Maternal undernutrition and cardiometabolic disease: a latin american perspective

BMC Medicine

Jose Lopez-Lopez¹  Daniel Mantilla-Garcia¹  Aristides Sotomayor-Rubio¹  Diego Gomez-Arbelaez³  Patricio Lopez-Jaramillo² 

[1] Escuela de Medicina, Universidad Autónoma de Bucaramanga – UNAB, Bucaramanga, Colombia;Instituto de Investigaciones MASIRA, Universidad de Santander – UDES, Bucaramanga, Colombia;Departamento de Endocrinología, Escuela de Medicina, Universidad de Santiago de Compostela - España, Santiago de Compostela, La Coruña, Spain

关键词: Developing countries;    Latin America;    Socio-economic inequalities;    Low-birth weight;    Maternal undernutrition;    Cardiovascular diseases;    Obesity;   

Others  :  1134633
DOI  :  10.1186/s12916-015-0293-8

 received in 2014-10-01, accepted in 2015-02-12,  发布年份 2015

【 摘 要 】

The current epidemic of obesity and cardiometabolic diseases in developing countries is described as being driven by socioeconomic inequalities. These populations have a greater vulnerability to cardiometabolic diseases due to the discrepancy between the maternal undernutrition and its consequence, low-birth weight progeny, and the subsequent modern lifestyles which are associated with socioeconomic and environmental changes that modify dietary habits, discourage physical activity and encourage sedentary behaviors. Maternal undernutrition can generate epigenetic modifications, with potential long-term consequences. Throughout life, people are faced with the challenge of adapting to changes in their environment, such as excessive intake of high energy density foods and sedentary behavior. However, a mismatch between conditions experienced during fetal programming and current environmental conditions will make adaptation difficult for them, and will increase their susceptibility to obesity and cardiovascular diseases. It is important to conduct research in the Latin American context, in order to define the best strategies to prevent the epidemic of cardiometabolic diseases in the region.

【 授权许可】

   
2015 Lopez-Jaramillo et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Kelly T, Yang W, Chen CS, Reynolds K, He J: Global burden of obesity in 2005 and projections to 2030. Int J Obes (Lond) 2008, 32:1431-1437.
• [2]Cuevas A, Alvarez V, Carrasco F: Epidemic of metabolic syndrome in Latin America. Curr Opin Endocrinol Diabetes Obes 2011, 18:134-138.
• [3]Cuevas A, Alvarez V, Olivos C: The emerging obesity problem in Latin America. Expert Rev Cardiovasc Ther 2009, 7:281-288.
• [4]Rueda-Clausen CF, Silva FA, López-Jaramillo P: Epidemic of overweight and obesity in Latin America and the Caribbean. Int J Cardiol 2008, 125:111-112.
• [5]Lopez-Jaramillo P, Lahera V, Lopez-Lopez J: Epidemic of cardiometabolic diseases: a Latin American point of view. Ther Adv Cardiovasc Dis 2011, 5:119-131.
• [6]Uauy R, Albala C, Kain J: Obesity trends in Latin America: transiting from under- to overweight. J Nutr 2001, 131:893S-899S.
• [7]Lear SA, Teo K, Gasevic D, Zhang X, Poirier PP, Rangarajan S, et al.: The association between ownership of common household devices and obesity and diabetes in high, middle and low income countries. CMAJ 2014, 186:258-266.
• [8]Gómez-Arbeláez D, Camacho PA, Cohen DD, Rincón-Romero K, Alvarado-Jurado L, Pinzón S, et al.: Higher household income and the availability of electronic devices and transport at home are associated with higher waist circumference in Colombian children: the ACFIES study. Int J Environ Res Public Health 2014, 11:1834-1843.
• [9]Barría RM, Amigo H: Nutrition transition: a review of Latin American profile. Arch Latinoam Nutr 2006, 56:3-11.
• [10]López-Jaramillo P: Cardiometabolic disease in Latin America: the role of fetal programming in response to maternal malnutrition. Rev Esp Cardiol (Engl Ed) 2009, 62:670-676.
• [11]Negrato CA, Gomes MB: Low birth weight: causes and consequences. Diabetol Metab Syndr 2013, 5:49.
• [12]Lopez-Jaramillo P: Defining the research priorities to fight the burden of cardiovascular diseases in Latin America. J Hypertens 2008, 26:1886-1889.
