Sweetened beverages intake, hyperuricemia and metabolic syndrome. The Mexico City Diabetes Study

Ingesta de bebidas endulzadas, hiperuricemia y síndrome metabólico. Estudio de la Diabetes en la Ciudad de México

Rubén López-Molina, MSc,⁽¹⁾ Socorro Parra-Cabrera, DSc,⁽¹⁾ Ruy López-Ridaura, MD, PhD,⁽¹⁾ María E González-Villalpando, MD,⁽²⁾ Ele Ferrannini, MD,⁽³⁾ Clicerio González-Villalpando, MD.^(1,2)

(1) Unidad de Investigación en Diabetes y Riesgo Cardiovascular, Instituto Nacional de Salud Pública. México.

(3) Department of Medicine, School of Medicine, University of Pisa. Italy.

Corresponding author

Abstract

Objective. To determine prevalence of hyperuricemia and its relation with intake of sweetened beverages (SB) and metabolic syndrome (MS) in low income urban Mexican population.

Materials and methods. A cross-sectional analysis of The Mexico City Diabetes Study, a prospective population-based investigation (1 173 participants) was performed. We used logistic regression, adjusted by pertinent variables. We determined prevalence of hyperuricemia and explored associations of uric acid levels with MS and intake of SB.

Results. Prevalence of hyperuricemia was 26.5 and 19.8% in males and females respectively. In an adjusted multivariate model, body mass index, waist circumference, and triglyceride were higher as uric acid quartiles increased (p<0.005-0.001). The odds ratio for MS was 1.48 for 3rd uric acid quartile and 2.03 for 4th quartile. Higher consumption of SB was associated with higher uric acid levels (p<0.001).

Conclusion. Prevalence of hyperuricemia is high. Potential association with intake of SB, resulting in metabolic alterations should be considered.

Resumen

Objetivo. Determinar prevalencia de hiperuricemia en población mexicana urbana de bajos ingresos, relación con ingesta de bebidas endulzadas y síndrome metabólico.

Material y métodos. Análisis transversal del Estudio de la Diabetes en la Ciudad de México (1 173 participantes), utilizando regresión logística, ajustada por variables pertinentes. Se determinó prevalencia de hiperuricemia, se exploraron asociaciones de niveles de ácido úrico con síndrome metabólico y bebidas endulzadas.

Resultados. La prevalencia de hiperuricemia fue 26.5 y 19.8%, hombres y mujeres, respectivamente. El índice de masa corporal, circunferencia de cintura y triglicéridos fueron más altos con cada cuartil de ácido úrico (p<0.005 - 0.001). La razón de momios para síndrome metabólico fue 1.48 para el tercer cuartil y 2.03 para el cuarto. Se encontró mayor consumo de bebidas endulzadas a mayores niveles de acido úrico (p<0.001).

Conclusión. La prevalencia de hiperuricemia es alta. La asociación con bebidas endulzadas y las alteraciones metabólicas resultantes deben considerarse.

Palabras clave: hiperuricemia; bebidas; metabolismo; México.

The interest in serum uric acid (UA) has re-emerged due to its possible role as a cardiovascular risk factor. Moreover, hyperuricemia (HU) contributes to the development of renal disease, a cardiovascular risk factor.¹ The mechanism by which UA enhances these risks remains under investigation. Excessive dietary intake of fructose has recently emerged as a relevant association, since it is an ingredient in foods and beverages consumed in increasing quantities in Mexico.^2,3 In studies in healthy subjects, physiological increments in insulin concentration acutely decreased renal UA clearance jointly with an increased sodium reabsorption. Hence, the chronic hyperinsulinemia associated with insulin resistance imposes a chronic antiuricosuric and antinatriuretic pressure on the kidney, eventually influencing both UA and blood pressure levels.^4,5 Moreover, HU has been related to endothelial dysfunction and it is considered an independent risk factor for high blood pressure (HBP). The suggested mechanism is UA-mediated glomerular hypertension, cortical vasoconstriction, glomerular damage, and tubular ischemia. The intricacies and the specific sequence of pathophysiologic events remain still a matter of scientific investigation. Recent studies have shown that lowering serum UA by reducing fructose intake and/or the administration of allopurinol, results in improvement of the metabolic alterations.⁶ In view of the high prevalence of the components of the metabolic syndrome (MS) in the Mexican population,⁷ the high carbohydrate content in the Mexican diet,^8,9 and the significant consumption of sweetened beverages with high fructose content in Mexico^10,11 we explored the prevalence of HU, the possible role of sweetened beverage intake and its association with the MS components as elements possibly implicated in the chronic kidney disease epidemic in the country. We present the results of an analysis performed in the latest follow-up phase of the Mexico City Diabetes Study (MCDS).

