J. Biosoc. Sci., (2016) 48, 143–157, © Cambridge University Press, 2015 doi:10.1017/S0021932015000127 First published online 4 Jun 2015
E T H N I C I T Y A N D IN C O M E I M P A C T ON B M I AND STATURE OF SCHOOL CHILDREN L I V I N G I N U R B A N SO U T H E R N M E X I C O NINA MENDEZ*1, THE LATE MARIO BARRERA-PÉREZ*, MARCO PALMA-SOLIS†, JORGE ZAVALA-CASTRO*, FEDERICO DICKINSON‡, HUGO AZCORRA‡ AND MICHAEL PRELIP§ *Regional Research Centre ‘Dr Hideyo Noguchi’, Biomedical Unit, Merida, Yucatan, Mexico, †Faculty of Medicine, Autonomous University of Yucatan, Merida, Yucatan, Mexico, ‡Centres for Research and Advanced Studies, Department of Human Ecology, Merida, Yucatan, Mexico and §Fielding School of Public Health, University of California Los Angeles, Los Angeles, CA, USA Summary. Obesity affects quality of life and increases the risk of morbidity and mortality. Mexico, a middle-income country, has a high prevalence of overweight and obesity among urban children. Merida is the most populated and growing city in southern Mexico with a mixed Mayan and non-Maya population. Local urbanization and access to industrialized foods have impacted the eating habits and physical activity of children, increasing the risk of overweight and obesity. This study aimed to contribute to the existing literature on the global prevalence of overweight and obesity and examined the association of parental income, ethnicity and nutritional status with body mass index (BMI) and height in primary school children in Merida. The heights and weights of 3243 children aged 6–12 from sixteen randomly selected schools in the city were collected between April and December 2012. Multinomial logistic regression models were used to examine differences in the prevalence of BMI and height categories (based on WHO reference values) by ethnicity and income levels. Of the total students, 1648 (50.9%) were overweight or obese. Stunting was found in 227 children (7%), while 755 (23.3%) were defined as having short stature. Combined stunting and overweight/obesity was found in 301 students (9.3%) and twelve (0.4%) were classified as stunted and of low weight. Having two Mayan surnames was inversely associated with having adequate height (OR = 0.69, p < 0.05) and the presence of two Maya surnames in children increased the odds of short stature and stunting. Children from lower income families had twice the odds of being stunted and obese. Overweight, obesity and short stature were frequent among the studied children. A significant proportion of Meridan children could face an increased risk of
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Corresponding author. Email: [email protected]
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N. Mendez et al. developing cardiovascular disease and its associated negative economic and social outcomes unless healthier habits are adopted. Action is needed to reduce the prevalence of obesity among southern Mexican families of all ethnic groups, particularly those of lower income. Introduction
The rate of obesity throughout the world has risen dramatically over the last three decades (Stevens et al., 2012), to the point that it is now considered to be a major global health problem (Lehnert et al., 2013). It has a negative impact on quality of life, increases mortality and is related to morbidity and disability (Lim et al., 2013). Childhood obesity is associated with a higher likelihood of becoming obese as an adult and has been linked to numerous health problems later in life including type 2 diabetes, hypertension and cardiovascular disease (Freedman et al., 2007). According to the National Survey of Health and Nutrition (ENSANUT) 2012, in Mexico, 34.4% of school-aged children were overweight/obese, while in urban and rural communities of the Yucatan, 45.2% of the children aged 5–11 were overweight or obese (INSP, 2013). Merida is the most populated city in southern Mexico with almost one million residents and is home to almost half of the total population of the state of Yucatan (Monkkonen, 2010). Merida is a thriving tourist destination as people from around the world are not only attracted to its Mayan culture and coastal resorts, but also to the agricultural lands that have been transformed into golf courses and the colonial hacienda tourist corridor (Lutz et al., 2000; Diggles, 2008). Merida is also a strategic business centre where several transnational companies have established their factories and headquarters (Biles, 2004; Caro-Encalada & Leyva-Morales, 2008). Many institutions have centred their operations in Merida and are a major provider of nonrural jobs (Kaltmeier, 2011). Industrialization and urbanization are rapidly transforming Merida. Its population density has increased dramatically in the last 20 years (COMEY, 2010). The forests and cultivated land that used to surround the city are now used for residential construction to satisfy the increased need for housing the growing population (SEDESOL, 2010). Affordable houses for middle-income residents are commonly clustered together and have very limited access to parks or green areas. Higher and lower income neighbourhoods are less densely populated (Graniel et al., 1999), but lower income housing units commonly lack basic urban services (Monkkonen, 2010). Two socioeconomic traits distinguish the inhabitants of Merida: the strong presence of the indigenous population and the high economic disparities between social groups. Merida is the city with the second largest proportion of indigenous-speaking population in Mexico (INEGI, 2009). Mayan heritage is present among the contemporary citizenry of Merida. Recent studies conducted with Maya families in the south of Merida, where the poorest neighbourhoods are located, show a prevalence of stunting (low heightfor-age) in children (aged 4–9 years) ranging from 11 to 31%, and a prevalence of overweight/obesity above 30% (Varela-Silva et al., 2009, 2012; Azcorra et al., 2013a). These studies also showed an association between child stunting and maternal overweigh/obesity (Varela-Silva et al., 2012; Azcorra et al., 2013a). Social disparities in Merida are evident in the context of the urban infrastructure. The northern area of
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Merida is home to the population with the highest levels of income and, in general, this area shows more advanced infrastructure and services. In contrast, the south is the home to the lowest income population and lacks proper infrastructures in terms of education, health and recreation services (García Gil et al., 2012). Although ENSANUT is an important resource to identify BMI status of Mexicans, the 2012 edition only included a sample of 159 children aged 5–11 from urban communities in Yucatan. To the authors’ knowledge there are no recently published studies about overweight, obesity or short stature prevalence among primary school children in the city of Merida. Having detailed information about the nutritional status of school children would be useful for planning school-based interventions, as a reference for future comparisons and for programme evaluation. It would also contribute to the understanding of child obesity as a global health problem. Previously, Shultz and colleagues used the Social Determinants of Health and Environmental Health Promotion model to describe how socioeconomic processes interact with the built environment mediate to between fundamental factors, such as physical activity and overweight/obesity, which can ultimately increase the risk of developing cardiovascular diseases (Schulz et al., 2005). Social disadvantage in a child’s broader environment may confer higher risk of obesity (Grow et al., 2010), and ethnicity (in this study, by Mayan surnames) might be associated with children’s BMI and stature under certain socioeconomic conditions (Krieger et al., 2003; Kumanyika, 2008; Quiroz-Carranza, 2012). As in many other rapidly growing cities, socioeconomic disparities can be found within the city of Merida (Cruz, 2009; Gómez & Salazar, 2011; García Gil et al., 2012) and therefore the present study examines the association of the BMI and stature of children living in Merida with their parent(s) income and ethnicity.