• [13]López-Jaramillo P, Silva SY, Rodríguez-Salamanca N, Duran A, Mosquera W, Castillo V: Are nutrition-induced epigenetic changes the link between socioeconomic pathology and cardiovascular diseases? Am J Ther 2008, 15:362-372.
• [14]Gallou-Kabani C, Junien C: Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes 2005, 54:1899-1906.
• [15]López-Jaramillo P, Rey JJ, Gómez-Arbeláez D, Rodríguez YA, López-López J: Combating the type 2 diabetes mellitus epidemic in Latin America: special features demanding innovative actions. Clin Investig Arterioscler 2011, 23:90-99.
• [16]Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, et al.: National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2 · 7 million participants. Lancet 2011, 378:31-40.
• [17]King H, Aubert RE, Herman WH: Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care 1998, 21:1414-1431.
• [18]Pérez CM, Guzmán M, Ortiz AP, Estrella M, Valle Y, Pérez N, et al.: Prevalence of the metabolic syndrome in San Juan, Puerto Rico. Ethn Dis 2008, 18:434-441.
• [19]Medina-Lezama J, Zea-Diaz H, Morey-Vargas OL, Bolaños-Salazar JF, Muñoz-Atahualpa E, Postigo-MacDowall M, et al.: Prevalence of the metabolic syndrome in Peruvian Andean hispanics: the PREVENCION study. Diabetes Res Clin Pract 2007, 78:270-281.
• [20]Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, et al.: National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9 · 1 million participants. Lancet 2011, 377:557-567.
• [21]Ford ES, Giles WH, Dietz WH: Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 2002, 287:356-359.
• [22]López-Jaramillo P, Rueda-Clausen CF, Silva FA: The utility of different definitions of metabolic syndrome in Andean population. Int J Cardiol 2007, 116:421-2.
• [23]Valenzuela AA, Maíz A, Margozzini P, Ferreccio C, Rigotti A, Olea R, et al.: Prevalence of metabolic syndrome among Chilean adults. Rev Med Chil 2010, 138:707-714.
• [24]Villalpando S, Shamah-Levy T, Rojas R, Aguilar-Salinas CA: Trends for type 2 diabetes and other cardiovascular risk factors in Mexico from 1993–2006. Salud Publica Mex 2010, 52:72-79.
• [25]Rojas R, Aguilar-Salinas CA, Jiménez-Corona A, Shamah-Levy T, Rauda J, Avila-Burgos L, et al.: Metabolic syndrome in Mexican adults: results from the National Health and Nutrition Survey 2006. Salud Publica Mex 2010, 52:11-18.
• [26]Florez H, Silva E, Fernández V, Ryder E, Sulbarán T, Campos G, et al.: Prevalence and risk factors associated with the metabolic syndrome and dyslipidemia in White, Black, Amerindian and Mixed Hispanics in Zulia State, Venezuela. Diabetes Res Clin Pract 2005, 69:63-77.
• [27]Sempértegui F, Estrella B, Tucker KL, Hamer DH, Narvaez X, Sempértegui M, et al.: Metabolic syndrome in the elderly living in marginal peri-urban communities in Quito, Ecuador. Public Health Nutr 2011, 14:758-767.
• [28]Rodrigues SL, Baldo MP, Mill JG: Association of waist-stature ratio with hypertension and metabolic syndrome: population-based study. Arq Bras Cardiol 2010, 95:186-191.
• [29]Caceres M, Teran CG, Rodriguez S, Medina M: Prevalence of insulin resistance and its association with metabolic syndrome criteria among Bolivian children and adolescents with obesity. BMC Pediatr 2008, 8:31.
• [30]Bustos P, Saez K, Gleisner A, Ulloa N, Calvo C, Asenjo S: Metabolic syndrome in obese adolescents. Pediatr Diabetes 2010, 11:55-60.
• [31]Cohen DD, Gómez-Arbeláez D, Camacho PA, Pinzon S, Hormiga C, Trejos-Suarez J, et al.: Low muscle strength is associated with metabolic risk factors in Colombian children: the ACFIES study. PLoS One 2014, 9:e93150.
• [32]Chow CK, Teo KK, Rangarajan S, Islam S, Gupta R, Avezum A, et al.: Prevalence, awareness, treatment, and control of hypertension in rural and urban communities in high-, middle-, and low-income countries. JAMA 2013, 310:959-968.