The MCDS is a population-based, prospective, investigation designed to characterize the prevalence, incidence and natural history of type 2 diabetes (T2D) and cardiovascular risk factors, in low-income urban inhabitants of Mexico City. The methodology and its results have been previously reported.^12,13 The baseline phase started in 1990 with 2 282 men and non-pregnant women (35 to 64 years). For the present analysis, we used the data corresponding to the latest follow-up (2008). In this phase, there were 1 174 participants, 463 (39%) men. One subject did not have UA determination. Therefore, the total cohort was 1 173 subjects. To estimate prevalence, we assumed that self-reported allopurinol users (n=13) had HU independently of their serum UA level. We excluded subjects who self-reported the use of thiazides, (n=39). For the association with MS, we further excluded allopurinol users (n=13) and subjects with incomplete information on metabolic markers (n=5). The final cohort therefore consisted of 1116 subjects, 438 (39%) males. The Institutional Review Board of both the Instituto Nacional de Salud Pública and the Centro de Estudios en Diabetes approved the study protocol. Informed consent was obtained from the participating subjects in accordance with the ethical principles for medical research involving human subjects. All participants underwent a physical exam. Blood pressure (BP) was measured three times, using a calibrated sphygmomanometer, in the sitting position after five min of rest, the mean of the last two readings was used.¹⁴ Height and weight were measured without shoes and upper garments. Body mass index (BMI) was calculated as weight (kilograms) divided by height (meters) squared. Waist circumference (WC) was measured using standard methods. Participants previously diagnosed by a physician with HBP, and reporting use of antihypertensive medication were considered hypertensives regardless of their blood pressure values. For subjects that were not known as hypertensives, we used the criteria of the Joint Commission for The Diagnosis & Treatment of Hypertension (JNC VII).¹⁵ Participants who self-reported that they had a previous diagnosis of T2D by a physician and were receiving pharmacologic treatment for diabetes, were considered to have T2D regardless of their blood glucose values. For subjects not known to be diabetic we used the American Diabetes Association diagnostic criteria (fasting glucose ≥126 mg/dL, or two-hour plasma glucose ≥200 mg/dL after a standard, 75-g oral glucose load).

We used the Food Frequency Questionnaire (FFQ) approach to estimate participant’s usual diet. This instrument was applied at baseline, and it was previously validated in the Mexican population.^16,17 This method is useful to measure dietary patterns in long-term cohorts.¹⁸ To determine the habitual sweetened beverages intake in this population, we established four categories: less than one bottle per week, one bottle per week to less than one bottle a day, one bottle per day and more than one per day. Smoking was defined by self-reporting as current, past smoker or never smoker. Fasting venous blood samples were taken for laboratory determination: Total cholesterol, triglycerides, glucose, creatinine, and uric acid were done in an auto-analyser.¹⁹ HbA_1c was measured using ion-exchange chromatography all at the clinical laboratory of the ABC Hospital, Mexico City. Glomerular Filtration Rate (eGFR) was estimated using the Cockroft-Gault formula. HU was defined using the National Institutes of Health criteria (fasting concentrations: ≥7mg/dL and ≥6mg/dL for men and women, respectively).²⁰ For each of the following four MS components, we used the criteria established in Adult Treatment Panel, (ATP-III): 1) Hyperglycemia (FPG ≥100 mg/dL or pharmacologic treatment for hyperglycemia), 2) Hypertriglyceridemia (fasting triglycerides levels ≥150mg/dl or current use of lipid lowering drugs), 3) Abdominal obesity (WC ≥102 cm and ≥88cm for males and females, respectively), and 4) HBP (blood pressure ≥130/85 mmHg or current use of antihypertensive drugs).²¹ HDL was not used because it was not measured in this follow up. We classified participants as having none, only 1, any 2, any 3 or all 4 criteria, and defined MS with at least any of 3 of these components.