Methods Sample selection and data collection This was a cross-sectional, school-based study conducted over a period of nine months from April to December 2012. Sample size calculation was based on the total population (70,778) of students attending public elementary schools in Merida. Sample sizes were calculated expecting 80% participant participation. With a confidence of 99% and an error margin of 2.06, the estimated sample size was 3296 students using the last published prevalence of overweight/obesity among children aged 5–11 living in Yucatan (0.38) (Olaiz-Fernández et al., 2006). For the selection of schools, the inclusion criterion was primary schools located within the city limits. This information was obtained from the Board of Education of the State of Yucatan Statistics for the 2011–2012 school year (SEEY, 2012). After assigning random order to the list of schools that met the inclusion criteria (256), the first sixteen schools were selected and it was verified that the schools were distributed throughout the city using city maps. Each school was visited and permission obtained from the schools’ principals, then the teachers, parents and students were informed about the objectives of the study. The research staff personally provided most of the parents with a consent form for each student during parent meetings. When it was not possible to personally reach the parents, informational brochures were sent home with the students’ homework.
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On the day of the measurements, children were asked for their assent to participate. Measurements were taken in school rooms specifically designated for this purpose. Children’s weight was measured with a digital scale to the nearest 100 grams (Terrailon© TPRO 3100) while they were wearing as little clothing as possible and without shoes (lightweight clothing was provided when needed). Height was measured with a portable stadiometer (Seca© 206) to the nearest millimetre following standard procedures (Lohman et al., 1991). Data transformation The 2007 WHO reference (Onis et al., 2007) was used to describe the anthropometric status of sample children, since it has been proven to be useful for both clinical and epidemiologic purposes (De Onis & Lobstein, 2010) and to be a good predictor of cardiovascular risk (De Onis et al., 2012). BMI and height and BMI z-score standard deviations (SD) were calculated using the WHO AnthroPlus software program by entering date of measurement, sex, height, weight and age. Age was confirmed using the Mexican Birth Registry for each child. According to the WHO reference, in children aged 5–19, a z-score value between ≥+1SD and 4 MDS and 0.05). The distribution of the sample by sex (girls 53.3% vs boys 48.8%) is consistent with the sex distribution in Merida. Socioeconomic characteristics About 40% of the sample were in the lower income range, 42% in the intermediate range and about 18% in the higher income range. Almost half of the sample had at least one Mayan surname (M-NM = 34%, M-M = 13%), and the remaining 53% had no Maya surnames. Anthropometric characteristics and nutritional status The descriptive statistics of measured and derived anthropometric variables of the children by age and sex are given in Table 2. The BMI mean z-score for the sample was 1.03 SD (±1.30) and the average height z-score was −0.48 SD (±1.00). No significant differences in height, z-score values of height and BMI were found between boys and girls. Girls, as a group, showed significantly higher z-score BMI values than boys
Table 1. Distribution of participant children by age and sex, Merida, Mexico, 2012 Boys Age (years) 6 7 8 9 10 11 12 Total
Girls
n
%
n
%
Total
178 212 223 246 265 241 151 1516
47.6 45.5 44.8 48.8 49.4 42.8 49.8 46.7
196 254 274 258 271 322 152 1727
52.4 54.5 55.1 51.2 50.6 57.2 50.2 53.2
374 466 497 504 536 563 303 3243
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Table 2. Descriptive statistics of measured and derived anthropometric variables of children by age, Merida, Mexico, 2012 Height (cm) Age (years) 6 7 8 9 10 11 12 Total
HAZ
BMI (kg/m2)
BMIZ
n
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
374 466 497 504 536 563 303 3243
116.19 121.63 127.27 132.32 138.48 143.81 148.24 132.65
(5.36) (5.59) (6.15) (6.39) (7.09) (7.26) (7.57) (12.08)
−0.47 −0.49 −0.49 −0.54 −0.44 −0.47 −0.39 −0.48
(1.03) (1.00) (1.00) (0.98) (1.03) (1.02) (0.98) (1.00)
17.31 18.08 18.68 19.31 20.27 20.51 21.77 19.40
(3.04) (3.23) (3.38) (3.52) (3.96) (3.97) (4.36) (3.88)
+0.94 +1.08 +1.09 +1.05 +1.11 +0.91 +1.06 +1.03
(1.45) (1.32) (1.30) (1.27) (1.28) (1.21) (1.23) (1.30)
HAZ: height-for-age z-score; BMIZ: BMI-for-age z-score.
