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Association of rs9939609-FTO with metabolic syndrome components among women from Mayan communities of Chiapas, Mexico

Journal of Physiological Anthropology volume 40, Article number: 11 (2021) Cite this article

Abstract

Background

Metabolic syndrome (MetS) is a complex cluster of risk factors, considered as a polygenic and multifactorial entity. The objective of this study was to determine the association of rs9939609-FTO polymorphism and MetS components in adult women of Mayan communities of Chiapas.

Methods

In a cross-sectional study, sociodemographic, anthropometric, clinical, and biochemical data were obtained from 291 adult women from three regions of Chiapas, Mexico. The prevalence of MetS and the allele and genotype frequencies of the rs9939609-FTO were estimated. Multivariate logistic regression models were used to assess the association of the single nucleotide polymorphism (SNP) with each of the MetS components.

Results

The MetS prevalence was 60%. We found a statistically significant association between rs9939609-FTO and hyperglycemia in the dominant model (OR 2.6; 95% CI 1.3–5.3; p = 0.007).

Conclusions

Women from Mayan communities of Chiapas presented a high prevalence of MetS and a relevant association of the FTO variant with hyperglycemia. This is the first study carried out in these Mayan indigenous communities from Chiapas.

Background

Chronic diseases are one of the biggest challenges that Mexico’s health system is facing [1]. This is due to their high prevalence, great contribution to overall mortality, premature disability, and high costs of their treatment. Metabolic syndrome (MetS) is characterized by the presence of insulin resistance, hyperglycemia and/or type 2 diabetes (T2D), dyslipidemias, abdominal obesity, high blood pressure (HBP), and endothelial dysfunction [2]. All these alterations may sequentially or simultaneously be present in MetS, potentially contribute to the development of cardiovascular diseases (CVD) [3], and confer a high risk of morbidity/mortality [4].

Due to the complexity of this set of pathologies, comprehensive studies are currently carried out for a better understanding of its pathophysiology. MetS has been considered a polygenic and multifactorial entity [5]. Family and population studies show that MetS is influenced by a strong genetic component, with great variability among different ethnic groups. In fact, 45% of first-grade family members of patients with T2D, even at normal glucose levels, show to have insulin resistance [6].

In our study, we evaluated the single nucleotide polymorphism (SNP), rs9939609, located at the first intron of the FTO gene. This SNP is one of the most extensively studied, explaining approximately 1% of body mass index (BMI) heritability [7]. In addition, several studies have systematically confirmed the association of a group of SNPs in the first intron of this gene with obesity-related traits in Europeans [7,8,9], Asian [10, 11], and African populations [12, 13].

With regard to the Mexican mestizo population, there are studies that have shown the association of this genetic variant with the development of the pathologies involved in MetS [14, 15]. Although the function of the FTO protein has not been clearly elucidated, some previous studies linked this protein to impaired fasting glucose and insulin resistance [16,17,18]. However, the association of this FTO variant has not been studied in Mayan indigenous communities from Chiapas, Mexico.

The objective of this research was to determine the prevalence of MetS and the allele frequency of the SNP rs9939609-FTO as well as its association with the components of Mets in women from Mayan indigenous communities of Chiapas, Mexico.

Methods

Study population

The study population belongs to three regions of Mayan ancestry of Chiapas, Mexico: Tzotzil-Tzeltal (11 communities), Selva (79 communities), and Soconusco (2 communities). Data were collected from two cross-sectional studies conducted in 2017–2018 in the regions mentioned above [19, 20]. In total, 310 women participated in these studies. A high percentage of the general population of these regions belongs to marginalized and extremely poor indigenous groups (Fig. 1). Participants with missing information in the main variables of this study were excluded (n = 12) from the analysis. The final sample included 291 individuals. All participants gave their informed consent for inclusion in the study.

Fig. 1
figure 1

Study area: Tzotzil-Tzeltal, Selva, and Soconusco regions of Chiapas, Mexico

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Data collection

A validated structured questionnaire was applied with the following sections: sociodemographic data, non-pathological personal history, family medical history, anthropometric and clinical measures, and frequency of food consumption. Sociodemographic data included age, geographic area, ethnicity and years of schooling, household items, and type of cooking fuel.

