http://informahealthcare.com/pgm ISSN: 0032-5481 (print), 1941-9260 (electronic) Postgrad Med, 2015; 127(5): 503–510 DOI: 10.1080/00325481.2015.1021234
CLINICAL FOCUS: DIABETES REVIEW
Hispanic Americans living in the United States and their risk for obesity, diabetes and kidney disease: Genetic and environmental considerations
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Joseph M. Yracheta*1, Javier Alfonso*2, Miguel A. Lanaspa2,3, Carlos Roncal-Jimenez2,3, Sarah B Johnson2, Laura G. Sánchez-Lozada3,4 and Richard J. Johnson 2,3 1
Department of Pharmaceutics, School of Pharmacy, University of Washington, Seattle, WA, USA, 2Division of Renal Diseases and Hypertension, University of Colorado, Aurora, CO, USA, 3Colorado Research Partners LLC, Aurora, CO, USA, and 4Laboratory of Renal Physiopathology and Department of Nephrology, INC Ignacio Chavez, Mexico City, Mexico Abstract
Keywords
The Hispanic American, the largest minority population in the United States, is at increased risk for obesity, diabetes and end-stage renal disease. Here we review genetic and environmental factors that might account for their increased risk for these conditions. Whereas many environmental and genetic factors have important roles in driving the increased risk for obesity and kidney disease in this population, a case is made that excessive intake of sugary beverages is a contributory cause. Studies focusing on decreasing intake of sugary beverages among the Hispanic American could potentially reduce renal and cardiovascular complications in this population.
Hispanic American, diabetes, obesity, metabolic syndrome, chronic kidney disease, health disparities, sugar, fructose
Hispanic Americans are an ethnicity defined as Americans of Mexican, Cuban, Puerto Rican, Central American, or Southern American culture or origin. Hispanic Americans constitute the largest minority (16%) in the United States and are projected to account for one in three Americans by 2050 [1-4]. Hispanic Americans have some of the highest prevalence rates of obesity and diabetes in the United States, as well as increased frequency of chronic kidney disease (CKD), but interestingly have less coronary artery disease events and cardiovascular mortality [5-7]. Regional diversity is also present among Hispanic Americans based on origins (Cuban, Mexican, Puerto Rican, etc.) or environment that can lead to some variation in the frequency of diabetes and cardiovascular diseases [7-9]. Here we review the metabolic and cardiorenal status of the Hispanic American and discuss potential environmental and genetic mechanisms to account for these findings, with a special emphasis on the role of sugar intake.
Increased prevalence of obesity and diabetes yet lower prevalence of cardiovascular disease: The Hispanic paradox The Hispanic American is currently at increased risk for obesity and metabolic syndrome compared to non-Hispanic
History Received 11 November 2014 Accepted 17 February 2015 Published online 7 March 2015
Whites (Table 1) [5,6,10-14]. Obesity is especially prevalent in female Hispanic Americans with 44% obese compared to 32% in non-Hispanic Whites. This is accompanied by an increased prevalence rate for metabolic syndrome [13], fatty liver [14], and diabetes [10]. Obesity and diabetes are common in Hispanic Americans in adolescence [14,15], with type 2 diabetes occurring four times more in Hispanic American adolescents compared to non-Hispanic Whites [16]. Diabetes is almost twice as common (12%) in adults as compared to the non-Hispanic White (7%), and is especially common in Mexican Americans where it occurs at an earlier age than in non-Hispanic Whites [15]. Interestingly, Cuban Americans have a lower frequency of diabetes compared to Mexican or Puerto Rican Americans [17]. Despite the higher prevalence of obesity and metabolic syndrome, the prevalence of hypertension tends to be equivalent or slightly lower to that observed in the non-Hispanic White [18-20]. An exception is the Caribbean Hispanic, who has a greater prevalence of hypertension [21,22], possibly related to the greater African heritage compared to Mexican Americans [23]. Despite similar rates of hypertension, the incidence of stroke is greater in the Hispanic Americans, especially in those under the age of 60 [24]. Nevertheless, stroke mortality is lower in Hispanic Americans (although these differences do not appear in some regions) [25,26].