Data are presented as mean±SD, Student t test was used for group comparisons of continuous variables. For the prevalence estimates, we calculated 95% confidence intervals (CI) using the Agresti-Coull binomial confidence intervals for proportions. To explore the possible relationships between UA and the MS components, the population was divided into quartiles of UA concentrations including both male and female participants. To determine if there was an association between MS components and UA quartiles, we calculated odds ratios (OR) and 95% CI, using logistic regression models for the combination of at least three of the MS components. Tests for trend across quartiles were calculated by modelling UA quartiles linearly, using the median value of each quartile; a p-value of <0.05 was considered statistically significant. All models were gender and age adjusted. Additionally, we calculated another model adjusting by years of study, current smoking, glomerular filtration rate and sweetened beverage intake. All statistical analyses were performed using the Stata 12.0 software.

Results

The mean age of the population was 62.8±7 years. Overall, 120 men and 135 women met HU criteria, only 13 (5.3 %) of these subjects were receiving treatment for HU. The mean value of UA level was 5.3 mg /dL for the entire population (1 134 participants excluding thiazide takers). After excluding allopurinol users, the mean UA level was 8.1 ± 0.9 mg/dL and 7.1 ± 1.1 mg/dL for hyperuricemic men and women, respectively. There were no statistically significant differences between the diabetic and hypertensive subgroups as shown in table I.

Upon stratifying the study population by quartile of UA concentrations (table II), BMI, WC, and triglycerides were significantly higher as UA concentrations increased. Mean values for both systolic and diastolic blood pressure levels tended to be similar in all uric acid quartiles. Fasting, 2-hour glucose levels and HbA_1c tended to be high in all groups, reflecting the high prevalence of dysglicemia in this population. Surprisingly, glucose and HbA1c levels decreased across UA quartile. Renal function, as estimated by serum creatinine levels or eGFR, was progressively worse at higher UA levels. The proportion of subjects with high intake of sweetened beverage (> 1 bottle/day) increased steadily with UA quartile (p<.001). We estimated that the intake of 1 bottle of sweetened beverage per day could provide 45.9% of total daily fructose intake.

The proportion of individual MS components in the UA quartiles is shown in table III. The prevalence of obesity (BMI ≥30 kg/m²) was higher with each incremental level as was the proportion of subjects with high waist circumference. The proportion of individuals with high triglycerides rose above 60% in the top two UA quartiles. We explored the association of various MS components with UA quartiles by gender. There were 402 women with a mean UA concentration of 4.9±0.6 mg/dL who had less than three MS components, and 275 women with a mean UA level of 5.1±0.08 mg/dL presenting more than three components (p=0.09). In men, 313 individuals with a mean UA of 5.9±0.8 mg/dL had less than three MS components, while 125 subjects with a mean UA of 6.3±0.13 mg/dL had more than three components (p=0.008) (data not shown in table III).

We evaluated the association between UA quartile, MS risk (three or more components) and sweetened beverage intake by means of logistic regression (table IV). In model 1 adjusting for age and gender, we found a 62% increased risk for the highest quartile. In model 2, after also adjusting for smoking and schooling, the associations between uric acid quartiles and MS did not change significantly. When entering eGFR (model 3), MS risk was increased at the 3^rd UA quartile (OR=1.48; 95% CI 1.02-2.14, p< 0.036), and the 4th quartile (OR=2.03; 95% CI 1.37-3.00, p<0.001). Finally, when adding sweetened beverage intake (model 4), the association between MS and UA remained statistically significant (p<0.002). However we did not demonstrated an additional effect, moreover the p value decreased, remaining statistically significant.

Discussion

The biochemical pathway linking fructose metabolism to UA is known. Fructose phosphorylation by fructokinase depletes intracellular ATP, thereby pushing both UA synthesis (via inosine-monophosphate) and triglyceride formation (via glycerol-3-phosphate).²² Experimental evidence in laboratory animals and humans has confirmed that excessive fructose ingestion raises UA levels inducing features of metabolic syndrome.^23,24

The prevalence of HU was found to be 26.5% (95%CI, 22.7-30.8) in men and 19.8% (95%CI, 17-23) in women. Although others have reported a relatively high prevalence of HU in the Mexican population, we find higher rates as compared with other estimates. This might be due to age structure differences of the study population, ours being older (62.8±7.7 years).^25,26 Alarmingly, in a small sample of medical students, 17 to 23 years old, the prevalence of HU was 19.8%.²⁷ Similar figures are seen in other countries: In 1 661 Brazilian individuals (25-64 years old), prevalence of HU was of 13.2% (95%CI, 11.4-15%), statistically higher in men 16% (95%CI, 14-18%) than women 10.7% (95%CI, 9-12%).²⁸ In a subsample of approximately 9 000 US adults a 18.9% prevalence of HU has been found.²⁹