Family medical history included first and second degree of consanguinity relatives’ diseases: obesity, diabetes, HBP, and CVD. Non-pathological personal history included smoking and alcohol consumption.

Anthropometric and clinical assessment

Weight (kg) was measured by electronic scales (Model UM081, Tanita Corporation, accuracy ± 100 g, Tokyo, Japan). Height (m) was measured using stadiometers (SECA, accuracy ± 1 mm, Berlin, Germany). Waist circumference was measured by anthropometric tapes (SECA, precision ± 1 mm, Berlin, Germany). BMI was estimated as weight divided by height squared. Then, weight status was categorized as follows: underweight and normal weight (BMI < 25 kg/m2) and overweight or obesity (BMI ≥ 25 kg/m2).

Blood pressure was measured twice, using a digital monitor (Model CH-453, Citizen, Japan). The readings were taken with the participant seated and after a 5-min rest.

Frequency of food consumption

The frequency of food intake was assessed by using a 37-item food frequency questionnaire (FFQ) [19]. Participants were asked on how often they consumed each food over 1 week. The frequency of food intake was categorized as follows: 0–1, 2–4, or 5 or more times per week.

Biochemical measurements

Fasting 5-mL blood samples (10 h) were taken from the antecubital vein for biochemical analysis. The determinations of serum glucose, triglycerides, and HDL-c were performed by photometric enzymatic methods (Diasys, Diagnostic System, Holzheim, Germany), in an automated analyzer (Vitalab Selectra E, Vitalab Scientific, Île-de-France, France).

Classification of metabolic syndrome (MetS)

MetS was identified using the criteria of the Joint Statement of International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity [21]. MetS was defined as the presence of three or more of the following conditions: elevated waist circumference (≥ 80 cm); elevated triglycerides (≥ 150 mg/dL) or drug treatment for elevated triglycerides; reduced HDL-c < 50 mg/dL or drug treatment for reduced HDL-c; systolic blood pressure (SBP) ≥ 130 mm Hg or diastolic blood pressure (DBP) ≥ 85 mmHg or antihypertensive drug treatment in a patient with a history of hypertension; and fasting glucose levels ≥ 100 mg/dL or drug treatment for elevated glucose.

Genotyping

The isolation of genomic DNA was performed in ECOSUR Health Laboratory at San Cristobal de Las Casas, Chiapas, using commercial kits based on columns (Universal Quick-DNATM Kit/Zymo Research, USA). The DNA samples were frozen at − 42 °C and transported to the Biochemistry Unit of the Centro Médico Nacional Siglo XXI (National Medical Center of the 21st Century) in Mexico City, where all the molecular analyses were performed. The purity and concentration of genomic DNA were verified by spectrophotometry at 260/280 nm (Epoch, Biotek, Winooski, Vermont), and the integrity of the DNA was confirmed by electrophoresis in an agarose gel at 0.8%. The analysis of the SNP rs9939609-FTO was made using TaqMan-probe-based real-time PCR (7900HT Applied Biosystems, Foster City, CA, USA), following standard protocols. A concordance of 100% was observed in 30 duplicate samples for quality control of each probe.

Statistical analysis

A descriptive analysis of the variables was performed by MetS using percentages and 95% confidence intervals (95% CI) for categorical variables. For continuous variables, we have conducted the Shapiro–Wilk test for normal data distribution. Medians and interquartile ranges were calculated for skewed biochemical and dietary measurements. Differences between groups were analyzed using chi-square tests for categorical variables and Mann- Whitney U tests for continuous variables. Allele and genotype frequencies were estimated. Hardy–Weinberg equilibrium (HWE) was estimated for the variant under study. To assess the association between MetS components and rs9939609-FTO, logistic regression models assuming three different modes of inheritance (codominant, dominant, and recessive) were fitted. Odds ratios (ORs) and 95% CI were estimated to measure the magnitude of association between rs9939609-FTO and MetS components. Models were adjusted for age (years, continuous), BMI (kg/m2, continuous), schooling (years, continuous), and presence of T2D. For all the analyses, we considered a p-value of ≤ 0.05 as a significant level. To assess a possible interaction between geographic region or previously diagnosed hypertension and rs9939609-FTO, we introduced the product terms of the variables in the logistic regression models and considered p < 0.05 in the likelihood ratio test as statistically significant. All analyses were performed using STATA software (StataCorp, College Station, TX 77,845, USA; version 16.1, 2019).