Correspondence: Richard J Johnson, MD, Division of Renal Diseases and Hypertension, University of Colorado, 12700 East 19th Ave, Room 7015, Aurora, CO 80045, USA. E-mail: [email protected] *These authors contributed equally to this work. 2015 Informa UK Ltd.
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Table 1. Increased obesity, diabetes and CKD in the Hispanic American.
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Obesity prevalence, males (BMI > 30, ‡ 18 yrs), (2007–2010) Obesity prevalence, females (BMI > 30, ‡ 18 yrs), (2007–2010 Metabolic syndrome IDF criteria, men, age > 20, adjusteda Metabolic syndrome, IDF criteria, women, age > 20 yrsa Metabolic syndrome, NCEP criteria, men, age > 20, adjusteda Metabolic syndrome, NCEP criteria, women, age > 20 yrsa Nonalcoholic fatty liver disease (Dallas Heart Study) Diabetes prevalence, (‡ 18 yrs), 2010 Hypertension prevalence, (‡ 18 yrs), 2007–2010 % of Hypertensive subjects with BP controlled (age adjusted) Chronic kidney disease (Stages 1 to 5, NHANES, 1999–2004)a Heart failure prevalence, 2008, (%)
ESRD, Incidence, 2001, cases/million ESRD, Incidence, 2011, cases/million Coronary artery disease and strokes, deaths/100k, 2009 Stroke, deaths/100k in 2006 CAD deaths/100k in 2006
Hispanic (%)
Non-Hispanic White (%)
Ref.
35 44 51 46 40 44 45 12 28 34 19 2
33 32 42 34 35 32 33 7 29 53 16 3
[10] [10] [13] [13] [13] [13] [14] [10] [10] [10] [6] [11]
Hispanic (Rate)
Non-Hispanic White (Rate)
Ref.
600 536 86 34 106
283 286 118 44 137
[5] [5] [10] [12] [12]
a
Mexican Americans. Abbreviations: BMI = Body mass index; BP = Blood pressure; CAD = Coronary artery disease; CKD = Chronic kidney disease; ESRD = End-stage renal disease; IDF = International Diabetes Federation; NCEP = National Cholesterol Education Program; NHANES = National Health and Nutrition Examination Survey.
Furthermore, the incidence of cardiovascular events (myocardial infarction) and prevalence of heart failure, as well as cardiovascular mortality, are lower in the Hispanic American compared to the non-Hispanic White (Table 1) [10,27,28]. The observation that certain risk factors such as obesity and diabetes are more common, yet cardiovascular events and mortality are lower, has been called the Hispanic Paradox [29-32]. To date no environmental factors have been identified that can adequately explain this paradox [32]. Interestingly, a similar pattern is evident among Native Americans [33,34], suggesting that this may be due to Native American genetic polymorphisms that may have carried over to this subgroup of Hispanic Americans. Hypertension also appears to be less prevalent than would be expected based on the increased frequency of obesity and metabolic syndrome, but overall stroke prevalence is higher among Mexican Americans compared to non-Hispanic Whites [35]. This may relate to the relatively poor health care of the Hispanic American and the fact that only one-third of Hispanic Americans with hypertension have their blood pressure adequately controlled (Table 1) [10]. An exception may be the Caribbean Hispanic American, who has a greater black heritage and also has a higher prevalence of hypertension than other Hispanic American groups [36]. Hypertension is much more frequent in the African American than other groups in the United States, and likely has genetic origins. It is known, for example, that early studies of the Bantu documented high prevalence of hypertension and kidney disease [37-39]. CKD may also be increased in the Hispanic American compared to non-Hispanic Whites, although there remains some controversy, especially related to Hispanic American subgroups [2]. CKD is especially common among the Hispanic poor [40]. Hispanic Americans with CKD have higher rates of self-reported diabetes, a higher prevalence of
hypertension, less use of drugs that inhibit the renin angiotensin system, and lower mean eGFR than non-Hispanic Whites or African Americans with CKD [41]. This likely accounts for the consistent finding that both diabetics and nondiabetic Hispanic Americans with CKD show a more rapid progression to end-stage renal disease (ESRD) than non-Hispanic Whites, despite a lower risk for cardiovascular events and mortality [31,42].