Most HU cases were undiagnosed; consequently, few were under medical treatment. Since the majority of participants (98%) had healthcare access, lack of medical management suggests insufficient public and professional awareness. The previously reported high prevalence of the various components of the MS, as well as its consequences,³⁰ makes undiagnosed HU a significant finding. In fact, HU likely enhances risk for chronic kidney disease (CKD)³¹ in a population already with a high prevalence of nephropathy, as implicated by the frequent occurrence of microalbuminuria.^32-34

Overall, MS (at least three MS components) was present in one third of our cohort, with most of MS components (BMI, WC and triglycerides) increasing in frequency across increasing UA quartiles. The association between UA and the MS components in our population is so consistent, as to suggest HU as an additional component of MS, contributing along with disglycemia, hypertension, and dislipidemia³⁵ and even other nephrotoxic agents such as lead³⁶ to both cardiovascular and renal damage. Perhaps a more robust public health intervention to prevent CKD and atherosclerotic cardiovascular disease in México, could be to deal with this cluster of conditions in a comprehensive approach.

The reduction in glycemia and A1C levels across the uric acid quartiles parallels the reduction in renal function, as estimated by creatinine and eGFR. These are related phenomena since it is known that the kidney plays an important role in insulin metabolism and a diminution in renal capability is also a reduction in insulin metabolism resulting in higher insulin effect, which is reflected in decrements in glycemia and glycohemoglobin values. This is a cohort effect, since the participants in this phase of the MCDS are older adults.

In our population, sweetened beverage intake is high.³⁷ We found that its consumption increases across UA quartiles, suggesting at least a possible role in the differences seen in the prevalence of HU. Our results support findings of a recent study³⁸ demonstrating the association of sweetened beverage intake with the prevalence of HU and CKD.³⁹

We recognize several limitations in our study; namely: The diet assessment was obtained at baseline only, without taking into account possible modifications during follow-up. The estimate of sweetened beverage intake was done using a FFQ. We did not include HDL as part of the metabolic syndrome because it was not measured in this follow up. A potential cohort effect might explain the high prevalence of diabetes, hypertension and dyslipidemia in our population. However, our findings coincide with others and likely reflect a growing health problem in Mexico.

The Mexico City Diabetes Study grants support : RO1HL 24799 from the National Heart, Lung and Blood Institute, USA; Consejo Nacional de Ciencia y Tecnología (2092, M9303, F677-M9407, 251M & 2005-C01- 14502, SALUD 2010-2-151165).

References

1. Gagliardi AC, Miname MH, Santos RD. Uric acid: A marker of increased cardiovascular risk. Atherosclerosis 2009; 202:11-17.         [ Links ]

2. Rho YH, Zhu Y, Choi HK. The epidemiology of uric acid and fructose. Semin Nephrol 2011;31:410-419.         [ Links ]

3. Rivera JA, Muñoz-Hernández O, Rosas-Peralta M, Aguilar-Salinas CA, Popkin BM, Willett WC. [Beverage consumption for a healthy life: recommendations for the Mexican population]. Salud Publica Mex 2008;50:173-195.         [ Links ]

4. Quiñones-Galván A, Natali A, Baldi S, Frascerra S, Sanna G, Ciociaro D, et al. Effect of insulin on uric acid excretion in humans. Am J Physiol 1995;268: E1-5.         [ Links ]

5. Muscelli E, Natali A, Bianchi S, Bigazzi R, Galvan AQ, Sironi AM, et al. Effect of insulin on renal sodium and uric acid handling in essential hypertension. Am J Hypertens 1996;9:746-752.         [ Links ]

6. Perez-Pozo SE, Schold J, Nakagawa T, Sánchez-Lozada LG, Johnson RJ, Lillo JL. Excessive fructose intake induces the features of metabolic syndrome in healthy adult men: role of uric acid in the hypertensive response. Int J Obes 2010;34:454-461.         [ Links ]

7. Marquez-Sandoval F, Macedo-Ojeda G, Viramontes-Horner D, Fernández Ballart JD, Salas- Salvadó J, et al. The prevalence of metabolic syndrome in Latin America: a systematic review. Public Health Nutr 2011;14:1702-1713.         [ Links ]