Results

Sociodemographic characteristics of the study population by MetS

The sociodemographic characteristics of the study population by MetS are shown in Table 1. Women over 45 years had the highest prevalence of MetS (75%).

Table 1 Sociodemographic characteristics of the study population by MetS
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Women living in rural areas had a higher prevalence of MetS than those living in urban areas (localities of more than 2500 people) which in Mexico represents more than 70% of its geographical area.

Women with less than 5 years of schooling had a higher prevalence of MetS than those with the highest schooling. Women who speak an indigenous language had a slightly higher prevalence of MetS (62%) than women who only speak Spanish (60%). With regard to household conditions, a great proportion of the study population lacks basic amenities such as piped water inside the house, stove, and fridge. However, no marked differences were observed.

Anthropometric, clinical, and biochemical parameters of the study population by MetS

Table 2 shows the anthropometric, clinical, and biochemical parameters of the study population by MetS. Ninety-two percent of the total participants had a waist circumference greater than 80 cm. A high percentage of them (88%) presented a BMI ≥ 25 kg/m2, 61% had high level of triglycerides (≥ 150 mg/dL), and 70% had low HDL-c (< 50 mg/dL). We identified a low percentage of women with alterations in fasting glucose and blood pressure levels (22% and 32%, respectively).

Table 2 Anthropometric, clinical, and biochemical parameters of the study population by MetS
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Among women with MetS, 99% had a waist circumference greater than 80 cm, 96% presented overweight or obesity, 87% had high levels of triglycerides, and 85% had low HDL-c levels. Thirty-three percent presented hyperglycemia and 49% HBP.

Comorbidities and frequency of food consumption according to MetS

Women with MetS had a higher prevalence of T2D, hypertension, and polycystic ovary syndrome than women without MetS (Table 3). They consumed the following food groups five or more times per week: dairy products (41%), fruits (40%), vegetables (37%), red meat (3.5%), poultry (1.7%), cereals and tubers (100%), legumes (75%), and sugar-sweetened beverages (13.3%). No statistically significant differences between food groups were observed between women with and without MetS.

Table 3 Comorbidities and frequency of food intake by metabolic syndrome in women from Chiapas, México
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Allele and genotype frequencies of the study population

Table 4 shows the allele frequencies of the rs9939609-FTO analyzed in our study population and their comparison with those reported in other studies for main blocks of the population (American, European, East Asian, African) and Mexican population. In our study, the SNP rs9939609 was in HWE (p > 0.05). TT genotype was identified in 233 samples (80%), TA in 54 samples (18%), and AA in 4 samples (1%). The frequency of the A allele was 0.10.

Table 4 Comparison of the allele frequencies of rs-9939609/FTO between our study population with other population studies
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There are statistically significant differences between the frequencies reported in our study and those reported for American, European, African, and Mexican populations. No significant differences were found between the allele frequency reported for the East Asian population and our study population.

Association between MetS components and different rs9939609-FTO genotypes in the study population

We analyzed different modes of inheritance (co-dominant, dominant, and recessive) for the rs9939609-FTO genotypes with regard to MetS components. Table 5 shows the association between rs9939609-FTO and hyperglycemia in the study population. For this analysis, only individuals who presented fasting glucose levels ≥ 100 mg/dL were considered (treatment for elevated glucose was not included as an outcome). A significant association was observed between the rs9939609/FTO and hyperglycemia in the dominant model. The TA/AA genotype carriers were twice more likely to develop hyperglycemia than those with the TT genotype (OR = 2.6; 95% CI 1.3–5.3, p = 0.007).

Table 5 Associations between rs9939609-FTO and hyperglycemia in women from Mayan communities of Chiapas, Mexico
Full size table

No significant interactions were observed for the geographic region or previously diagnosed hypertension (p for interaction > 0.05).