Environmental and genetic factors driving obesity and diabetes Obesity, metabolic syndrome, fatty liver and diabetes are commonly observed together and can be considered a cluster of signs with a common underlying pathway [43-45]. One of the central underlying pathophysiological pathways that link these disorders is the development of insulin resistance [46,47]. The observation that many animals store fat by increasing fat in the adipose tissue, liver and serum coupled with the development of insulin resistance suggests it is a physiological mechanism for fat storage that eventually breaks down, resulting in type 2 diabetes [45]. Hence, grouping these conditions together may be useful from the standpoint of understanding etiology. Environmental factors that may contribute to the increased frequency of obesity and metabolic syndrome in the Hispanic American The Hispanic American falls into a disadvantaged minority that suffers from many environmental factors that could contribute to the increased frequency of obesity. These include a lower socioeconomic status with higher rates of poverty, lower rates of education, less overall diet quality, higher rates of sedentary activity, community effects that include not only
Hispanic American and obesity
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Table 2. Demographic and behavioral characteristics of Hispanic Americans and non-Hispanic Whites. Hispanic (%) Social/economic Did not complete high school (‡ 25 yrs), 2011a Poverty level (‡ 18 yrs), 2011a Unemployed (age 18–64), 2011a No health insurance, (age 18–64), 2010a Preterm births (%), 2010a Habits Smoking, age ‡ 18 yrs, 2009–2010a Self-reported alcohol use, moderate or heavy (2004–2008)b Heavy (> 1 drink/d) soft drinks, 2005 (NYC data)c Percent calories from soft drinks, age ‡ 20, 2005–2008d ‡ 25% Total intake from added sugars (NHANES 2005–2008)e
505
Non-Hispanic White (%)
38 16 12 41 12
7 12 8 16 11
23 13 49 8 12
26 23 18 5 9
Data obtained from aCenters for Disease Control Health Disparities and Inequalities Report – United States, 2013 [10]. From the National Health Statistics Report (2004–2008) [51]. c From the 2005 New York City Community Health Survey [52]. d From the Centers for Disease Control and Prevention National Center for Health Statistics (2005–2008) [53]. e From the National Health and Nutrition Examination Survey (NHANES, 2005–2008) [54].
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b
socioeconomic factors and education, but also access to physical features such as parks and recreational facilities (the “built environment”) [48-50]. In addition, inadequate health coverage, language barriers with the health care community, different social mores, a relative lack of Hispanic American physicians, and health care provider bias may also impair health care delivery that may lead to health care disparities (Table 2) [10,51-54]. Many of these environmental factors, such as low socioeconomic status and poor education, are thought to influence obesity by increasing the likelihood for sedentary behavior and intake of diets of poor quality [48]. However, during the early twentieth century the risk for obesity and diabetes was the highest among the rich and educated, with the reversal of this pattern occurring in the mid-twentieth century [55]. Thus, there has been a socioeconomic reversal in the relationship of obesity and diabetes in the last century. One potential mechanism could be changing dietary habits, such as an increased intake in poor-quality foods among the poor, such as higher intake of fast foods, and foods high in fat or sugar [56,57]. Of these, intake of added sugars (sucrose and high fructose corn syrup) has recently emerged as a major risk factor for accounting not only for this paradox but also for the increased frequency of obesity and diabetes in