A comparative study of fruit and vegetable consumption and physical activity among adolescents in 49 Low-and-Middle-Income Countries

Physical inactivity and low consumption of fruits and vegetables (FV) during adolescence may persist through adulthood, putting adolescents at risk of developing chronic diseases. Although studies from high-income countries have reported differences in FV consumption and physical activity (PA) between adolescent boys and girls, few exist from low-and-middle-income countries (LMICs). In this study, we examined patterns of FV consumption and PA among adolescent boys and girls in LMICs. Country selection was based on availability of Global School-Based Student Health Survey (GSHS) data from 2004 to 2013. The total analytic sample was 164,771 adolescents from 49 LMICs. Descriptive statistics were generated to determine adolescents meeting the World Health Organization (WHO) recommendations for FV and PA. A Rao-Scott adjusted chi-square statistic was computed to assess gender differences. Less than 30% of adolescents across all countries met the WHO guidelines for FV consumption or PA. Morocco (29.5%) and India (29.5%) however had the highest percentage of adolescents meeting recommendations for FV and PA, respectively. Adolescent boys were more active than girls, and this difference was more notable in the Middle East and North African region. Adolescents achieving the WHO recommendations for daily consumption of FV and PA were consistently low in all countries.


Methods
Study design and sampling method. This study utilizes an ecologic study design to compare patterns of FV consumption and PA among adolescents from countries and regions demarcated by the World Bank as LMICs. The World Bank regions are Sub-Saharan Africa, Middle East and North Africa, South Asia, Latin America and the Caribbean, Europe and Central Asia and East Asia and the Pacific 15 . The study sample of LMICs included countries from the regions demarcated by the World Bank if they had (1) publicly available data on FV intake and PA behaviors), and (2) data available to allow the assessment of differences between adolescent boys and girls for these health behaviors.
Data and Sample. The primary data source is the Global School-based Student Health Survey (GSHS). The GSHS is a standardized survey developed by the WHO in collaboration with the United Nations International Children's Emergency Fund, the United Nations Educational, Scientific and Cultural Organization, and the United Nations Program on HIV/AIDS, with technical assistance provided by the Centers for Disease Control and Prevention. The GSHS is a collaborative surveillance project designed to help countries measure and assess health behaviors and protective factors among students between the ages of 13 to 17 years. It allows countries to develop priorities, establish programs, and advocate for resources for youth health programs and policies 16 . As of December 2013, 90 countries (mostly LMICs) had completed the GSHS, and representatives from over 120 countries have been trained to administer the GSHS 16 . GSHS data from 2004 to 2013 that were publicly available for LMICs 15 were used. According to the World Bank, these are countries that had a gross national income (GNI) of less than $12,616 in 2012 15 . A total of 49 countries with publicly available data on dietary behaviors and    PA for adolescents met this definition for inclusion in our study. Figure 1 shows the LMICs included in the study (n = 49 countries).

Survey Measures. The survey measures used were based on the following GSHS questions 17 :
Fruit; i) "During the past 30 days, how many times per day did you usually eat fruits, such as COUNTRY SPECIFIC EXAMPLES?" Response options were; (A) I did not eat fruit during the past 30 days (B) Less than one time per day (C) 1 time per day (D) 2 times per day (E) 3 times per day (F) 4 times per day (G) 5 or more times per day.
Vegetables; ii) "During the past 30 days, how many times per day did you usually eat vegetables, such as COUNTRY SPECIFIC EXAMPLES?"The response options were (A) I did not eat vegetables during the past 30 days (B) Less than one time per day (C)1 time per day (D) 2 times per day (E) 3 times per day (F) 4 times per day (G)5 or more times per day. Physical Activity; iii) "During the past 7 days, on how many days were you physically active for a total of at least 60 minutes per day?" The response options; A) 0 days B) 1 day C) 2 days D) 3 days E) 4 days F) 5 days G) 6 days H) 7 days. Data analysis. The data were analyzed using SPSS version 21 software (SPSS, Inc., Chicago, IL). The GSHS employs a complex sampling design, and the data were analyzed taking into account this sampling design. The weighting process was also used. This process adds weights, stratum and primary sampling unit (PSU) to every student record in the GSHS data file to reflect the weighting process and the 2-staged sampling design. The weight variable allows generalizability of the GSHS results to the entire students' population whereas the stratum and PSU account for the 2-stage sample design used for the GSHS. Specifically, the stratum reflects the GSHS sampling process at the first level, which is done in schools and the PSU reflects the second level of the GSHS sampling process conducted in classrooms 18 .
Descriptive statistics were generated to determine the number and percentage of adolescents in each of the LMICs meeting the WHO recommendations of daily intake of FV and PA. In generating the descriptive statistics, the variables took values of 1 (two otherwise) for i) consumption of fruits: adequate (2 or more/day), ii) consumption of vegetables: adequate (3 or more/day), iii) consumption of FV: adequate (adequate on both FV), iv) PA: adequate (60 minutes/day).The Rao-Scott adjusted chi-square statistic was used to test if there was a statistically significant difference between adolescent boys and girls in meeting the WHO recommendations of daily fruit servings, daily vegetable servings, daily FV servings and daily PA for each country and odds ratios were also calculated. The Rao-Scott adjusted chi-square statistic takes into consideration the complex sample design utilized in the GSHS data collection. The p-value of the adjusted F-statistics generated was used in determining statistical significance because it provides a better approximation of the significance 19 .
Availability of data and material. The datasets generated and/or analyzed during the current study are available at http://www.who.int/chp/gshs/datasets/en/. Figure 2 summarizes the pattern of FV consumption and PA among adolescents in LMICs grouped by World Bank regions. The sample represented 164,771 adolescents from 49 LMICs. There was significant variability regarding the outcomes of interest throughout the different regions and countries included in this study. In all countries, less than 50% of adolescents consumed five or more FV per day (Fig. 2). Morocco had the highest proportion of adolescents consuming the recommended daily FV intake (29.5%). Lastly, adolescents in India were the most active (29.5%) in terms of meeting the WHO recommendation for daily PA (Fig. 3).