Discussion

MetS has been associated with an increased risk of developing CVD and T2D [21]. In Mexico, some studies have been conducted to estimate the proportion of the Mexican population with MetS. For instance, Aguilar-Salinas et al. [24] reported in 2004 a prevalence of 14% according to the World Health Organization (WHO) criteria and 27% according to the National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATPIII) criteria in population from 20 to 69 years of age. González-Villalpando et al. [14] in a study performed among the Mexican diabetic population reported MetS prevalence of 39.9% and 59.9% in males and females, respectively, based on the NCEP-ATPIII criteria. It is noteworthy that previous studies were carried out in other Mexican states such as Guanajuato, Jalisco, Puebla, Baja California Norte, Morelos, Querétaro, and Mexico City [25]. By contrast, in the southeast region of the country with a high proportion of the indigenous population, only few studies have been carried out on this topic. As an example, the study conducted by Castro et al. in 2011 identified a prevalence of 49% of MetS in adults from Merida, Yucatan, according to the IDF criteria [26]. We found that 60% of the participants in our study presented MetS, under the criteria published by Alberti et al. in 2009 [21], which represents a much higher percentage than the previously mentioned for the Mayan population [26], and it is even higher than the one reported for the overall Mexican population [27]. Our study population is conformed by a high percentage of native peoples (35%), with low educational levels (36%). Moreover, they live in poor household conditions with low availability of public services. They belong to population groups who in the last decades have changed their diet and physical activity, adopting habits and activities that predispose them to suffer various diseases [28], especially those of cardiovascular and endocrine-metabolic nature. As mentioned above, the study population is a vulnerable population at high risk to develop these important diseases, due to the interaction of several risk factors such as diet, physical activity, and socioeconomic level, among others.

Regarding the frequency of the variant rs9939609 of the FTO gene, we found differences between our results with those previously reported for American, European, African [23], and Mexican populations [22, 29]. This could be due to the distinction among ethnic groups analyzed. Nevertheless, it cannot be ruled out that different sample sizes might explain such differences in the results. In the case of allele frequencies reported for the East Asian population [23], no differences were observed when compared with our results.

This FTO variant has been extensively studied because it presents a strong association with obesity markers, i.e., a 3-kg increase of additional body weight for each copy of the risk allele in carriers has been documented in several populations [7]. Additionally, several research lines have linked this SNP in FTO to variations in food consumption patterns [30, 31]. Epidemiological studies suggest a positive association between the risk genotype of FTO and high energy consumption [32, 33], low satiety power [30], higher protein intake [34], and greater preference for high-fat meals [35]. Although further evidence shows contradictory results, for instance, some studies have found less robust associations and outcomes in opposite directions [36,37,38]. A study among the German population found that SNPs of the FTO were strongly associated with obesity and T2D [9, 39]. Other studies have also demonstrated that the carriers of the A allele were more likely to develop hyperglycemia than their counterparts with the T allele [40,41,42].

Studies carried out in other regions of Mexico have analyzed the association of FTO polymorphisms with MetS components [17, 43,44,45]. However, none of them has found a significant association of this polymorphism with hyperglycemia. In our study, we found a statistically significant association between the rs9939609/FTO and hyperglycemia. Women with TA/AA genotypes showed a higher probability of hyperglycemia than women with the TT genotype (p = 0.007).

Differences between our results and those reported in the literature may be due to different factors, for example, the ethnicity of the population evaluated, differences in body composition, diet, and the presence of other comorbidities [30].

It is remarkable that no previous studies have been carried out in this Mayan region of Mexico on the relationship of this rs9939609-FTO variant with MetS components. This paper would be the first one to report for Mayan indigenous populations an association between the presence of A allele of rs9939609/FTO and hyperglycemia.

Conclusions

In our study, the TA/AA genotypes of the rs9939609-FTO polymorphism increased the risk of hyperglycemia among women from three Mayan regions of Chiapas, Mexico. This finding has never been reported before in the Mayan indigenous population from Chiapas, specifically, in women with a high prevalence of MetS (60%).

Thus, this investigation sets up the basis to understand the influence of a common variant on cardiometabolic risk factors among this population.

However, further studies in the Mexican indigenous population are required, particularly in the most vulnerable groups to generate more evidence about this topic.

Finally, on the basis of our results, we recommend to implement effective public health policies to control and prevent the increasing MetS prevalence and its cardiovascular effects among the indigenous population of Mexico.