Hispanic Americans today. Intake of added sugars as a mechanism to account for the socioeconomic risk factor reversal and the risk for obesity and diabetes Emerson was one of the first to show a strong epidemiological linkage of sugar intake with the development of diabetes [58]. In his seminal work performed in the early 1920s, he found that it was the wealthy and more educated population in New York City that were at risk for diabetes, and he linked this with the intake of sugar, which was less affordable to the poor at that time in history [58]. Over the last century sugar became less expensive, and today intake is greatest among the poor and less educated [56]. Today 25% of Americans are drinking more than one soft drink per day, and 5% are drinking more than four 12-ounce beverages [53]. In turn, multiple studies have confirmed that intake of sugar-
sweetened beverages is strongly associated with the development of obesity and diabetes [59-61]. Hispanic Americans ingest almost twice the percent daily calories from soft drinks compared to non-Hispanic Whites [53]. In a study performed in New York City, the intake of at least one soft drink per day was observed in almost half (49%) of Hispanic Americans and was nearly three times greater than that observed in non-Hispanic Whites; intake also correlated with physical inactivity and BMI in women (Table 2) [52]. Furthermore, intake of soft drinks is the highest in Hispanic Americans who are poor [52,56]; similarly diabetes is also more common among Hispanic Americans who are poor [15,62]. Intake of sugar and soft drinks has also been associated with beta islet cell dysfunction in adolescent Hispanic Americans [63]. One might argue that focusing on added sugars ignores the role of other dietary components that may also influence the risk for obesity, including the role of saturated and trans fats, a low intake in dairy products, high glycemic carbohydrates, and the intake of fast foods. Indeed, the role of these other types of foods should not be discounted. Nevertheless, there are reasons sugar comes to the top of the list as a risk factor for obesity and diabetes in the Hispanic American. First, between 1982–1984 and 1999–2006 the rate of obesity and diabetes increased significantly in the Hispanic American, yet during the same time the intake of total fat, saturated fat and protein decreased whereas that of carbohydrates (including sugar) increased [64]. The increased frequency of obesity and diabetes occurred despite falling levels of poverty and increasing levels of education [64]. Second, a study of Hispanic women attending a prenatal clinic showed that the risk for having an infant with obesity was markedly enhanced if the mother ingested more than two soft drinks per week (4.7-fold) or had at least two sweets per week (11-fold) during pregnancy, whereas no relationship was observed with intake of saturated fat, fast foods, fruits, vegetables, alcohol or exercise [65]. Another study reported that 3-year old Hispanic children had higher intakes of sugar-sweetened beverages, fast food, and lower dairy (1% milk or skim milk) and saturated fat intake compared to non-Hispanic Whites, suggesting that intake of saturated fats cannot explain the increased risk for
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Fructose metabolism Fructose Fat, glucose ATP depletion Uric acid
Systemic effects
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↓ No and vasoconstriction decreased adiponectin insulin resistance
Renal effects
Decreased fat oxidation increased lipogenesis increased glucose production
↑ Oxidative stress inflammation vasoconstriction glomerular hypertension direct tubular effects
Chronic kidney disease
Type 2 diabetes fatty liver obesity
Figure 1. Mechanism for how fructose may cause insulin resistance and kidney disease.
