future studies should therefore investigate the clustering of diet, physical activity and sedentary behaviour in South African boys and girls, as well as what may be driving distinct clusters of both healthy and unhealthy behaviour between sexes.

Body-image perceptions and eating attitudes
This review found that, in general, white girls desire to be thinner more commonly than their black or mixed-ancestry counterparts and tend to prefer a smaller body size, with rural black girls having the lowest desire to be thinner. This is supported by the fact that black adolescents believed higher BMIs to be the 'best', the 'happiest' and to receive the 'most respect', while underweight silhouettes were perceived as the 'weakest'. Similar findings have been documented between black and white girls in HICs, with black girls desiring to be thinner at comparatively higher BMIs. 109,110 Ethnic differences around desirable body size are maintained in adulthood and have been associated with cultural ideals, as well as stigmatisation of thinness in African settings. 111,112 However, despite a preference towards a higher body size, black South African adolescents had more disordered eating attitudes than their white counterparts, with higher scores for oral control documented across studies. A previous study comparing urban and rural black South Africa women suggested that the EAT-26 may have poor applicability to rural settings, due to misinterpretation of the questionnaire in a food-insecure context. 113 This may similarly explain the differences exhibited between black and white adolescents in our review, with disordered eating attitudes reflecting restrictive eating behaviours due to limited food resources, rather than as methods of weight control.
Although cultural perceptions around ideal body size persist in South Africa, there is evidence of a shift in these social norms, with the majority of adolescents perceiving a normal-weight female silhouette to be the 'best'. In addition, older urban adolescents perceived an obese silhouette as the 'worst' and as 'unhappy'. 58 Such changes in desirability have been largely linked to urbanisation and increased exposure to, and adoption of, Western ideals. 114 This suggests a possible avenue for intervention in South African adolescents who already exhibit desire towards normal bodyweights-alongside potential declines in the influence of traditional barriers to change. 113 However, caution must be taken in promoting a healthy bodyweight while preventing development of more disordered attitudes to eating and weight loss during the vulnerable adolescent period. Research suggests that promotion of physical activity may be a critical component in such interventions, with exercise being associated with improved body-image perceptions, alongside the beneficial effects on adiposity. 113,115 Taking into account the perceptions towards activity, as well as the facilitators and barriers, is important,; particularly between rural and urban contexts. Qualitative studies identified in this review showed that, while adolescent girls were aware of the health benefits associated with being active, physical activity was more common in those from rural settings. In urban settings, limited availability of facilities and concerns around safety were reported as key barriers to active recreation. Multisectoral approaches that address individual, household, school and community level factors and both encourage, and allow, adolescents to safely partake in physical activity are therefore needed.

Community engagement for intervention development
As previously mentioned, research that explores current diet and activity patterns in South African adolescents, as well as the drivers of these, is critical in developing interventions to promote healthy growth in boys and girls. However, development of targeted and effective interventions will only be successful if adolescents themselves are involved in this process. Studies show that involving teenagers in intervention design has a significant impact on its outcomes, facilitating ownership of, and accountability to, the intervention itself. 116 In addition, community engagement facilitates mutual benefit to both the researchers and the community members themselves, helping to identify those interventions for which the priorities of various community members-i.e. adolescents, parents and teachers-overlap. 116,117 Limitations This review provides a comprehensive overview of available literature describing adolescent nutritional status in South Africa, with the inclusion of both quantitative and qualitative data adding a multifaceted understanding to potential determinants. While review findings have, to an extent, been supported by literature from other settings, the strength of and comparability between included studies is limited. Across review objectives substantial differences in study design were identified, with the majority of studies using cross-sectional designs and various exposure and outcome variables measured by multiple techniques at a range of adolescent ages. For example, where SES was described, this was defined by a number of methods, including wealth indices, household income and highest level of education achieved. However, while comparison may be restricted between studies, all have been extensively utilised as proxies for SES at household level and provide useful information on associations between SES and adolescent nutritional status across studies in a South African context. In addition, sample sizes differed substantially between studies and were relatively low in prospective cohort designs. This not only made drawing conclusions across studies difficult but limited the ability to make within-study comparisons-for example in cases where sex-and age-stratified results were not provided, potentially leading to bias in the presented study estimates. Similarly, the lack of comparative data-and longitudinal data in particular-makes it difficult to examine trends in South Africa across the study period. In addition, studies used various international standards and guidelines to both define and assess adequacy of nutritional status, with the standards or guidelines used often dependent on the timing of the study within the review period (for example pre-or post-introduction of the WHO growth standards in 2007 or the DRIs in 2001). Whether these international standards are applicable to African populations is debated and may explain why an unexpected decrease in overweight/obesity prevalence was observed in boys between early and mid-adolescence. Data have shown a delay in the onset of puberty, and therefore skeletal maturity, in black South African boys, which may lead to a degree of misclassification in both stunting and overweight/ obesity prevalence in younger boys when compared with international standards. 118 However, while use of different guidelines may make direct comparison between studies challenging, these studies still provide useful data describing nutrient adequacy over time. In addition, studies have shown a high degree of comparability between standards of weight classification (i.e. CDC/NCHS, IOTF and WHO growth standards) in adolescents, as well as in their associations with health outcomes, suggesting that the degree of misclassification between studies would be small overall. 119 For those studies reporting dietary intakes, all used either 24-hour recall or FFQ methodologies. While these are the most commonly utilised methods in African settings, innate limitations of using reported intakes exist, with strengths and weaknesses between specific methods being commonly acknowledged. 120 Recall bias, assumptions around regularity of eating habits, seasonality and inaccuracy in portion size estimation are all limitations of these methodologies and must be considered when interpreting the review findings. 121,122 Conclusion In South Africa, rapid urbanisation over the last two decades has resulted in a substantial rise in adolescent overweight and obesity, with urban females being most affected as they age. Rising adiposity in adolescents is driven by a transition towards increasingly Westernised diets characterised by high intakes of energy-dense, processed and convenience food products high in sugar and fat, but low in essential micronutrients.
In addition, the changes in dietary intake demonstrated across South African populations are exacerbated in adolescents as they age and adopt more obesogenic behaviours, including irregular breakfast consumption and fewer family meals, increased snacking and consumption of purchased/fast-food products and reduced levels of physical activity. However, this review highlights a scarcity of data for the implications of these shifting dietary-intake and behaviour patterns on the micronutrient status of adolescents, which may have severe implications for their ability to grow into healthy and productive adults. In addition, little is known about the way in which diet, activity and sedentary behaviours cluster in adolescent boys and girls, as well as the patterns of behaviour that may facilitate healthy growth and reduced adiposity between the sexes.