Availability of data and materials

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

Abbreviations

MetS:

Metabolic syndrome

SNPs:

Single nucleotide polymorphisms

FTO:

Fat mass and obesity-associated gene

IR:

Insulin resistance

T2D:

Type 2 diabetes

HBP:

High blood pressure

BMI:

Body mass index

OB:

Obesity

HDL-c:

High-density lipoprotein cholesterol

SBP:

Systolic blood pressure

DBP:

Diastolic blood pressure

HWE:

Hardy–Weinberg equilibrium

OR:

Odds ratio

CI:

Confidence intervals

CVD:

Cardiovascular disease

WHO:

World Health Organization

NCEP-ATPIII:

National Cholesterol Education Program Adult Treatment Panel III

References

  1. Córdova-Villalobos J, Meléndez J, Lara-Esqueda A, et al. Chronic non-communicable diseases in Mexico: epidemiologic synopsis and integral prevention. Salud Pública Méx. 2008;50:419–27.

    Article  PubMed  Google Scholar 

  2. De Fronzo R, Ferrannini E. Insulin resistance: a multifocal syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14:173–94.

    Article  Google Scholar 

  3. Stern M. The insulin resistance syndrome: the controversy is dead, long live the controversy. Diabetologia. 1994;37:956–8. https://doi.org/10.1007/BF00400955.

    CAS  Article  PubMed  Google Scholar 

  4. Isomma B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24:683–9. https://doi.org/10.2337/diacare.24.4.683.

    Article  Google Scholar 

  5. Groop L. Genetics of the metabolic syndrome. Br J Nutr. 2000;83:39–48. https://doi.org/10.1017/s0007114500000945.

    Article  Google Scholar 

  6. Beck-Nielsen H, Groop L. Metabolic and genetic characterization of prediabetic states. Sequence of events leading to non-insulin dependent diabetes mellitus. J Clin Invest. 1994;94:1714–21. https://doi.org/10.1172/JCI117518.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Frayling T, Timpson N, Weedon M, et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science. 2007;316:889–94. https://doi.org/10.1126/science.1141634.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Dina C, Meyre D, Gallina S, et al. Variation in FTO contributes to childhood obesity and severe adult obesity. Nat Genet. 2007;39:724–6. https://doi.org/10.1038/ng2048.

    CAS  Article  PubMed  Google Scholar 

  9. Scuteri A, Sanna S, Chen W, et al. Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits. PLoS Genet. 2007;3:1200–10. https://doi.org/10.1371/journal.pgen.0030115.

    CAS  Article  Google Scholar 

  10. Chang Y, Liu P, Lee W, et al. Common variation in the fat mass and obesity-associated (FTO) gene confers risk of obesity and modulates BMI in the Chinese population. Diabetes. 2008;57:2245–52. https://doi.org/10.2337/db08-0377.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Fang H, Li Y, Du S, et al. Variant rs9939609 in the FTO gene is associated with body mass index among Chinese children. BMC Med Genet. 2010;11:136. https://doi.org/10.1186/1471-2350-11-136.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Grant S, Li M, Bradfield J, et al. Association analysis of the FTO gene with obesity in children of Caucasian and African ancestry reveals a common tagging SNP. PLoS One. 2008;3:1746. https://doi.org/10.1371/journal.pone.0001746.

    CAS  Article  Google Scholar 

  13. Song Y, You N, Hsu Y, et al. FTO polymorphisms are associated with obesity but not diabetes risk in postmenopausal women. Obesity. 2008;16:2472–80. https://doi.org/10.1038/oby.2008.408.

    CAS  Article  PubMed  Google Scholar 

  14. Villalobos M, Flores M, Villarreal M, et al. The FTO gene is associated with adulthood obesity in the Mexican population. Obesity. 2008;16:2296–301. https://doi.org/10.1038/oby.2008.367.

    CAS  Article  Google Scholar 

  15. León P, Villamil H, Villalobos M, et al. Contribution of common genetic variants to obesity and obesity-related traits in Mexican children and adults. PLoS One. 2013;8:70640. https://doi.org/10.1371/journal.pone.0070640.

    CAS  Article  Google Scholar 

  16. Saber-Ayad M, Manzoor S, El Serafi A, Mahmoud I, Hammoudeh S, Rani A, Abusnana S, Sulaiman N. The FTO rs9939609 “A” allele is associated with impaired fasting glucose and insulin resistance in Emirati population. Gene. 2019;10(681):93–8. https://doi.org/10.1016/j.gene.2018.09.053. Epub 2018 Sep 29. PMID: 30273662.