Results
Differences in the outcomes of interest between adolescent boys and girls were observed in some but not all countries. In the sub-Saharan African region, only two countries (Senegal and Swaziland) showed girls more likely to meet the daily recommended intake of fruits compared to boys. Similarly, in two other countries (Seychelles and Tanzania) girls were more likely (p < 0.05) to meet the daily recommended intake of vegetables (Table 1).
In the Middle East and North African region, a significant difference was observed in the daily intake of fruits among adolescent boys and girls in 50% of the countries examined. In four (Algeria, Djibouti, Morocco and Tunisia) out of the five countries, adolescent girls were more likely to meet the daily recommended servings of fruit as compared to boys. In Lebanon, however, adolescent girls were less likely to consume two servings of fruits daily compared to adolescent boys {OR = 0.74; 95%CI (0.63-0.88); p-value = 0.002} (Table 1).
With regards to daily servings of vegetables (≥3 per day), a statistically significant difference between adolescent girls and boys was seen in three countries in the Middle East and North Africa. In two of the three countries (Lebanon and Tunisia), adolescent girls were less likely to consume ≥3 servings of vegetables per day than boys. Nonetheless, in Morocco {OR = 1.28; 95%CI (1.07-1.53); p-value = 0.01}, girls were more likely to consume the daily recommended intake of vegetables compared to boys (Table 1). In six countries there were significant differences between adolescent girls and boys meeting the recommended five servings of FV daily. In four countries (Lebanon, Syria, Tunisia, and Yemen), adolescent girls were less likely to consume the daily recommended servings of FV compared to boys. However, in Algeria {OR = 1.23; 95%CI (1.03-1.48); p-value = 0.026} and Morocco {OR = 1.31; 95%CI (1.08-1.60); p-value = 0.01}, girls were more likely to have five or more servings of FV daily than boys (Table 2).
In the South Asian region, only the Maldives recorded a significant difference between adolescent boys and girls meeting the recommended daily intake of fruit. Specifically, girls were less likely to consume ≥2 servings of fruit or vegetables daily compared to boys. Girls in Pakistan were also less likely to consume the recommended servings of vegetables compared to boys (Tables 1 and 2). In the Latin American and the Caribbean region, 29% of countries recorded differences (p < 0.05) between adolescent boys and girls in terms of FV intake, particularly in Costa Rica, Dominica, Jamaica, and Peru. More boys met the recommendations for daily fruit intake than the girls in Costa Rica, Dominica and Jamaica. Adolescent girls in Peru on the other hand, were more likely to meet the ≥2 servings of fruit {OR = 1.26; 95%CI (1.05-1.51); p-value = 0.014} than adolescent boys. In Argentina, girls were more likely to have ≥5 servings of FV daily compared to boys {OR = 1.43; 95%CI (1.02-2.00); p-value = 0.037} (Tables 1 and 2).
Lastly, in the East Asian and Pacific region, girls were less likely to meet the daily intake of vegetables compared to boys in Malaysia and Mongolia. Also, in Malaysia, girls were less likely to have ≥5 servings of FV daily {OR = 0.88; 95%CI (0.79-0.96); p-value = 0.007} compared to boys (Tables 1 and 2).
Regarding the daily WHO recommendations for daily PA, differences were observed between adolescent boys and girls in 50% of countries examined in the sub-Saharan African region. In all five countries (Benin, Mauritania, Senegal, Seychelles, and Tanzania), boys were more likely to meet the recommended daily PA guidelines compared to adolescent girls (Table 3).
In the Middle East and North African region, almost all the countries recorded a significant difference between boys and girls except for Yemen. In all the countries that showed a statistically significant difference, adolescent boys were more active and were more likely to meet the recommended daily PA guidelines than girls. Also, in the South Asian region, adolescent boys in the Maldives and Sri Lanka were more active than the girls (Table 3).
In the Latin American and the Caribbean region, adolescent boys were more likely to have 60 minutes of daily PA compared to girls, especially in Argentina, Belize, Bolivia, Costa Rica, Guatemala, Honduras, St. Vincent and the Grenadines, and Suriname. In the Former Yugoslav Republic of Macedonia, boys were more active than girls as the results showed boys as being more likely to have 60 minutes of daily PA {OR = 1.52; 95%CI (1.21-1.89); p-value = 0.001} compared to girls ( Table 3).
Six of the eight countries (75%) in the East Asian and Pacific region recorded a significant difference between adolescent boys and girls in meeting the daily recommended PA. Five of the six countries (83%) showed that adolescent boys were more likely to have 60 minutes of daily PA for seven days compared to adolescent girls, especially in Fiji, Malaysia, Mongolia, Myanmar, and Thailand. However, in Tonga, adolescent boys were less active, rather the girls were more likely to have 60 minutes of daily PA for seven days {OR = 0.70; 95%CI (0.52-0.94); p-value = 0.018} compared to the boys (Table 3).