(girls = 1.18 vs boys = 0.91, p < 0.001). No significant differences in BMI and z-score height and BMI values were found among categories of income and ethnicity (Table 3). However, height increased significantly with income (low = 131.73 ± 12.01 cm, intermediate = 132.80 ± 12.41 cm, high = 134.30 ± 11.19 cm; p < 0.05) and decreased significantly as the number of Maya surnames decreased (NM-NM = 133.96 ± 12.00 cm; NM-M = 131.38 ± 11.83 cm, M-M = 130.42 ± 12.39 cm; p < 0.05). The results for BMI and height status are displayed in Table 4. The overall prevalence of overweight was 24.1% and that of obesity was 26.8%. The combined prevalence of overweight and obese in the sample was 50.8% (±2.06, with a confidence value of 99%). It was observed that 23.3% of the children had short stature and 7.0% were classified as stunted. The combined prevalence for short stature and stunting was 30.3%. The combination of stunting and underweight was only present in 0.4% of the sample. The percentage of children classified as stunted was significantly higher in girls (7.9%) than in boys (6.08%). Tables 5 and 6 present the results of multinomial logistic regression models of association between income, ethnicity and BMI status, adjusted by age. Table 5 shows the results of the association between ethnicity, BMI and height status, where having two Maya surnames significantly increased the odds for short height (OR = 1.42, 95% IC = 1.11–1.82), and stunting (OR = 1.53, 95% IC = 1.00–2.33), but not for being overweight, obese or having the ‘double burden’ of short stature/stunting + overweight/ obesity. Table 6 presents the results for the association between income level and BMI and height status, where belonging to a lower income group doubled the odds of being stunted (OR = 2.185, 95% IC = 1.38–3.34) and was also associated with double burden; intermediate and lower income categories were associated with increased risk of being obese. Discussion The study sample of 6- to 12-year-old primary school children in urban Mexico had an average BMI SD value of +1.03 (±0.04), indicating that as a group the sample tends to
131.73 −0.51 19.39 +1.00
(12.01) (0.99) (3.88) (1.26)
132.80 −0.45 19.34 +1.05
(12.41) (1.01) (3.84) (1.33)
134.30 −0.47 19.59 +1.08
Mean (11.19) (1.01) (3.96) (1.31)
(SD)
High income (>9 MDS) N = 581 (17.92%)
133.96 −0.47 19.50 +1.05
Mean (12.00) (0.99) (3.97) (1.33)
(SD)
NM-NM N = 1742 (53.72%)
MDS: Minimum Daily Salary; M: Mayan surname, NM: non-Mayan surname. HAZ: height-for-age z-score; BMIZ: BMI-for-age z-score. *p < 0.05.
Height* HAZ BMI BMIZ
(SD)
Mean
Mean
(SD)
Middle income (5–8 MDS) N = 1379 (42.52%)
Low income (1–4 MDS) N = 1283 (39.56%)
131.38 −0.46 19.33 +1.03
Mean
(11.83) (1.02) (3.84) (1.30)
(SD)
NM-M N = 1092 (33.67%)
130.42 −0.55 19.19 +1.02
Mean
(12.39) (1.02) (3.54) (1.15)
(SD)
M-M N = 409 (12.61%)
Table 3. Descriptive statistics of anthropometric variables by income levels and ethnicity, Merida, Mexico, 2012
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Table 4. Anthropometric status categories by children’s sex, Merida, Mexico, 2012 Total Characteristic Short height Stunting Underweight Overweight Obesity Double burdena Stunting+underweight
Boys
Girls
n
%
n
%
n
%
755 227 148 780 868 301 12
23.3 7.0 4.6 24.1 26.8 9.2 0.4
452 91 75 225 591 152 9
46.0 40.0 51.0 15.0 39.0 10.0 0.6
530 136 73 305 501 149 3
54.0 60.0 49.0 18.0 29.0 8.6 0.2
Difference χ2 χ2 χ2 χ2 χ2 χ2 χ2
= = = = = = =
0.27, p > 0.05 4.31, p < 0.05 0.00, p > 0.05 2.29, p > 0.05 36.03, p < 0.05 1.90, p > 0.05 3.87, p < 0.05
a
Double burden is stunting/short height + overweight/obese. Height and BMI status was defined based on the WHO reference values: height z-score between ≤−1SD and >−2SD = short; height z-score ≤−2SD = stunting; BMI z-score z
Lower
Upper
0.80 0.69
0.12 0.12
0.072 0.001
0.63 0.55
1.02 0.87
1.12 1.43
0.91 0.12
0.209 0.011
0.94 1.11
1.34 1.83
1.14 1.53
0.09 0.21
0.150 0.047
0.95 1.01
1.37 2.33
1.05 1.10
0.08 0.11
0.529 0.372
0.90 0.89
1.22 1.37
0.87 1.14
0.13 0.14
0.284 0.967
0.67 0.76
1.13 1.32
1.35 1.25
0.08 0.35
0.084 0.346
0.97 0.86
1.66 1.53
1.19 1.33
0.13 0.18
0.194 0.116
0.91 0.93
1.54 1.90
a
Reference category: NM-NM. Double burden is stunting/short height+overweight/obese. BMI and height status was defined based on WHO reference values. The underweight category was excluded from the analysis due to the small number of underweight participants. M-M = two Mayan surnames; M-NM = one Mayan and one non-Mayan surname; NM-NM = two non-Mayan surnames. Significant p < 0.05 values are shown in bold, italic font. Data adjusted by age. b
More research is needed to describe the social and health factors that might be related to the potential growth retardation and nutrition imbalance of mixed ancestry children. Children living in the east and south of Merida (where there is a higher proportion of the NM-M population) receive hypercaloric, vitamin-enriched nutritional supplements as a part of in-kind nutritional programmes, similar to what Leroy and colleagues reported in rural communities (Leroy et al., 2010). This effort operates under the supposition that offering more calories and vitamins to children from underserved communities will prevent malnutrition and help them to grow taller. Research to further understand the impact of this type of programme on not only height but weight is recommended. Recent studies on Maya families from the south of Merida have described how this population has undergone a nutritional transition, with a shift from traditional and locally produced foods to a globalized diet with a high presence of processed
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Table 6. Multinominal logistic regression models association of BMI and height status with income levela, Merida, Mexico, 2012 95% CI Status Adequate height Intermediate income Lower income Short height Intermediate income Lower income Stunted Intermediate income Lower income Healthy BMI Intermediate income Lower income Overweight Intermediate income Lower income Obesity Intermediate income Lower income Double burden Intermediate income Lower income
OR
SE
p>z
Lower
Upper
0.65 0.67
0.13 0.17
0.198 0.000
0.56 0.54
0.78 0.84
0.90 1.23
0.12 0.11
0.389 0.071
0.71 0.98
1.14 1.56
1.33 2.18
0.24 0.23
0.232 0.001
0.83 1.39
2.14 3.34
0.32 0.47
0.10 0.10
0.000 0.000
0.26 0.38
0.39 0.58
1.08 1.12
0.17 0.11
0.494 0.311
0.86 0.89
1.37 1.42
1.69 1.81
0.17 0.20
0.002 0.004
1.21 1.21
2.35 2.72
0.97 10.50
0.18 0.17
0.894 0.021
0.681 1.06
1.40 2.13
a
Reference category: higher income. BMI and height status was defined based on the WHO reference values. The underweight category was excluded from the analysis due to the small number of underweight participants. Significant p < 0.05 values are shown in bold, italic font. Data are adjusted by age.