• [33]Yusuf S, Islam S, Chow CK, Rangarajan S, Dagenais G, Diaz R, et al.: Teo KK; Prospective Urban Rural Epidemiology (PURE) Study Investigators: Use of secondary prevention drugs for cardiovascular disease in the community in high-income, middle-income, and low-income countries (the PURE Study): a prospective epidemiological survey. Lancet 2011, 378:1231-1243.
• [34]Teo K, Lear S, Islam S, Mony P, Dehghan M, Li W, et al.: Pure Investigators: Prevalence of a healthy lifestyle among individuals with cardiovascular disease in high-, middle- and low-income countries: The Prospective Urban Rural Epidemiology (PURE) study. JAMA 2013, 309:1613-1621.
• [35]Arredondo A, Zuñiga A: Epidemiological changes and financial consequences of hypertension in Latin America: implications for the health system and patients in Mexico. Cad Saude Publica 2012, 28:497-502.
• [36]Hossain P, Kawar B, El Nahas M: Obesity and diabetes in the developing world–a growing challenge. N Engl J Med 2007, 356:213-215.
• [37]López-Jaramillo P, Sánchez RA, Diaz M, Cobos L, Bryce A, Parra Carrillo JZ, et al.: Latin American consensus on hypertension in patients with diabetes type 2 and metabolic syndrome. J Hypertens 2013, 31:223-238.
• [38]Lopez-Jaramillo P, Molina DI: The 20 × 20 Latin American Society of Hypertension target. J Hypertens 2015, 33:189-190.
• [39]Henikoff S, Matzke MA: Exploring and explaining epigenetic effects. Trends Genet 1997, 13:293-295.
• [40]Attig L, Gabory A, Junien C: Early nutrition and epigenetic programming: chasing shadows. Curr Opin Clin Nutr Metab Care 2010, 13:284-93.
• [41]Probst AV, Dunleavy E, Almouzni G: Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 2009, 10:192-206.
• [42]Bestor TH, Chandler VL, Feinberg AP: Epigenetic effects in eukaryotic gene expression. Dev Genet 1994, 15:458-462.
• [43]Ling C, Groop L: Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 2009, 58:2718-2725.
• [44]Gabory A, Attig L, Junien C: Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 2009, 304:8-18.
• [45]VerMilyea MD, O’Neill LP, Turner BM: Transcription-independent heritability of induced histone modifications in the mouse preimplantation embryo. PLoS One 2009, 4:e6086.
• [46]Attig L, Gabory A, Junien C: Nutritional developmental epigenomics: immediate and long-lasting effects. Proc Nutr Soc 2010, 69:221-231.
• [47]Weaver IC: Shaping adult phenotypes through early life environments. Birth Defects Res C Embryo Today 2009, 87:314-326.
• [48]Karemaker R, Karemaker JM, Kavelaars A, Tersteeg-Kamperman M, Baerts W, Veen S, et al.: Effects of neonatal dexamethasone treatment on the cardiovascular stress response of children at school age. Pediatrics 2008, 122:978-987.
• [49]Barrès R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, et al.: Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009, 10:189-198.
• [50]Plagemann A, Harder T, Brunn M, Harder A, Roepke K, Wittrock-Staar M, et al.: Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome. J Physiol 2009, 587:4963-4976.
• [51]Plagemann A, Roepke K, Harder T, Brunn M, Harder A, Wittrock-Staar M, et al.: Epigenetic malprogramming of the insulin receptor promoter due to developmental overfeeding. J Perinat Med 2010, 38:393-400.
• [52]Godfrey KM, Gluckman PD, Hanson MA: Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab 2010, 21:199-205.
• [53]Burdge GC, Lillycrop KA: Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr 2010, 30:315-339.
• [54]Cooney CA: Germ cells carry the epigenetic benefits of grandmother’s diet. Proc Natl Acad Sci U S A 2006, 103:17071-17072.
• [55]Aguilera O, Fernández AF, Muñoz A, Fraga MF: Epigenetics and environment: a complex relationship. J Appl Physiol (1985) 2010, 109:243-251.
• [56]Youngson NA, Whitelaw E: Transgenerational epigenetic effects. Annu Rev Genomics Hum Genet 2008, 9:233-257.