obesity in this population [66]. Importantly, however, there is evidence that Hispanic Americans are ingesting lower amounts of dietary omega-3 polyunsaturated fatty acids, which have been shown to provide some cardioprotective benefits [67]. Scientific studies suggest that added sugars may increase the risk of diabetes and obesity due to both the fructose content (present in both sucrose and the sweetener, high fructose corn syrup) and the high glycemic content [68-70]. Experimental studies document that the fructose is not simply a caloric source, but activates a side-chain reaction (the AMP deaminase-uric acid-mitochondrial oxidative stress pathway) that results in gluconeogenesis, an increase in fat synthesis, and a decrease in fat oxidation (Figure 1) [71-73]. Fructose also stimulates leptin resistance in animals leading to overnutrition, resulting in excessive energy intake and a decrease in energy expenditure [74,75]. Sucrose and fructose intake in animals can also induce islet dysfunction [76,77]. Thus, although the importance of socioeconomic and cultural factors cannot be discounted, there is increasing evidence that added sugars, such as high fructose corn syrup and sucrose, may be important factors driving the increased risk for obesity and metabolic syndrome in the Hispanic American. Role of genetic mechanisms in obesity and diabetes Although sugar intake and poor food selection may lead to overnutrition and metabolic syndrome, genetic mechanisms are also contributory and may involve environmental–genetic interactions [78]. The genetic profile of the Hispanic American is heterogeneous, with conventional wisdom assuming that Caribbean Hispanic Americans have a higher frequency of African American genetic polymorphisms and MexicanAmericans and Central and South Americans having a higher Native American ancestry [23,79]. Although this general trend holds, recent studies have identified some unexpected patterns of tri-racial admixture and gender biased admixture in several Latin American populations [9]. Among different
Hispanic subgroups, Puerto Rican have a more balanced triracial group (African American, non-Hispanic White, and Hispanic), Mexicans are skewed toward Native American ancestry whereas Cuban Hispanics are skewed toward European ancestry [9]. Thus, the genetics of the Hispanic peoples may be difficult to interpret based on reported studies given the diversity in underlying populations. Despite these concerns, studies of Mexican Americans have identified several genetic polymorphisms associated with obesity (FTO [80,81]), diabetes (ENPP1 [82,83], SLC16A11 [84] and TMPRSS6 [85]), fatty liver (PNPLA3) [86], and eGFR (Loci 20q11 [87]). Although the Hispanic American has a marked increased frequency of nonalcoholic fatty liver, the frequency in the Cuban Hispanic is less, likely because of higher admixture with African American genes (particularly polymorphisms in PNPLA3), which are associated with lower frequencies of hepatic steatosis [88,89]. Epigenetic mechanisms may also play a role in the increased frequency of obesity and diabetes. Although the original focus was on the effects of low birth weight on later adult life (fetal programming), differences in the frequency of premature births are relatively minor between Hispanic Americans and non-Hispanic Whites (Table 2). More recently emphasis has been placed on the relationships of diets rich in sugars and fat during pregnancy [90,91] and/or of maternal obesity itself on the future development of obesity and diabetes in the progeny, including potential effects of diet on the gut microbiome [92].
CKD in the Hispanic American The increased incidence of ESRD in Hispanic Americans relates in part to the higher frequency of diabetes in this population compared to non-Hispanic Whites [93], and is significantly less than that observed in African Americans and Hawaiians/Pacific Islanders (Figure 2). One study showed that Cuban Americans had higher serum creatinine levels
Hispanic American and obesity
DOI: 10.1080/00325481.2015.1021234
Incidence of ESRD, 2011 (USRDS)
Frequency per million
2500
2368
1500
452
517
280
0
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White
African Native Hispanic American American American
1.0 1.7 (1.1–2.6) 4.6 (2.5–8.3)
Shown is the odds ratio (OR) for CKD, defined as an estimated creatinine clearance < 60 mL/min/1.73 m2. The OR was adjusted for demographic, clinical, and socioeconomic factors (including known predictors of chronic kidney disease). From [94]. Abbreviation: CKD = Chronic kidney disease.
940
1000
500
Table 3. Rates of chronic kidney disease in Hispanic Americans based on the Hispanic Health and Nutrition Examination Survey (HHANES). Hispanic subgroup OR (adjusted) Mexican American Puerto Ricans Cuban Americans
2000
507
Pacific lslander
Figure 2. Age- and sex-adjusted incidence of ESRD, 2011 [5]. Abbreviation: ESRD = End-stage renal disease.