products, high in sugar, fats and poor in micronutrients and fibre (Azcorra et al., 2013b; Bogin et al., 2014). Nutritional transition is not necessarily bad for health. From 2006 to 2012 the rates of stunting in urban communities of Yucatan declined by 12% in 1- to 4-year-old children. It is possible that increased availability of energy in foods is contributing to reduced rates of chronic malnutrition among urban Maya children. However, this shift in the dietetic pattern seems to be related to the combination of short stature and overweight/obesity in children (nutritional double burden) resulting from a diet deficient in essential nutrients for lineal growth, but excessive in total energy (Steven et al., 2012). Previous studies in the Guatemalan Mayan migrant population conducted in the US (where ‘Mayan’ was defined as those who had migrated from Guatemala, irrespective of their surnames or self-identity) showed a similar prevalence of overweight and obesity as in the present study. Another similarity was that girls were more likely to be overweight while boys were more likely to be obese. The authors of that study described the changes
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in diet as a result of migration, with greater access to food, resulting in a high frequency of overweight and obesity (Smith et al., 2002). However, in the present study, a similar prevalence was found in the city of Merida, which possibly indicates that migration and acculturation to a different country might not be a determinant factor underlying overweight and obesity among Mayan children. Instead, the westernization of diets might be a global phenomenon affecting not only high-income countries, or touristbased economies in small towns in the Yucatan (Leatherman et al., 2010), but also lower income families living in urban settings of middle-income countries such as Mexico. Socioeconomic status generally (Murasko, 2009), as well as Mayan ethnicity (Makkes et al., 2011), have been considered to have a positive relation with children’s height (Murasko, 2009), but in this sample it was found that short stature and stunting were also prevalent among children without Mayan surnames (NM-NM children). Further studies will be needed to better understand the factors underlying the high prevalence of short stature and stunting among children living in Merida. Inter-generational influences of adverse living conditions have been proposed to explain the persistence of linear growth deficit among Maya children in Yucatan (Azcorra et al., 2013a). This study demonstrated that overweight/obesity and also short stature are common among the Meridan population aged 6–12 years attending public primary schools. Short height and stunting was more common among children from the lower income group. It was also found that children with two Mayan surnames and those with one Mayan surname and one non-Mayan surname might be more likely to develop a short height accompanied by being overweight/obese. In conclusion, overweight, obesity and short stature are major health issues among children aged 6–12 attending primary public schools of Merida, Yucatan. These health issues affect children from the higher income group less, when compared with intermediate and lower income groups. Short height was more common among children in the lower income group. This study provides useful information supporting the view that childhood overweight/obesity and short stature are global health problems that are common in urbanized areas.
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Lehnert, T., Sonntag, D., Konnopka, A., Riedel-Heller, S. & König, H-H. (2013) Economic costs of overweight and obesity. Best Practice & Research. Clinical Endocrinology & Metabolism 27, 105–115. Leroy, J. L., Gadsden, P., Rodríguez-Ramírez, S. & González-de-Cossío, T. (2010) Cash and in-kind transfers in poor rural communities in México increase household fruit, vegetable, and micronutrient consumption but also lead to excess energy consumption. Journal of Nutrition 140, 612–617. Lim, S. S., Vos, T., Flaxman, A. D., Danaei, G., Shibuya, K., Adair-Rohani, H. et al. (2013) A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380(9859), 2224–2260. Lohman, T. G., Roche, A. F. & Martorell, R. (1991) Anthropometric Standardization Reference Manual. Human Kinetics Books, Champaign, III, Chicago, USA. Lutz, W., Prieto, L. & Sanderson, W. (2000) Population, Development, and Environment on the Yucatán Peninsula. International Institute for Applied Systems Analysis, Laxenburg, Vienna, Austria. McLorg, P. A. (2005) Anthropometric patterns in middle-aged and older rural Yucatec Maya women. Annals of Human Biology 32 (4), 487–497. Makkes, S., Montenegro-Bethancourt, G., Groeneveld, I. F., Doak, C. M. & Solomons, N. W. (2011) Beverage consumption and anthropometric outcomes among schoolchildren in Guatemala. Maternal Child Nutrition 7(4), 410–420. Mendez, N. (2013) Aspects of the family and school environment concerning habits food and physical activity associated with overweight among schoolchildren in Merida Yucatan. Doctoral Thesis, Universidad Autonoma de Yucatan. Monkkonen, P. (2010) Measuring Residential Segregation in Urban Mexico: Levels and Patterns. University of California at Berkeley Working Paper 2010-05. Murasko, J. E. (2009) Socioeconomic status, height, and obesity in children. Economics and Human Biology 7(3), 376–386. Olaiz-Fernández, G., Rivera-Dommarco, J., Shamah-Levy, T. et al. (2006) Encuesta nacional de salud y nutrición 2006 [National survey of health and nutrition 2006]. Instituto Nacional de Salud Pública, Cuernavaca, México. Onis, M. D., Onyango, A. W., Borghi, E., Siyam, A., Nishida, C. & Siekmann, J. (2007) Development of a WHO growth reference for school-aged children and adolescents. Bulletin of the World Health Organization 85(9), 660–667. Osorio, J. (2011) Cardiovascular endocrinology: obesity-associated risk is reversible. Nature Reviews Endocrinology 8(2), 67. Quiroz-Carranza, R. (2012) Aprendiendo a ser joven con derechos propios en condiciones de pobreza y exclusión social. Un estudio de caso en Mérida, Yucatán, México [Learning to be young and have rights in conditions of poverty and social exclusion. A case study in Merida, Yucatan, Mexico]. Second International Sociological Association Forum of Sociology, 1–4th August 2012. Rogers, I., Metcalfe, C., Gunnell, D., Emmett, P., Dunger, D. & Holly, J. (2006) Insulin-like growth factor-I and growth in height, leg length, and trunk length between ages 5 and 10 years. Journal of Endocrinology & Metabolism 91(7), 2514–2519. Rtveladze, K., Marsh, T., Barquera, S., Romero, L. M. S., Levy, D., Melendez, G. et al. (2013) Obesity prevalence in Mexico: impact on health and economic burden. Public Health Nutrition 17(1), 233–239. Schulz, A. J., Kannan, S., Dvonch, J. T., Israel, B. A., Allen III, A. , James, S. A. et al. (2005) Social and physical environments and disparities in risk for cardiovascular disease: the healthy environments partnership conceptual model. Environmental Health Perspectives 113(12), 1817.