• [57]Gallou-Kabani C, Vigé A, Gross MS, Junien C: Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond. Clin Chem Lab Med 2007, 45:321-327.
• [58]Gluckman PD, Hanson MA, Cooper C, Thornburg KL: Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008, 359:61-73.
• [59]Burdge GC, Lillycrop KA, Jackson AA: Nutrition in early life, and risk of cancer and metabolic disease: alternative endings in an epigenetic tale? Br J Nutr 2009, 101:619-630.
• [60]Anway MD, Cupp AS, Uzumcu M, Skinner MK: Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
• [61]Anway MD, Skinner MK: Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 2006, 147:43-49.
• [62]Jirtle RL, Skinner MK: Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007, 8:253-262.
• [63]Barker DJ, Martyn CN: The maternal and fetal origins of cardiovascular disease. J Epidemiol Community Health 1992, 46:8-11.
• [64]Jackson AA, Burdge GC, Lillycrop KA: Diet, nutrition and modulation of genomic expression in fetal origins of adult disease. World Rev Nutr Diet 2010, 101:56-72.
• [65]Chmurzynska A: Fetal programming: link between early nutrition, DNA methylation, and complex diseases. Nutr Rev 2010, 68:87-98.
• [66]SzarcvelSzic K, Ndlovu MN, Haegeman G, VandenBerghe W: Nature or nurture: let food be your epigenetic medicine in chronic inflammatory disorders. Biochem Pharmacol 2010, 80:1816-1832.
• [67]American Association for Cancer Research Human Epigenome Task Force; European Union, Network of Excellence, Scientific Advisory Board: Moving AHEAD with an international human epigenome project Nature 2008, 454:711-715.
• [68]De Assis S, Hilakivi-Clarke L: Timing of dietary estrogenic exposures and breast cancer risk. Ann N Y Acad Sci 2006, 1089:14-35.
• [69]Guerrero-Bosagna CM, Sabat P, Valdovinos FS, Valladares LE, Clark SJ: Epigenetic and phenotypic changes result from a continuous pre and post natal dietary exposure to phytoestrogens in an experimental population of mice. BMC Physiol 2008, 8:17.
• [70]Hunter P: We are what we eat. The link between diet, evolution and non-genetic inheritance. EMBO Rep 2008, 9:413-415.
• [71]Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ: Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008, 115:1243-1249.
• [72]Lumey LH, Stein AD: Transgenerational effects of prenatal exposure to the Dutch famine. BJOG 2009, 116:868.
• [73]Roseboom T, de Rooij S, Painter R: The Dutch famine and its long-term consequences for adult health. Early Hum Dev 2006, 82:485-491.
• [74]Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, et al.: DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA 2007, 104:19351-19356.
• [75]Kwong WY, Miller DJ, Ursell E, Wild AE, Wilkins AP, Osmond C, et al.: Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction 2006, 132:265-277.
• [76]Kwong WY, Miller DJ, Wilkins AP, Dear MS, Wright JN, Osmond C, et al.: Maternal low protein diet restricted to the preimplantation period induces a gender-specific change on hepatic gene expression in rat fetuses. Mol Reprod Dev 2007, 74:48-56.
• [77]Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, et al.: DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 2009, 18:3769-3778.
• [78]Pinney SE, Simmons RA: Epigenetic mechanisms in the development of type 2 diabetes. Trends Endocrinol Metab 2010, 21:223-229.
• [79]Raychaudhuri N, Raychaudhuri S, Thamotharan M, Devaskar SU: Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J Biol Chem 2008, 283:13611-13626.
• [80]Levent E, Atik T, Darcan S, Ulger Z, Gökşen D, Ozyürek AR: The relation of arterial stiffness with intrauterine growth retardation. Pediatr Int 2009, 51:807-811.
• [81]Martyn CN, Barker DJ, Jespersen S, Greenwald S, Osmond C, Berry C: Growth in utero, adult blood pressure, and arterial compliance. Br Heart J 1995, 73:116-121.
• [82]Liew G, Wang JJ, Duncan BB, Klein R, Sharrett AR, Brancati F, et al.: Low birthweight is associated with narrower arterioles in adults. Hypertension 2008, 51:933-938.
• [83]Martin H, Gazelius B, Norman M: Impaired acetylcholine-induced vascular relaxation in low birth weight infants: implications for adult hypertension? Pediatr Res 2000, 47:457-462.