    CAS  Article  Google Scholar 

  17. Taneera J, Prasad RB, Dhaiban S, Mohammed AK, Haataja L, Arvan P, et al. Silencing of the FTO gene inhibits insulin secretion: an in vitro study using GRINCH cells. Mol Cell Endocrinol. 2018. https://doi.org/10.1016/j.mce.2018.06.003.

  18. Shimaoka I, Kamide K, Ohishi M, Katsuya T, Akasaka H, Saitoh S, et al. Association of gene polymorphism of the fat-mass and obesity-associated gene with insulin resistance in Japanese. Hypertens Res. 2010;33(3):214–8.

    CAS  Article  PubMed  Google Scholar 

  19. Flores E, Ochoa-Díaz-López H, Castro-Quezada I, et al. Intrauterine growth restriction and overweight, obesity, and stunting in adolescents of indigenous communities of Chiapas, Mexico. Eur J Clin Nutr. 2020;74:149–57. https://doi.org/10.1038/s41430-019-0440-y.

    Article  Google Scholar 

  20. Causa R, Ochoa-Díaz-López H, Dor A, Rodríguez F, Solís R, Pacheco A. Emerging arboviruses (dengue, chikungunya, and Zika) in Southeastern Mexico: influence of socio-environmental determinants on knowledge and practices. Cad Saúde Pública. 2020;36:e00110519. https://doi.org/10.1590/0102-311x00110519.

    Article  PubMed  Google Scholar 

  21. Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644.

    CAS  Article  PubMed  Google Scholar 

  22. The Population Architecture using Genomics and Epidemiology (PAGE) study. https://www.pagestudy.org. Accessed 10 Mar 2020.

  23. Karczewski KJ, Francioli LC, Tiao G, et al. The mutational constraint spectrum quantified from variation in 141,456 humans. Nature. 2020;581:434–43. https://doi.org/10.1038/s41586-020-2308-7.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Aguilar C, Rojas R, Gómez F, et al. High prevalence of metabolic syndrome in Mexico. Arch Med Res. 2004;35:76–81. https://doi.org/10.1016/j.arcmed.2003.06.006.

    Article  Google Scholar 

  25. Lorenzo C, Williams K, González C, Haffner S. The prevalence of the metabolic syndrome did not increase in Mexico City between 1990–1992 and 1997–1999 despite more central obesity. Diabetes Care. 2005;28:2480–5. https://doi.org/10.2337/diacare.28.10.2480.

    Article  PubMed  Google Scholar 

  26. Castro C, Hernández V, Arjona R. Prevalencia de Síndrome Metabólico en sujetos adultos que viven en Mérida, Yucatán, Mexico. Rev Bioméd. 2001;22:49–58. https://doi.org/10.32776/revbiomed.v22i2.100.

    Article  Google Scholar 

  27. Gutiérrez A, Datta S, Méndez R. Prevalence of metabolic syndrome in Mexico: a systematic review and meta-analysis. Metab Syndr Relat Disord. 2018;16:395–405. https://doi.org/10.1089/met.2017.0157.

    Article  Google Scholar 

  28. Ruiz W, Gurri FD. La doble carga de la transición nutricional en zonas rurales de la frontera sur. In: Ochoa H, Academia Nacional de Medicina de México, editors. La Frontera sur de México, ¿Una salud en crisis?. CDMX: Academia Nacional de Medicina de México; 2018. p. 39–48.

  29. Cruz M, Valladares A, Garcia J, et al. Candidate gene association study conditioning on individual ancestry in patients with type 2 diabetes and metabolic syndrome from Mexico City. Diabetes Metab Res Rev. 2010;26:261–70. https://doi.org/10.1002/dmrr.1082.

    CAS  Article  PubMed  Google Scholar 

  30. Wardle J, Carnell S, Haworth C, Farooqi I, O’Rahilly S, Plomin R. Obesity associated genetic variation in FTO is associated with diminished satiety. J Clin Endocrinol Metab. 2008;3:3640–3. https://doi.org/10.1210/jc.2008-0472.

    CAS  Article  Google Scholar 

  31. Tanofsky M, Han J, Anandalingam K, et al. The FTO gene rs9939609 obesity-risk allele and loss of control over eating. Am J Clin Nutr. 2009;90:1483–14888. https://doi.org/10.3945/ajcn.2009.28439.