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Secretaria de desarrollo social. (2010) Atlas de riesgos de peligros naturales del municipio de Mérida Yucatán, México [Atlas of risks from natural hazards of the municipality of Mérida, Yucatán, Mexico.]. Municipality of Merida, Mexico. SEEY. (2012) Catálogos y Estadísticas. Secretaría de Educación del Estado de Yucatán. URL: http://www.educacion.yucatan.gob.mx/ (accessed 3rd March 2012). Smith, P. K., Bogin, B., Varela-Silva, M. I., Orden, B. & Loucky, J. (2002) Does immigration help or harm children’s health? The Mayan case. Social Science Quarterly 83(4), 994–1002. Sonneville, K. R., La Pelle, N., Taveras, E. M., Gillman, M. W. & Prosser, L. A. (2009) Economic and other barriers to adopting recommendations to prevent childhood obesity: results of a focus group study with parents. BMC Pediatrics 9(1), 81. Stevens, G. A., Singh, G. M., Lu, Y., Danaei, G., Lin, J. K., Finucane, M. M. et al. (2012) National, regional, and global trends in adult overweight and obesity prevalences. Population Health Metrics 10(1), 22. Torres Ornelas, P., Evangelista-Salazar, J. J. & Martínez-Salgado, H. (2011) Coexistence of obesity and anemia in children between 2 and 18 years of age in Mexico. Boletín médico del Hospital Infantil de México 68(6), 431–437. Valencia Villalvazo, E. Y., Canto-Cetina, T., Romero Arauz, J. F., Coral-Vázquez, R. M., Canizales-Quinteros, S., Coronel, A. et al. (2012) Analysis of polymorphisms in interleukin-10, interleukin-6, and interleukin-1 receptor antagonist in Mexican-mestizo women with pre-eclampsia. Genetic Testing and Molecular Biomarkers 16(11), 1263–1269. Varela-Silva, M., Azcorra, H., Dickinson, F., Bogin, B. & Frisancho, A. (2009) Influence of maternal stature, pregnant age, and infant birth weight on growth during childhood in Yucatan, Mexico: a test of the intergenerational effects hypothesis. American Journal of Human Biology 21(5), 657–663. Varela-Silva, M., Dickinson, F., Wilson, H., Azcorra, H., Griffiths, P. & Bogin, B. (2012) The nutritional dual-burden in developing countries – how is it assessed and what are the health implications? Collegium Antropologicum 36(1). Wang, N. A., Zhang, X., Xiang, Y-B., Yang, G., Li, H-L., Gao, J. et al. (2011) Associations of adult height and its components with mortality: a report from cohort studies of 135 000 Chinese women and men. International Journal of Epidemiology 40(6), 1715–1726. Whitley, E., Martin, R. M., Davey Smith, G., Holly, J. M. & Gunnell, D. (2012) The association of childhood height, leg length and other measures of skeletal growth with adult cardiovascular disease: the Boyd–Orr cohort. Journal of Epidemiology and Community Health 66(1), 18–23. Wolañski, N., Dickinson, F., Siniarska, A. & Varela-Silva, M. I. (1993) Biological traits and living conditions of Maya Indian and non-Maya girls from Mérida, México. International Journal of Anthropology 8, 233–246.
E T H N I C I T Y A N D IN C O M E I M P A C T ON B M I AND STATURE OF SCHOOL CHILDREN L I V I N G I N U R B A N SO U T H E R N M E X I C O NINA MENDEZ*1, THE LATE MARIO BARRERA-PÉREZ*, MARCO PALMA-SOLIS†, JORGE ZAVALA-CASTRO*, FEDERICO DICKINSON‡, HUGO AZCORRA‡ AND MICHAEL PRELIP§ *Regional Research Centre ‘Dr Hideyo Noguchi’, Biomedical Unit, Merida, Yucatan, Mexico, †Faculty of Medicine, Autonomous University of Yucatan, Merida, Yucatan, Mexico, ‡Centres for Research and Advanced Studies, Department of Human Ecology, Merida, Yucatan, Mexico and §Fielding School of Public Health, University of California Los Angeles, Los Angeles, CA, USA Summary. Obesity affects quality of life and increases the risk of morbidity and mortality. Mexico, a middle-income country, has a high prevalence of overweight and obesity among urban children. Merida is the most populated and growing city in southern Mexico with a mixed Mayan and non-Maya population. Local urbanization and access to industrialized foods have impacted the eating habits and physical activity of children, increasing the risk of overweight and obesity. This study aimed to contribute to the existing literature on the global prevalence of overweight and obesity and examined the association of parental income, ethnicity and nutritional status with body mass index (BMI) and height in primary school children in Merida. The heights and weights of 3243 children aged 6–12 from sixteen randomly selected schools in the city were collected between April and December 2012. Multinomial logistic regression models were used to examine differences in the prevalence of BMI and height categories (based on WHO reference values) by ethnicity and income levels. Of the total students, 1648 (50.9%) were overweight or obese. Stunting was found in 227 children (7%), while 755 (23.3%) were defined as having short stature. Combined stunting and overweight/obesity was found in 301 students (9.3%) and twelve (0.4%) were classified as stunted and of low weight. Having two Mayan surnames was inversely associated with having adequate height (OR = 0.69, p < 0.05) and the presence of two Maya surnames in children increased the odds of short stature and stunting. Children from lower income families had twice the odds of being stunted and obese. Overweight, obesity and short stature were frequent among the studied children. A significant proportion of Meridan children could face an increased risk of
1
Corresponding author. Email: [email protected]
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N. Mendez et al. developing cardiovascular disease and its associated negative economic and social outcomes unless healthier habits are adopted. Action is needed to reduce the prevalence of obesity among southern Mexican families of all ethnic groups, particularly those of lower income. Introduction