than Puerto Rican Americans or Mexican Americans across gender and age with an odd ratio of 4.6 (2.5–8.3) predicting CKD [94]. The higher prevalence rate of CKD in the African Americans has been shown to be due in part to the presence of specific polymorphisms in the apolipoprotein L1 (APOL1) gene, and similar linkage has been found in Hispanic Americans who may have as much as 20 to 30% of their genes of African ancestry [95,96]. If one looks at CKD rates in different subgroups of Hispanics, the rate of CKD is highest in Cuban Americans and Puerto Ricans compared to Mexican Americans (Table 3) [94]. Further studies such as the Hispanic Chronic Renal Insufficiency Cohort study should provide a better assessment [97]. This is especially important as it may be possible in the future to target treatments aimed at the APOL1 polymorphisms that increase the risk for kidney disease [98]. These discrepancies across Hispanic subgroups may point to the environmental mechanisms that play a role in the CKD. Sugar-sweetened beverage intake, for example, is associated with increased risk for kidney disease in some [99,100] but not all studies [99], and administration of fructose to laboratory animals can cause tubular injury and accelerate CKD (Figure 1) [101,102]. In addition, recent studies have identified a potential role for heat and dehydration in inducing CKD in animals [103], raising the possibility that manual labor in hot environments such as the South may also emerge as a risk factor, similar to what has been shown in Thailand, Nicaragua, and Sri Lanka [104,105].
control of hypertension and diabetes, the expression of the APOL1 polymorphisms in certain individuals, and from environmental factors including unhealthy diets rich in sugar and hot climate predisposing to dehydration. The physician needs to be cognizant of the challenges in taking care of the Hispanic American, especially the challenges related to their higher frequency of poor health care coverage, language and sociocultural barriers, and health care provider bias. Interventions need to involve coordinated efforts to educate healthy food selection (including inclusion of healthy traditional foods), to increase physical activity, to provide counseling, and to improve community access to parks and recreational facilities. Using such approaches, some success has been achieved [106]. In addition, reducing intake of added sugars should also be of benefit, with a goal to limiting it to 10% of overall energy intake [107]. Reversing the epidemics of obesity, diabetes and hypertension will require a multipronged approach that includes education on healthy diets and hydration, improving health care delivery, treatment adherence, and programs to help prevent obesity.
Declaration of interest R Johnson, CA Roncal-Jimenez, MA Lanaspa and LG Sánchez-Lozada hold shares in Colorado Research Partners, who are trying to develop fructose inhibitors. R Johnson and MA Lanaspa are listed as inventors on patent applications for the University of Colorado. R Johnson is also on the scientific board for Amway and holds stock in XORT. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.
References Recommendations for the health care practitioner In summary, the Hispanic American has characteristics similar to the Native American in having a higher prevalence of obesity, diabetes and CKD compared to non-Hispanic Whites, while having a lower risk for cardiovascular events and mortality. Both genetic and epigenetic factors contribute to the increased risk for diabetes and obesity. Environmental factors, especially the intake of sugar-sweetened beverages, are also important. The increased prevalence of CKD also results in part from the increased frequency of diabetes, the poorer