Discussion
This study found that adolescent boys and girls living in LMICs commonly do not meet WHO recommendations for FV intake and physical activity. In all countries, less than 50% of adolescents consumed five servings of FV daily. Morocco had the highest percentage of adolescents meeting the WHO recommendations for the daily intake of FV. According to the FAO 20 , the Moroccan diet is Mediterranean and it is based on a high consumption of FV. Similar findings with respect to the low daily intake of FV among adolescents, have been observed among adolescents in Ghana where 48% rarely ate fruits 7 and in China where less than 50% ate fruit daily 8 . The variation could be due to differences in dietary cultural preferences among countries or regions as well as the availability of FV in the countries, income and urbanization rate 6 .
The results showed a clear, although variable trend in the FV intake between boys and girls, in which girls were more likely to reach the WHO recommendations. In the case of fruit, 58% of the countries where sex differences were noted showed that girls were more likely to consume ≥2 servings of fruit daily than adolescent boys. On the contrary, for vegetables, 67% of the countries that recorded a sex difference showed that boys were more likely to consume ≥3 servings of vegetables daily than girls. Rasmussen et al. 10 , reviewed FV intake in several countries and found that most studies (27 out of 49) showed gender differences in which girls had a higher intake of fruits and/ or vegetables. Studies have attributed this gender difference to a preference for FV. It has also been reported that boys do not eat FV because they do not like them as much as girls do 21,22 . In addition to preference, Bere et al. 21 found that the gender differences could also be attributed to the perceived accessibility of FV at home. They found that girls have a greater knowledge, and stronger intentions and self-efficacy compared to boys 21 . Lastly, according to Cooke et al. 22 , girls liked fruits and vegetables more than boys. The boys preferred energy-dense foods such as fatty and sugary foods to adapt to their higher energy requirement more so than girls.
According to the WHO 2 , the prevalence of physical inactivity is increasing among LMICs and it is already one of the leading causes of death. Among LMICs, India showed the highest proportion of adolescents who engaged in PA 60 minutes daily. The results from this study are consistent with those from Hallal et al. 13 , who found that 80.3% of adolescents between 13-15 years from 105 countries did not meet the recommended daily PA.
The results showed that physical inactivity was more common among adolescent girls in LMICs. In almost all the countries (30 out of 31), boys were more likely to meet the WHO recommendations for PA daily compared to girls. This result is consistent with studies showing that PA declines during adolescence, especially among girls 11,12 . A notable statistical difference between adolescent boys and girls with respect to PA was seen predominantly in the Middle East and North African region. These differences may be attributable to cultural and gender norms. Evidence from the Middle East and North Africa suggest that a barrier for women to engage in PA among women is the lack of facilities separated by gender, where women feel more comfortable being physically active 23,24 .
Despite its design and results, the study had a few limitations. The study included the use of the GSHS data, which surveys adolescents in schools. Thus the results might not necessarily reflect the FV consumption pattern and PA behavior among all adolescents in the respective countries. Specifically, information from adolescents who are unable to attend school or have dropped out would not be captured. Second, in some countries, FV are seasonal staples. Hence their consumption might be high or low in a country based on the season in which the data were collected. As stated earlier, PA patterns may also be affected by cultural perspectives resulting in the differences observed between countries and regions. Third, adolescents had to recall and self-report their FV consumption and PA behavior during the past 30 days and week, respectively. This approach may result in either overestimating or underestimating intake behaviors, leading to information bias. Finally, we cannot be certain that the 5 servings reported by the adolescents were equivalent to 400 grams since we could not quantify the servings from the GSHS data.