    CAS  Article  Google Scholar 

  32. Cecil J, Tavendale R, Watt P, Hetherington M, Palmer C. An obesity-associated FTO gene variant and increased energy intake in children. N Engl J Med. 2008;359:2558–66. https://doi.org/10.1056/NEJMoa0803839.

    CAS  Article  PubMed  Google Scholar 

  33. Qi Q, Downer M, Kilpelainen T, et al. Dietary intake, FTO genetic variants, and adiposity: a combined analysis of over 16,000 children and adolescents. Diabetes. 2015;64:2467–76. https://doi.org/10.2337/db14-1629.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Tanaka T, Ngwa J, van-Rooij FJA, et al. Genome-wide meta-analysis of observational studies shows common genetic variants associated with macronutrient intake. Am J Clin Nutr. 2013;97:1395–402. https://doi.org/10.3945/ajcn.112.052183.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Timpson N, Emmett P, Frayling T, et al. The fat mass- and obesity-associated locus and dietary intake in children. Am J Clin Nutr. 2008;88:971–8. https://doi.org/10.1093/ajcn/88.4.971.

    CAS  Article  PubMed  Google Scholar 

  36. Livingstone K, Celis C, Lara J, et al. Associations between FTO genotype and total energy and macronutrient. Obes Rev. 2015;16:666–78. https://doi.org/10.1111/obr.12290.

    CAS  Article  PubMed  Google Scholar 

  37. Steemburgo T, Azevedo M, Gross J, Milagro F, Campion J, Martínez J. The rs9939609 polymorphism in the FTO gene is associated with fat and fiber intakes in patients with type 2 diabetes. J Nutrigenet Nutrigenomics. 2013;6:97–106. https://doi.org/10.1159/000350741.

    CAS  Article  PubMed  Google Scholar 

  38. Speakman J, Rance K, Johnstone A. Polymorphisms of the FTO gene are associated with variation in energy intake, but not energy expenditure. Obesity. 2008;16:1961–5. https://doi.org/10.1038/oby.2008.318.

    CAS  Article  PubMed  Google Scholar 

  39. Hinney A, Nguyen TT, Scherag A, et al. Genome wide association (GWA) study for early onset extreme obesity supports the role of fat mass and obesity associated gene (FTO) variants. PLoS One. 2007;2:e1361. https://doi.org/10.1371/journal.pone.0001361.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Sikhayeva N, Iskakova A, Saigi-Morgui N, Zholdybaeva E, Eap CB, Ramanculov E. Association between 28 single nucleotide polymorphisms and type 2 diabetes mellitus in the Kazakh population: a case-control study. BMC Med Genet. 2017;18:76. https://doi.org/10.1186/s12881-017-0443-2.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Lappalainen T, Kolehmainen M, Schwab U, et al. Association of the FTO gene variant (rs9939609) with cardiovascular disease in men with abnormal glucose metabolism - the Finnish Diabetes Prevention Study. Nutr Metab Cardiovasc Dis. 2011;21:691–8. https://doi.org/10.1016/j.numecd.2010.01.006.

    CAS  Article  PubMed  Google Scholar 

  42. Szkup M, Owczarek AJ, Schneider D, Brodowski J, Łój B, Grochans E. Associations between the components of metabolic syndrome and the polymorphisms in the peroxisome proliferator-activated receptor gamma (PPAR-γ), the fat mass and obesity-associated (FTO), and the mela-nocortin-4 receptor (MC4R) genes. Aging. 2018;10:72–82. https://doi.org/10.18632/aging.101360.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. López G, Estrada A, Suárez T, Tejero M, Fernández J, Galván M. Common polymorphisms in MC4R and FTO genes are associated with BMI and metabolic indicators in Mexican children: differences by sex and genetic ancestry. Gene. 2020;754:144840. https://doi.org/10.1016/j.gene.2020.144840.