8. Barquera S, Campos-Nonato I, Hernández-Barrera L, Flores M, Durazo-Arvizu R, Kanter R, et al. Obesity and central adiposity in Mexican adults: results from the Mexican National Health and Nutrition Survey 2006. Salud Publica Mex 2009;51 (Suppl 4):S595-603.         [ Links ]

9. Aguilar-Salinas CA, Gómez-Pérez FJ, Rull J, Villalpando S, Barquera S, Rojas R. Prevalence of dyslipidemias in the Mexican National Health and Nutrition Survey 2006. Salud Publica Mex 2010; 52 (Suppl 1): S44-53.         [ Links ]

10. Ventura EE, Davis JN, Goran MI. Sugar content of popular sweetened beverages based on objective laboratory analysis: focus on fructose content. Obesity 2011;19:868-874.         [ Links ]

11. Encuesta Nacional de Ingresos y Gastos de los Hogares 2004. ENIGH. La Estructura, Distribución y Monto de los Ingresos de los Hogares 2004.[monografia en internet] Aguascalientes, Ags. Instituto Nacional de Estadística Geografía e Informática [consultado 2013 junio 4] Disponible en: http://www.inegi.gob.mx/prod.../encuestas/hogares/enigh/2004/enigh_2004.pdf        [ Links ]

12. Stern MP, González-Villalpando C, Mitchell BD, Villalpando E, Haffner SM, Hazuda HP. Genetic and environmental determinants of type II diabetes in Mexico City and San Antonio. Diabetes 1992; 41: 484-492.         [ Links ]

13. Hunt KJ, González ME, Lopez R Haffner SM, Stern MP, González-Villalpando C. Diabetes is more lethal in Mexicans and Mexican-Americans compared to Non-Hispanic whites. Ann Epidemiol 2011; 21:899-906.         [ Links ]

14. Haffner S, González-Villalpando C, Hazuda H, Valdez R, Mykkänen L, Stern M. Prevalence of hypertension in Mexico City and San Antonio,Texas. Circulation 1994;90:1542-1549.         [ Links ]

15. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL , et al. Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 2003;42:1206-1252.         [ Links ]

16. Hernández-Avila M, Romieu I, Parra S, Hernández-Avila J, Madrigal H, Willett W. Validity and reproducibility of a food frequency questionnaire to assess dietary intake of women living in Mexico City. Salud Publica Mex 1998;40:133-140.         [ Links ]

17. Stern MP, González-Villalpando C, Hernández M, Knapp JA, Hazuda HP, Villalpando E, et al. Performance of semiquantitative food frequency questionnaires in international comparisons. Mexico City versus San Antonio, Texas. Ann Epidemiol 1993;3:300-307.         [ Links ]

18. Millen BE, Quatromoni PA, Pencina M, Kimokoti R, Nam BH, Cobain S, et al. Unique dietary patterns and chronic disease risk profiles of adult men: The Framingham Nutrition Studies. J Am Diet Assoc 2005;105:1723-1734.         [ Links ]

19. Oeltgen PR, Welborn JR, Burgess MS. Evaluation of the Abbott Spectrum "High-Performance" Diagnostic System. Clin Chem 1988;34:180-181.         [ Links ]

20. Zhu Y, Pandya BJ, Choi HK. Prevalence of gout and hyperuricemia in the US general population: the National Health and Nutrition Examination Survey 2007-2008. Arthritis Rheum 2011; 63: 3136-3141.         [ Links ]

21. Alberti KG, Zimmet P, Shaw J , IDF Epidemiology Task Force Consensus Group. The metabolic syndrome--a new worldwide definition. Lancet 2005;366:1059-1062.         [ Links ]

22. Lanaspa MA, Tapia E, Soto V, Sautin Y, Sánchez-Lozada LG. Uric acid and fructose: potential biological mechanisms. Semin Nephrol 2011;31:426-432.         [ Links ]

23. Johnson RJ, Perez-Pozo SE, Sautin YY, Manitius J, Sanchez-Lozada LG, Feig DI, et al. Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocr Rev 2009;30:96-116.         [ Links ]

24. Teff KL, Grudziak J, Townsend RR, Dunn TN, Grant RW, Adams SH, et al. Endocrine and metabolic effects of consuming fructose- and glucose-sweetened beverages with meals in obese men and women: Influence of insulin resistance on plasma triglyceride responses. J Clin Endocrinol Metab 2009;94:1562-1569.         [ Links ]

25. González-Chávez A, Elizondo-Argueta S, Amancio-Chassin O. Relación entre síndrome metabólico e hiperuricemia en población aparentemente sana. Rev Med Hosp Gen Mex 2011; 74:132-137.         [ Links ]