• [84]Szostak-Wegierek D: Intrauterine nutrition: long-term consequences for vascular health. Int J Womens Health 2014, 6:647-656.
• [85]Wang T, Liu C, Feng C, Wang X, Lin G, Zhu Y, et al.: IUGR alters muscle fiber development and proteome in fetal pigs. Front Biosci (Landmark Ed) 2013, 18:598-607.
• [86]Lopez-Jaramillo P, Cohen DD, Gómez-Arbeláez D, Bosch J, Dyal L, Yusuf S, et al.: Association of handgrip strength to cardiovascular mortality in pre-diabetic and diabetic patients: a subanalysis of the ORIGIN trial. Int J Cardiol 2014, 174:458-461.
• [87]McConnell JM, Petrie L: Mitochondrial DNA turnover occurs during preimplantation development and can be modulated by environmental factors. Reprod Biomed Online 2004, 9:418-424.
• [88]Petrie L, Duthie SJ, Rees WD, McConnell JM: Serum concentrations of homocysteine are elevated during early pregnancy in rodent models of fetal programming. Br J Nutr 2002, 88:471-477.
• [89]Thompson JG, Gardner DK, Pugh PA, McMillan WH, Tervit HR: Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol Reprod 1995, 53:1385-1391.
• [90]Ecker DJ, Stein P, Xu Z, Williams CJ, Kopf GS, Bilker WB, et al.: Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci U S A 2004, 101:1595-1600.
• [91]Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP: Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 2000, 127:4195-4202.
• [92]Ashworth CJ, Toma LM, Hunter MG: Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B Biol Sci 2009, 364:3351-3361.
• [93]Snoeck A, Remacle C, Reusens B, Hoet JJ: Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 1990, 57:107-118.
• [94]Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ: Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 1991, 40:115-120.
• [95]Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al.: Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991, 303:1019-1022.
• [96]Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM: Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993, 36:62-67.
• [97]Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al.: Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005, 102:10604-10609.
• [98]Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, et al.: Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 2009, 5:e1000602.
• [99]Wierda RJ, Geutskens SB, Jukema JW, Quax PH, van den Elsen PJ: Epigenetics in atherosclerosis and inflammation. J Cell Mol Med 2010, 14:1225-1240.
• [100]Lund G, Zaina S: Epigenetics, transgenerational effects and risk factors for atherosclerosis. Curr Opin Lipidol 2009, 20:150-151.
• [101]Lund G, Zaina S: Atherosclerosis risk factors can impose aberrant DNA methylation patterns: a tale of traffic and homocysteine. Curr Opin Lipidol 2009, 20:448-449.
• [102]Waldo SW, Li Y, Buono C, Zhao B, Billings EM, Chang J, et al.: Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol 2008, 172:1112-1126.
• [103]Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, et al.: Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2006, 113:898-918.
• [104]Rueda-Clausen CF, Lahera V, Calderón J, Bolivar IC, Castillo VR, Gutiérrez M, et al.: The presence of abdominal obesity is associated with changes in vascular function independently of other cardiovascular risk factors. Int J Cardiol 2010, 139:32-41.
• [105]Yusuf S, Hawken S, Ounpuu S, Bautista L, Franzosi MG, Commerford P, et al.: Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case–control study. Lancet 2005, 366:1640-1649.
• [106]O’Donnell MJ, Xavier D, Liu L, Zhang H, Chin SL, Rao-Melacini P, et al.: Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case–control study. Lancet 2010, 376:112-123.
• [107]Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, et al.: The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 2010, 56:1113-1132.
• [108]Aschner P, Ruiz A, Balkau B, Massien C, Haffner SM: Latin America and the Caribbean International Day for Evaluation of Abdominal Adiposity (IDEA) National Coordinators and Investigators: Association of abdominal adiposity with diabetes and cardiovascular disease in Latin America. J Clin Hypertens (Greenwich) 2009, 11:769-774.
• [109]Gregory CO, Corvalán C, Ramirez-Zea M, Martorell R, Stein AD: Detection of cardio-metabolic risk by BMI and waist circumference among a population of Guatemalan adults. Public Health Nutr 2008, 11:1037-1045.
• [110]Katulanda P, Jayawardena MA, Sheriff MH, Matthews DR: Derivation of anthropometric cut-off levels to define CVD risk in Sri Lankan adults. Br J Nutr 2011, 105:1084-1090.