The rate of obesity throughout the world has risen dramatically over the last three decades (Stevens et al., 2012), to the point that it is now considered to be a major global health problem (Lehnert et al., 2013). It has a negative impact on quality of life, increases mortality and is related to morbidity and disability (Lim et al., 2013). Childhood obesity is associated with a higher likelihood of becoming obese as an adult and has been linked to numerous health problems later in life including type 2 diabetes, hypertension and cardiovascular disease (Freedman et al., 2007). According to the National Survey of Health and Nutrition (ENSANUT) 2012, in Mexico, 34.4% of school-aged children were overweight/obese, while in urban and rural communities of the Yucatan, 45.2% of the children aged 5–11 were overweight or obese (INSP, 2013). Merida is the most populated city in southern Mexico with almost one million residents and is home to almost half of the total population of the state of Yucatan (Monkkonen, 2010). Merida is a thriving tourist destination as people from around the world are not only attracted to its Mayan culture and coastal resorts, but also to the agricultural lands that have been transformed into golf courses and the colonial hacienda tourist corridor (Lutz et al., 2000; Diggles, 2008). Merida is also a strategic business centre where several transnational companies have established their factories and headquarters (Biles, 2004; Caro-Encalada & Leyva-Morales, 2008). Many institutions have centred their operations in Merida and are a major provider of nonrural jobs (Kaltmeier, 2011). Industrialization and urbanization are rapidly transforming Merida. Its population density has increased dramatically in the last 20 years (COMEY, 2010). The forests and cultivated land that used to surround the city are now used for residential construction to satisfy the increased need for housing the growing population (SEDESOL, 2010). Affordable houses for middle-income residents are commonly clustered together and have very limited access to parks or green areas. Higher and lower income neighbourhoods are less densely populated (Graniel et al., 1999), but lower income housing units commonly lack basic urban services (Monkkonen, 2010). Two socioeconomic traits distinguish the inhabitants of Merida: the strong presence of the indigenous population and the high economic disparities between social groups. Merida is the city with the second largest proportion of indigenous-speaking population in Mexico (INEGI, 2009). Mayan heritage is present among the contemporary citizenry of Merida. Recent studies conducted with Maya families in the south of Merida, where the poorest neighbourhoods are located, show a prevalence of stunting (low heightfor-age) in children (aged 4–9 years) ranging from 11 to 31%, and a prevalence of overweight/obesity above 30% (Varela-Silva et al., 2009, 2012; Azcorra et al., 2013a). These studies also showed an association between child stunting and maternal overweigh/obesity (Varela-Silva et al., 2012; Azcorra et al., 2013a). Social disparities in Merida are evident in the context of the urban infrastructure. The northern area of
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Merida is home to the population with the highest levels of income and, in general, this area shows more advanced infrastructure and services. In contrast, the south is the home to the lowest income population and lacks proper infrastructures in terms of education, health and recreation services (García Gil et al., 2012). Although ENSANUT is an important resource to identify BMI status of Mexicans, the 2012 edition only included a sample of 159 children aged 5–11 from urban communities in Yucatan. To the authors’ knowledge there are no recently published studies about overweight, obesity or short stature prevalence among primary school children in the city of Merida. Having detailed information about the nutritional status of school children would be useful for planning school-based interventions, as a reference for future comparisons and for programme evaluation. It would also contribute to the understanding of child obesity as a global health problem. Previously, Shultz and colleagues used the Social Determinants of Health and Environmental Health Promotion model to describe how socioeconomic processes interact with the built environment mediate to between fundamental factors, such as physical activity and overweight/obesity, which can ultimately increase the risk of developing cardiovascular diseases (Schulz et al., 2005). Social disadvantage in a child’s broader environment may confer higher risk of obesity (Grow et al., 2010), and ethnicity (in this study, by Mayan surnames) might be associated with children’s BMI and stature under certain socioeconomic conditions (Krieger et al., 2003; Kumanyika, 2008; Quiroz-Carranza, 2012). As in many other rapidly growing cities, socioeconomic disparities can be found within the city of Merida (Cruz, 2009; Gómez & Salazar, 2011; García Gil et al., 2012) and therefore the present study examines the association of the BMI and stature of children living in Merida with their parent(s) income and ethnicity.
Methods Sample selection and data collection This was a cross-sectional, school-based study conducted over a period of nine months from April to December 2012. Sample size calculation was based on the total population (70,778) of students attending public elementary schools in Merida. Sample sizes were calculated expecting 80% participant participation. With a confidence of 99% and an error margin of 2.06, the estimated sample size was 3296 students using the last published prevalence of overweight/obesity among children aged 5–11 living in Yucatan (0.38) (Olaiz-Fernández et al., 2006). For the selection of schools, the inclusion criterion was primary schools located within the city limits. This information was obtained from the Board of Education of the State of Yucatan Statistics for the 2011–2012 school year (SEEY, 2012). After assigning random order to the list of schools that met the inclusion criteria (256), the first sixteen schools were selected and it was verified that the schools were distributed throughout the city using city maps. Each school was visited and permission obtained from the schools’ principals, then the teachers, parents and students were informed about the objectives of the study. The research staff personally provided most of the parents with a consent form for each student during parent meetings. When it was not possible to personally reach the parents, informational brochures were sent home with the students’ homework.