26. Reyes-Jiménez AE, Navarro J, Cruz IM, Castro DLJ, Landgrave GJ, Narváez PC, et al. Prevalencia del síndrome metabólico en relación con las concentraciones de ácido úrico. Med Int Mex 2009;25:278-284.         [ Links ]

27. Llamazares-Azuara L, Rodríguez-Martínez M, De la Cruz-Mendoza E, Torres Ruvalcaba A, Flores-Sánchez J. Prevalencia de hiperuricemia, resistencia a la insulina, obesidad y dislipidemias en jovenes de 17 a 23 años. Bioquimia 2007;32:134.         [ Links ]

28. Rodrigues SL, Baldo MP, Capingana P, Magalhães P, Dantas EM, Molina M del C, et al. Gender distribution of serum uric acid and cardiovascular risk factors: population based study. Arq Bras Cardiol 2012; 98: 13-21.         [ Links ]

29. Choi HK, Ford ES. Prevalence of the metabolic syndrome in individuals with hyperuricemia. Am J Med 2007;120:442-447.         [ Links ]

30. Aguilar-Salinas CA, Rojas R, Gómez-Pérez FJ, Valles V, Ríos-Torres JM, Franco A, et al. High prevalence of metabolic syndrome in Mexico. Arch Med Res 2004;35: 76-81.         [ Links ]

31. Wen CP, David-Cheng TY, Chan HT, Tsai MK, Chung WS, Tsai SP, et al. Is high serum uric acid a risk marker or a target for treatment ? Examination of its independent effect in a large cohort with low cardiovascular risk. Am J Kidney Dis 2010;56:273-288.         [ Links ]

32. Obrador GT, Garcia-Garcia G, Villa AR, Rubilar X, Olvera N, Ferreira E, et al. Prevalence of chronic kidney disease in the Kidney Early Evaluation Program (KEEP) Mexico and comparison with KEEP US. Kidney Int Suppl 2010;116:S2-S8        [ Links ]

33. Haffner SM, González-Villalpando C, Valdez RA, Mykkänen L, Hazuda HP, Mitchell BD, et al. Is microalbuminuria part of the prediabetic state ? The Mexico City Diabetes Study. Diabetologia 1993;36:1002-1006.         [ Links ]

34. Jimenez-Corona A, Rivera-Martinez D, Hernandez-Avila M, Haffner S, Williams K, González-Villalpando ME, et al. Microalbuminuria as a predictor of myocardial infarction in a Mexican population: The Mexico City Diabetes Study. Kidney Int Suppl 2005;97:S34-S39.         [ Links ]

35. González-Villalpando C, Stern MP, González-Villalpando ME, Rivera MD, Simón J, Islas S, et al. The Mexico City Diabetes Study: A population based approach to the study genetic and environmental interactions in the pathogenesis of obesity and diabetes. Nutrition Reviews 1999;57:S71-S77.         [ Links ]

36. Hernández Avila M, González-Villalpando C, Palazuelos E, Hu H, González-Villalpando ME, Rivera Martínez D. Determinants of blood lead levels across the menopausal transition. Arch Environ Health 2000;55:355-360.         [ Links ]

37. Jiménez-Aguilar A, Flores M, Shamah-Levy T. Sugar-sweetened beverages consumption and BMI in Mexican adolescents: Mexican National Health and Nutrition Survey 2006. Salud Publica Mex 2009; 51 (Suppl 4):S604-612.         [ Links ]

38. Bomback ASI, Derebail VK, Shoham DA, Anderson CA, Steffen LM, Rosamond WD, et al. Sugar-sweetened soda consumption, hyperuricemia, and kidney disease. Kidney Int 2010;77:609-616.         [ Links ]

39. Cheng HT, Huang JW, Chiang CH, Yen CH, Hung KY, Wu KD. Metabolic syndrome and insulin resistance as risk factors for development of chronic kidney disease and rapid decline in renal function in elderly. J Clin Endocrinol Metab 2012;97:1268-1276.         [ Links ]

Received on: February 22, 2013
Accepted on: July 1, 2013

Corresponding author:
Dr. Clicerio González-Villalpando.
Unidad de Investigación en Diabetes y Riesgo Cardiovascular,
Instituto Nacional de Salud Pública. Sur 136 # 116-309, 01120 México DF.
E-mail: cliceriogonzalez@hotmail.com