• [111]Perez M, Casas JP, Cubillos-Garzón LA, Serrano NC, Silva F, Morillo CA, et al.: Using waist circumference as a screening tool to identify Colombian subjects at cardiovascular risk. Eur J Cardiovasc Prev Rehabil 2003, 10:328-335.
• [112]Garcia RG, Cifuentes AE, Caballero RS, Sanchez L, López-Jaramillo P: A proposal for an appropriate central obesity diagnosis in Latin American population. Int J Cardiol 2006, 110:263-264.
• [113]Tchernof A, Després JP: Pathophysiology of human visceral obesity: an update. Physiol Rev 2013, 93:359-404.
• [114]Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW: Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 2004, 145:2273-2282.
• [115]Ahima RS, Flier JS: Adipose tissue as an endocrine organ. Trends Endocrinol Metab 2000, 11:327-332.
• [116]Fried SK, Bunkin DA, Greenberg AS: Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab 1998, 83:847-850.
• [117]López-Jaramillo P, Pradilla LP, Castillo VR, Lahera V: Socioeconomic pathology as a cause of regional differences in the prevalence of metabolic syndrome and pregnancy-induced hypertension. Rev Esp Cardiol 2007, 60:168-178.
• [118]López-Jaramillo P, Casas JP, Morillo CA: C-reactive protein and cardiovascular diseases in Andean population. Circulation 2002, 105:E10.
• [119]Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S: Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 2007, 56:1010-1013.
• [120]Accini JL, Sotomayor A, Trujillo F, Barrera JG, Bautista L, López-Jaramillo P: Colombian study to assess the use of noninvasive determination of endothelium-mediated vasodilatation (CANDEV). Normal values and factors associated. Endothelium 2001, 8:157-166.
• [121]Ross R: Atherosclerosis–an inflammatory disease. N Engl J Med 1999, 340:115-126.
• [122]Gómez-Arbeláez D, López-Jaramillo P: Mechanisms of acute coronary syndromes. N Engl J Med 2013, 369:882.
• [123]Bogaty P, Poirier P, Simard S, Boyer L, Solymoss S, Dagenais GR: Biological profiles in subjects with recurrent acute coronary events compared with subjects with long-standing stable angina. Circulation 2001, 103:3062-3068.
• [124]Bautista LE, López-Jaramillo P, Vera LM, Casas JP, Otero AP, Guaracao AI: Is C-reactive protein an independent risk factor for essential hypertension? J Hypertens 2001, 19:857-861.
• [125]Teran E, Escudero C, Moya W, Flores M, Vallance P, Lopez-Jaramillo P: Elevated C-reactive protein and pro-inflammatory cytokines in Andean women with pre-eclampsia. Int J Gynaecol Obstet 2001, 75:243-249.
• [126]García RG, Celedón J, Sierra-Laguado J, Alarcón MA, Luengas C, Silva F, et al.: Raised C-reactive protein and impaired flow-mediated vasodilation precede the development of preeclampsia. Am J Hypertens 2007, 20:98-103.
• [127]Garcia RG, Perez M, Maas R, Schwedhelm E, Böger RH, López-Jaramillo P: Plasma concentrations of asymmetric dimethylarginine (ADMA) in metabolic syndrome. Int J Cardiol 2007, 122:176-178.
• [128]López-Jaramillo P, Herrera E, Garcia RG, Camacho PA, Castillo VR: Inter-relationships between body mass index, C-reactive protein and blood pressure in a Hispanic pediatric population. Am J Hypertens 2008, 21:527-532.
• [129]López-Jaramillo P, Gómez-Arbeláez D, López-López J, López-López C, Martínez-Ortega J, Gómez-Rodríguez A, et al.: The role of leptin/adiponectin ratio in metabolic syndrome and diabetes. Horm Mol Biol Clin Investig 2014, 18:37-45.
• [130]Medzhitov R, Horng T: Transcriptional control of the inflammatory response. Nat Rev Immunol 2009, 9:692-703.
• [131]Pasparakis M: Regulation of tissue homeostasis by NF-kappa B signalling: implications for inflammatory diseases. Nat Rev Immunol 2009, 9:778-788.