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[55] Yusuf S, Reddy S, Ounpuu S, Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 2001;104:2746–53. [56] Thompson FE, McNeel TS, Dowling EC, et al. Interrelationships of added sugars intake, socioeconomic status, and race/ethnicity in adults in the United States: National Health Interview Survey, 2005. J Am Diet Assoc 2009;109:1376–83. [57] Bermudez OI, Tucker KL. Trends in dietary patterns of Latin American populations. Cad Saude Publica 2003;19:S87–99. [58] Emerson H, Larimore LD. Diabetes mellitus: a contribution to its epidemiology based chiefly on mortality statistics. Arch Intern Med 1924;34:585–630. [59] Malik VS, Pan A, Willett WC, Hu FB. Sugar-sweetened beverages and weight gain in children and adults: a systematic review and meta-analysis. Am J Clin Nutr 2013;98:1084–102. [60] Malik VS, Popkin BM, Bray GA, et al. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care 2010;33:2477–83. [61] Malik VS, Willett WC, Hu FB. Sugar-sweetened beverages and BMI in children and adolescents: reanalyses of a meta-analysis. Am J Clin Nutr 2009;89:438–9; author reply 9-40. [62] Zhang J, Markides KS, Lee DJ. Health status of diabetic Mexican Americans: results from the Hispanic HANES. Ethn Dis 1991;1:273–9. [63] Davis JN, Ventura EE, Weigensberg MJ, et al. The relation of sugar intake to beta cell function in overweight Latino children. Am J Clin Nutr 2005;82:1004–10. [64] Fryar CD, Wright JD, Eberhardt MS, Dye BA. Trends in nutrient intakes and chronic health conditions among MexicanAmerican adults, a 25-year profile: United States, 1982-2006. Natl Health Stat Report 2012;1–20. [65] Watt TT, Appel L, Roberts K, et al. Sugar, stress, and the Supplemental Nutrition Assistance Program: early childhood obesity risks among a clinic-based sample of low-income Hispanics. J Community Health 2013;38:513–20. [66] de Hoog ML, Kleinman KP, Gillman MW, et al. Racial/ethnic and immigrant differences in early childhood diet quality. Public Health Nutr 2014;17:1308–17. [67] de Oliveira Otto MC, Wu JH, Baylin A, et al. Circulating and dietary omega-3 and omega-6 polyunsaturated fatty acids and incidence of CVD in the Multi-Ethnic Study of Atherosclerosis. J Am Heart Assoc 2013;2:e000506. [68] Ishimoto T, Lanaspa MA, Le MT, et al. Opposing effects of fructokinase C and A isoforms on fructose-induced metabolic syndrome in mice. Proc Natl Acad Sci USA 2012;109:4320–5. [69] Lanaspa MA, Ishimoto T, Li N, et al. Endogenous fructose production and metabolism in the liver contributes to the development of metabolic syndrome. Nat Commun 2013;4:2434. [70] Ludwig DS. The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 2002;287:2414–23. [71] Lanaspa MA, Cicerchi C, Garcia G, et al. Counteracting roles of AMP deaminase and AMP kinase in the development of fatty liver. PLoS One 2012;7:e48801. [72] Lanaspa MA, Sanchez-Lozada LG, Choi YJ, et al. Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem 2012;287:40732–44. [73] Cicerchi C, Li N, Kratzer J, et al. Uric acid-dependent inhibition of AMP kinase induces hepatic glucose production in diabetes and starvation: evolutionary implications of the uricase loss in hominids. FASEB J 2014;28:3339–50. [74] Shapiro A, Mu W, Roncal C, et al. Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high-fat feeding. Am J Physiol Regul Integr Comp Physiol 2008;295: R1370–5. [75] Shapiro A, Tumer N, Gao Y, et al. Prevention and reversal of diet-induced leptin resistance with a sugar-free diet despite high fat content. Br J Nutr 2011;106:390–7. [76] Roncal-Jimenez CA, Lanaspa MA, Rivard CJ, et al. Sucrose induces fatty liver and pancreatic inflammation in male breeder rats independent of excess energy intake. Metabolism 2011;60:1259–70.