    CAS  Article  Google Scholar 

  44. Saucedo R, Valencia J, Gutierrez C, et al. Gene variants in the FTO gene are associated with adiponectin and TNF-alpha levels in gestational diabetes mellitus. Diabetol Metab Syndr. 2017;9:32. https://doi.org/10.1186/s13098-017-0234-0.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Jiménez A, Musalem C, Cárdenas H, et al. Common polymorphisms linked to obesity and cardiovascular disease in Europeans and Asians are associated with type 2 diabetes in Mexican Mestizos. Medicina (Kaunas). 2019;55:40. https://doi.org/10.3390/medicina55020040.

    Article  Google Scholar 

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Acknowledgements

We thank the study participants for their collaboration and to all the personnel who assisted in the fieldwork, specially to the group of dietitians from Universidad de Ciencias y Artes de Chiapas, Universidad del Sureste, and Instituto de Estudios Superiores de Chiapas; the Biochemistry Unit of the National Medical Center of the 21st Century, in Mexico City, particularly to Dr. Miguel Cruz-López for his invaluable contribution to the genotyping analysis.

Funding

This study was supported by the National Council for Science and Technology of Mexico (CONACYT). PNO received a PhD scholarship from CONACYT. IC-Q received a postdoctoral scholarship from CONACYT.

Author information

Authors and Affiliations

  1. Health Department, El Colegio de La Frontera Sur, San Cristóbal de Las Casas, Chiapas, Mexico

    Pilar E. Núñez Ortega, Itandehui Castro-Quezada, Roberto Solís-Hernández, Rosario García-Miranda & Héctor Ochoa-Díaz-López

  2. National Council for Science and Technology, Postgraduate College Campus Puebla, Puebla, Mexico

    María E. Meneses

  3. Facultad de Medicina, Universidad de Colima, Colima, Mexico

    Iván Delgado-Enciso

  4. Instituto Estatal de Cancer, Secretaria de Salud de Colima, Colima, Mexico

    Iván Delgado-Enciso

  5. Health Department, El Colegio de La Frontera Sur, Villahermosa, Tabasco, Mexico

    César Antonio Irecta-Nájera

  6. Faculty of Nutrition and Food Science, University of Science and Arts of Chiapas, Tuxtla Gutiérrez, Chiapas, Mexico

    Elena Flores-Guillén

  7. School of Languages-Campus San Cristobal, Autonomous University of Chiapas, San Cristóbal de Las Casas, Chiapas, Mexico

    Rosario García-Miranda

  8. Unidad de Investigación Médica en Bioquímica, Hospital de Especialidades, Centro Médico Nacional Siglo XXI. Instituto Mexicano del Seguro Social, Mexico City, Mexico

    Adán Valladares-Salgado & Daniel Locia-Morales

Authors
  1. Pilar E. Núñez Ortega
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  2. María E. Meneses
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  6. Roberto Solís-Hernández
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  11. Héctor Ochoa-Díaz-López
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Contributions

H.O.-D-L conceived and directed the project. H.O.-D-L and P.E.N.-O. designed and planned the study. E.F-G and P.E.N.-O. supervised the data collection. P.E.N.-O, A.V.-S., and D.L-M conducted the analysis of genotyping at the Biochemistry Unit, Specialties Hospital, National Medical Center, Century XXI IMSS. R.S.-H. and P.E.N.-O performed the statistical analysis. H.O.-D-L, P.E.N.-O, I.C.-Q., and C.A.I.-N. contributed to the analysis and interpretation of the results. P.E.N.-O. and H.O.-D-L wrote the manuscript with contributions from all co-authors. All the co-authors revised the manuscript and approved the final version.

Corresponding author

Correspondence to Héctor Ochoa-Díaz-López.

Ethics declarations

Ethics approval and consent to participate

The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Research Ethics Committee of El Colegio de la Frontera Sur (CEI-O-076/16). Informed consent was obtained from all subjects involved in the study.

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Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Ortega, P.E.N., Meneses, M.E., Delgado-Enciso, I. et al. Association of rs9939609-FTO with metabolic syndrome components among women from Mayan communities of Chiapas, Mexico. J Physiol Anthropol 40, 11 (2021). https://doi.org/10.1186/s40101-021-00259-9

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  • DOI: https://doi.org/10.1186/s40101-021-00259-9

Keywords

  • Metabolic syndrome
  • Single nucleotide polymorphisms
  • FTO
  • Mayan indigenous women
  • Chiapas
  • Mexico

Journal of Physiological Anthropology

ISSN: 1880-6805

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