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On the day of the measurements, children were asked for their assent to participate. Measurements were taken in school rooms specifically designated for this purpose. Children’s weight was measured with a digital scale to the nearest 100 grams (Terrailon© TPRO 3100) while they were wearing as little clothing as possible and without shoes (lightweight clothing was provided when needed). Height was measured with a portable stadiometer (Seca© 206) to the nearest millimetre following standard procedures (Lohman et al., 1991). Data transformation The 2007 WHO reference (Onis et al., 2007) was used to describe the anthropometric status of sample children, since it has been proven to be useful for both clinical and epidemiologic purposes (De Onis & Lobstein, 2010) and to be a good predictor of cardiovascular risk (De Onis et al., 2012). BMI and height and BMI z-score standard deviations (SD) were calculated using the WHO AnthroPlus software program by entering date of measurement, sex, height, weight and age. Age was confirmed using the Mexican Birth Registry for each child. According to the WHO reference, in children aged 5–19, a z-score value between ≥+1SD and 4 MDS and 0.05). The distribution of the sample by sex (girls 53.3% vs boys 48.8%) is consistent with the sex distribution in Merida. Socioeconomic characteristics About 40% of the sample were in the lower income range, 42% in the intermediate range and about 18% in the higher income range. Almost half of the sample had at least one Mayan surname (M-NM = 34%, M-M = 13%), and the remaining 53% had no Maya surnames. Anthropometric characteristics and nutritional status The descriptive statistics of measured and derived anthropometric variables of the children by age and sex are given in Table 2. The BMI mean z-score for the sample was 1.03 SD (±1.30) and the average height z-score was −0.48 SD (±1.00). No significant differences in height, z-score values of height and BMI were found between boys and girls. Girls, as a group, showed significantly higher z-score BMI values than boys
Table 1. Distribution of participant children by age and sex, Merida, Mexico, 2012 Boys Age (years) 6 7 8 9 10 11 12 Total
Girls
n
%
n
%
Total
178 212 223 246 265 241 151 1516
47.6 45.5 44.8 48.8 49.4 42.8 49.8 46.7
196 254 274 258 271 322 152 1727
52.4 54.5 55.1 51.2 50.6 57.2 50.2 53.2
374 466 497 504 536 563 303 3243
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Table 2. Descriptive statistics of measured and derived anthropometric variables of children by age, Merida, Mexico, 2012 Height (cm) Age (years) 6 7 8 9 10 11 12 Total
HAZ
BMI (kg/m2)
BMIZ
n
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
374 466 497 504 536 563 303 3243
116.19 121.63 127.27 132.32 138.48 143.81 148.24 132.65
(5.36) (5.59) (6.15) (6.39) (7.09) (7.26) (7.57) (12.08)
−0.47 −0.49 −0.49 −0.54 −0.44 −0.47 −0.39 −0.48
(1.03) (1.00) (1.00) (0.98) (1.03) (1.02) (0.98) (1.00)
17.31 18.08 18.68 19.31 20.27 20.51 21.77 19.40
(3.04) (3.23) (3.38) (3.52) (3.96) (3.97) (4.36) (3.88)
+0.94 +1.08 +1.09 +1.05 +1.11 +0.91 +1.06 +1.03
(1.45) (1.32) (1.30) (1.27) (1.28) (1.21) (1.23) (1.30)
HAZ: height-for-age z-score; BMIZ: BMI-for-age z-score.
(girls = 1.18 vs boys = 0.91, p < 0.001). No significant differences in BMI and z-score height and BMI values were found among categories of income and ethnicity (Table 3). However, height increased significantly with income (low = 131.73 ± 12.01 cm, intermediate = 132.80 ± 12.41 cm, high = 134.30 ± 11.19 cm; p < 0.05) and decreased significantly as the number of Maya surnames decreased (NM-NM = 133.96 ± 12.00 cm; NM-M = 131.38 ± 11.83 cm, M-M = 130.42 ± 12.39 cm; p < 0.05). The results for BMI and height status are displayed in Table 4. The overall prevalence of overweight was 24.1% and that of obesity was 26.8%. The combined prevalence of overweight and obese in the sample was 50.8% (±2.06, with a confidence value of 99%). It was observed that 23.3% of the children had short stature and 7.0% were classified as stunted. The combined prevalence for short stature and stunting was 30.3%. The combination of stunting and underweight was only present in 0.4% of the sample. The percentage of children classified as stunted was significantly higher in girls (7.9%) than in boys (6.08%). Tables 5 and 6 present the results of multinomial logistic regression models of association between income, ethnicity and BMI status, adjusted by age. Table 5 shows the results of the association between ethnicity, BMI and height status, where having two Maya surnames significantly increased the odds for short height (OR = 1.42, 95% IC = 1.11–1.82), and stunting (OR = 1.53, 95% IC = 1.00–2.33), but not for being overweight, obese or having the ‘double burden’ of short stature/stunting + overweight/ obesity. Table 6 presents the results for the association between income level and BMI and height status, where belonging to a lower income group doubled the odds of being stunted (OR = 2.185, 95% IC = 1.38–3.34) and was also associated with double burden; intermediate and lower income categories were associated with increased risk of being obese. Discussion The study sample of 6- to 12-year-old primary school children in urban Mexico had an average BMI SD value of +1.03 (±0.04), indicating that as a group the sample tends to
131.73 −0.51 19.39 +1.00
(12.01) (0.99) (3.88) (1.26)
132.80 −0.45 19.34 +1.05
(12.41) (1.01) (3.84) (1.33)
134.30 −0.47 19.59 +1.08
Mean (11.19) (1.01) (3.96) (1.31)
(SD)
High income (>9 MDS) N = 581 (17.92%)
133.96 −0.47 19.50 +1.05
Mean (12.00) (0.99) (3.97) (1.33)
(SD)
NM-NM N = 1742 (53.72%)
MDS: Minimum Daily Salary; M: Mayan surname, NM: non-Mayan surname. HAZ: height-for-age z-score; BMIZ: BMI-for-age z-score. *p < 0.05.