• [132]Ghosh S, Hayden MS: New regulators of NF-kappa B in inflammation. Nat Rev Immunol 2008, 8:837-848.
• [133]Karin M, Greten FR: NF-kappa B: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005, 5:749-759.
• [134]Chen LF, Greene WC: Shaping the nuclear action of NF-kappa B. Nat Rev Mol Cell Biol 2004, 5:392-401.
• [135]Grivennikov SI, Karin M: Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 2010, 20:65-71.
• [136]Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, et al.: Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010, 140:197-208.
• [137]Olefsky JM: IKK epsilon: a bridge between obesity and inflammation. Cell 2009, 138:834-836.
• [138]Hotamisligil GS: Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
• [139]Mandl J, Mészáros T, Bánhegyi G, Hunyady L, Csala M: Endoplasmic reticulum: nutrient sensor in physiology and pathology. Trends Endocrinol Metab 2009, 20:194-201.
• [140]Karin M: Nuclear factor-kappa B in cancer development and progression. Nature 2006, 441:431-436.
• [141]Perkins ND: Integrating cell-signalling pathways with NF-kappa B and IKK function. Nat Rev Mol Cell Biol 2007, 8:49-62.
• [142]Nakanishi C, Toi M: Nuclear factor-kappa B inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005, 5:297-309.
• [143]Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, et al.: IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005, 11:191-198.
• [144]Tennant DA, Durán RV, Gottlieb E: Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010, 10:267-277.
• [145]De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G: The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 2007, 130:1083-1094.
• [146]Ghisletti S, Barozzi I, Mietton F, Polletti S, De Santa F, Venturini E, et al.: Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 2010, 32:317-328.
• [147]Ghisletti S, Huang W, Ogawa S, Pascual G, Lin ME, Willson TM, et al.: Parallel sumoylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARgamma. Mol Cell 2007, 25:57-70.
• [148]Xu J, Watts JA, Pope SD, Gadue P, Kamps M, Plath K, et al.: Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cells. Genes Dev 2009, 23:2824-2838.
• [149]Natoli G, Saccani S, Bosisio D, Marazzi I: Interactions of NF-kappa B with chromatin: the art of being at the right place at the right time. Nat Immunol 2005, 6:439-445.
• [150]Hager GL, McNally JG, Misteli T: Transcription dynamics. Mol Cell 2009, 35:741-753.
• [151]Sung MH, Salvatore L, De Lorenzi R, Indrawan A, Pasparakis M, Hager GL, et al.: Sustained oscillations of NF-kappa B produce distinct genome scanning and gene expression profiles. PLoS One 2009, 4:e7163.
• [152]Delage B, Dashwood RH: Dietary manipulation of histone structure and function. Annu Rev Nutr 2008, 28:347-366.
• [153]Link A, Balaguer F, Goel A: Cancer chemoprevention by dietary polyphenols: promising role for epigenetics. Biochem Pharmacol 2010, 80:1771-1792.
• [154]Hauser AT, Jung M: Targeting epigenetic mechanisms: potential of natural products in cancer chemoprevention. Planta Med 2008, 74:1593-1601.
• [155]Kirk H, Cefalu WT, Ribnicky D, Liu Z, Eilertsen KJ: Botanicals as epigenetic modulators for mechanisms contributing to development of metabolic syndrome. Metabolism 2008, 57:16-23.
• [156]Fang M, Chen D, Yang CS: Dietary polyphenols may affect DNA methylation. J Nutr 2007, 137:223-228.
• [157]Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, et al.: A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 2009, 138:114-128.
• [158]VandenBerghe W, Ndlovu MN, Hoya-Arias R, Dijsselbloem N, Gerlo S, Haegeman G: Keeping up NF-kappa B appearances: epigenetic control of immunity or inflammation-triggered epigenetics. Biochem Pharmacol 2006, 72:1114-1131.
• [159]O’Dea E, Hoffmann A: The regulatory logic of the NF-kappa B signaling system. Cold Spring Harb Perspect Biol 2010, 2:a000216.
• [160]Hayden MS, Ghosh S: Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
• [161]Natoli G, De Santa F: Shaping alternative NF-kappaB-dependent gene expression programs: new clues to specificity. Cell Death Differ 2006, 13:693-696.
• [162]Ford E, Thanos D: The transcriptional code of human IFN-beta gene expression. Biochim Biophys Acta 2010, 1799:328-336.