Height* HAZ BMI BMIZ
(SD)
Mean
Mean
(SD)
Middle income (5–8 MDS) N = 1379 (42.52%)
Low income (1–4 MDS) N = 1283 (39.56%)
131.38 −0.46 19.33 +1.03
Mean
(11.83) (1.02) (3.84) (1.30)
(SD)
NM-M N = 1092 (33.67%)
130.42 −0.55 19.19 +1.02
Mean
(12.39) (1.02) (3.54) (1.15)
(SD)
M-M N = 409 (12.61%)
Table 3. Descriptive statistics of anthropometric variables by income levels and ethnicity, Merida, Mexico, 2012
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Table 4. Anthropometric status categories by children’s sex, Merida, Mexico, 2012 Total Characteristic Short height Stunting Underweight Overweight Obesity Double burdena Stunting+underweight
Boys
Girls
n
%
n
%
n
%
755 227 148 780 868 301 12
23.3 7.0 4.6 24.1 26.8 9.2 0.4
452 91 75 225 591 152 9
46.0 40.0 51.0 15.0 39.0 10.0 0.6
530 136 73 305 501 149 3
54.0 60.0 49.0 18.0 29.0 8.6 0.2
Difference χ2 χ2 χ2 χ2 χ2 χ2 χ2
= = = = = = =
0.27, p > 0.05 4.31, p < 0.05 0.00, p > 0.05 2.29, p > 0.05 36.03, p < 0.05 1.90, p > 0.05 3.87, p < 0.05
a
Double burden is stunting/short height + overweight/obese. Height and BMI status was defined based on the WHO reference values: height z-score between ≤−1SD and >−2SD = short; height z-score ≤−2SD = stunting; BMI z-score z
Lower
Upper
0.80 0.69
0.12 0.12
0.072 0.001
0.63 0.55
1.02 0.87
1.12 1.43
0.91 0.12
0.209 0.011
0.94 1.11
1.34 1.83
1.14 1.53
0.09 0.21
0.150 0.047
0.95 1.01
1.37 2.33
1.05 1.10
0.08 0.11
0.529 0.372
0.90 0.89
1.22 1.37
0.87 1.14
0.13 0.14
0.284 0.967
0.67 0.76
1.13 1.32
1.35 1.25
0.08 0.35
0.084 0.346
0.97 0.86
1.66 1.53
1.19 1.33
0.13 0.18
0.194 0.116
0.91 0.93
1.54 1.90
a
Reference category: NM-NM. Double burden is stunting/short height+overweight/obese. BMI and height status was defined based on WHO reference values. The underweight category was excluded from the analysis due to the small number of underweight participants. M-M = two Mayan surnames; M-NM = one Mayan and one non-Mayan surname; NM-NM = two non-Mayan surnames. Significant p < 0.05 values are shown in bold, italic font. Data adjusted by age. b
More research is needed to describe the social and health factors that might be related to the potential growth retardation and nutrition imbalance of mixed ancestry children. Children living in the east and south of Merida (where there is a higher proportion of the NM-M population) receive hypercaloric, vitamin-enriched nutritional supplements as a part of in-kind nutritional programmes, similar to what Leroy and colleagues reported in rural communities (Leroy et al., 2010). This effort operates under the supposition that offering more calories and vitamins to children from underserved communities will prevent malnutrition and help them to grow taller. Research to further understand the impact of this type of programme on not only height but weight is recommended. Recent studies on Maya families from the south of Merida have described how this population has undergone a nutritional transition, with a shift from traditional and locally produced foods to a globalized diet with a high presence of processed
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Table 6. Multinominal logistic regression models association of BMI and height status with income levela, Merida, Mexico, 2012 95% CI Status Adequate height Intermediate income Lower income Short height Intermediate income Lower income Stunted Intermediate income Lower income Healthy BMI Intermediate income Lower income Overweight Intermediate income Lower income Obesity Intermediate income Lower income Double burden Intermediate income Lower income
OR
SE
p>z
Lower
Upper
0.65 0.67
0.13 0.17
0.198 0.000
0.56 0.54
0.78 0.84
0.90 1.23
0.12 0.11
0.389 0.071
0.71 0.98
1.14 1.56
1.33 2.18
0.24 0.23
0.232 0.001
0.83 1.39
2.14 3.34
0.32 0.47
0.10 0.10
0.000 0.000
0.26 0.38
0.39 0.58
1.08 1.12
0.17 0.11
0.494 0.311
0.86 0.89
1.37 1.42
1.69 1.81
0.17 0.20
0.002 0.004
1.21 1.21
2.35 2.72
0.97 10.50
0.18 0.17
0.894 0.021
0.681 1.06
1.40 2.13
a
Reference category: higher income. BMI and height status was defined based on the WHO reference values. The underweight category was excluded from the analysis due to the small number of underweight participants. Significant p < 0.05 values are shown in bold, italic font. Data are adjusted by age.
products, high in sugar, fats and poor in micronutrients and fibre (Azcorra et al., 2013b; Bogin et al., 2014). Nutritional transition is not necessarily bad for health. From 2006 to 2012 the rates of stunting in urban communities of Yucatan declined by 12% in 1- to 4-year-old children. It is possible that increased availability of energy in foods is contributing to reduced rates of chronic malnutrition among urban Maya children. However, this shift in the dietetic pattern seems to be related to the combination of short stature and overweight/obesity in children (nutritional double burden) resulting from a diet deficient in essential nutrients for lineal growth, but excessive in total energy (Steven et al., 2012). Previous studies in the Guatemalan Mayan migrant population conducted in the US (where ‘Mayan’ was defined as those who had migrated from Guatemala, irrespective of their surnames or self-identity) showed a similar prevalence of overweight and obesity as in the present study. Another similarity was that girls were more likely to be overweight while boys were more likely to be obese. The authors of that study described the changes
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in diet as a result of migration, with greater access to food, resulting in a high frequency of overweight and obesity (Smith et al., 2002). However, in the present study, a similar prevalence was found in the city of Merida, which possibly indicates that migration and acculturation to a different country might not be a determinant factor underlying overweight and obesity among Mayan children. Instead, the westernization of diets might be a global phenomenon affecting not only high-income countries, or touristbased economies in small towns in the Yucatan (Leatherman et al., 2010), but also lower income families living in urban settings of middle-income countries such as Mexico. Socioeconomic status generally (Murasko, 2009), as well as Mayan ethnicity (Makkes et al., 2011), have been considered to have a positive relation with children’s height (Murasko, 2009), but in this sample it was found that short stature and stunting were also prevalent among children without Mayan surnames (NM-NM children). Further studies will be needed to better understand the factors underlying the high prevalence of short stature and stunting among children living in Merida. Inter-generational influences of adverse living conditions have been proposed to explain the persistence of linear growth deficit among Maya children in Yucatan (Azcorra et al., 2013a). This study demonstrated that overweight/obesity and also short stature are common among the Meridan population aged 6–12 years attending public primary schools. Short height and stunting was more common among children from the lower income group. It was also found that children with two Mayan surnames and those with one Mayan surname and one non-Mayan surname might be more likely to develop a short height accompanied by being overweight/obese. In conclusion, overweight, obesity and short stature are major health issues among children aged 6–12 attending primary public schools of Merida, Yucatan. These health issues affect children from the higher income group less, when compared with intermediate and lower income groups. Short height was more common among children in the lower income group. This study provides useful information supporting the view that childhood overweight/obesity and short stature are global health problems that are common in urbanized areas.
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