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[77] Cummings BP, Stanhope KL, Graham JL, et al. Dietary fructose accelerates the development of diabetes in UCD-T2DM rats: amelioration by the antioxidant, alpha-lipoic acid. Am J Physiol Regul Integr Comp Physiol 2010;298:R1343–50. [78] Fowler SP, Puppala S, Arya R, et al. Genetic epidemiology of cardiometabolic risk factors and their clustering patterns in Mexican American children and adolescents: the SAFARI Study. Hum Genet 2013;132:1059–71. [79] Moreno-Estrada A, Gignoux CR, Fernandez-Lopez JC, et al. Human genetics. The genetics of Mexico recapitulates Native American substructure and affects biomedical traits. Science 2014;344:1280–5. [80] Leon-Mimila P, Villamil-Ramirez H, Villalobos-Comparan M, et al. Contribution of common genetic variants to obesity and obesity-related traits in mexican children and adults. PLoS One 2013;8:e70640. [81] Wing MR, Ziegler JM, Langefeld CD, et al. Analysis of FTO gene variants with obesity and glucose homeostasis measures in the multiethnic Insulin Resistance Atherosclerosis Study cohort. Int J Obes 2011;35:1173–82. [82] Jenkinson CP, Coletta DK, Flechtner-Mors M, et al. Association of genetic variation in ENPP1 with obesity-related phenotypes. Obesity (Silver Spring) 2008;16:1708–13. [83] Moore AF, Jablonski KA, Mason CC, et al. The association of ENPP1 K121Q with diabetes incidence is abolished by lifestyle modification in the diabetes prevention program. J Clin Endocrinol Metab 2009;94:449–55. [84] Williams AL, Jacobs SB, Moreno-Macias H, et al. Sequence variants in SLC16A11 are a common risk factor for type 2 diabetes in Mexico. Nature 2014;506:97–101. [85] Grimsby JL, Porneala BC, Vassy JL, et al. Race-ethnic differences in the association of genetic loci with HbA1c levels and mortality in U.S. adults: the third National Health and Nutrition Examination Survey (NHANES III). BMC Med Genet 2012;13:30. [86] Davis JN, Le KA, Walker RW, et al. Increased hepatic fat in overweight Hispanic youth influenced by interaction between genetic variation in PNPLA3 and high dietary carbohydrate and sugar consumption. Am J Clin Nutr 2010;92:1522–7. [87] Thameem F, Igo RP Jr, Freedman BI, et al. A genome-wide search for linkage of estimated glomerular filtration rate (eGFR) in the Family Investigation of Nephropathy and Diabetes (FIND). PLoS One 2013;8:e81888. [88] Kallwitz ER, Daviglus ML, Allison MA, et al. Prevalence of suspected nonalcoholic Fatty liver disease in hispanic/latino individuals differs by heritage. Clin Gastroenterol Hepatol 2015;13:569–76. [89] Palmer ND, Musani SK, Yerges-Armstrong LM, et al. Characterization of European ancestry nonalcoholic fatty liver diseaseassociated variants in individuals of African and Hispanic descent. Hepatology 2013;58:966–75. [90] Heerwagen MJ, Miller MR, Barbour LA, Friedman JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Physiol Regul Integr Comp Physiol 2010;299:R711– 22. [91] Kanaka-Gantenbein C. Fetal origins of adult diabetes. Ann N Y Acad Sci 2010;1205:99–105. [92] Tsai F, Coyle WJ. The microbiome and obesity: is obesity linked to our gut flora? Curr Gastroenterol Rep 2009;11:307–13. [93] Palmer Alves T, Lewis J. Racial differences in chronic kidney disease (CKD) and end-stage renal disease (ESRD) in the United States: a social and economic dilemma. Clin Nephrol 2010;74:S72–7. [94] Rodriguez RA, Hernandez GT, O’Hare AM, et al. Creatinine levels among Mexican Americans, Puerto Ricans, and Cuban Americans in the Hispanic Health and Nutrition Examination Survey. Kidney Int 2004;66:2368–73. [95] Behar DM, Rosset S, Tzur S, et al. African ancestry allelic variation at the MYH9 gene contributes to increased susceptibility to non-diabetic end-stage kidney disease in Hispanic Americans. Hum Mol Genet 2010;19:1816–27. [96] Tzur S, Rosset S, Skorecki K, Wasser WG. APOL1 allelic variants are associated with lower age of dialysis initiation and thereby increased dialysis vintage in African and Hispanic
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J. M. Yracheta et al. Americans with non-diabetic end-stage kidney disease. Nephrol Dial Transplant 2012;27:1498–505. Lora CM, Ricardo AC, Brecklin CS, et al. Recruitment of Hispanics into an observational study of chronic kidney disease: the Hispanic Chronic Renal Insufficiency Cohort Study experience. Contemp Clin Trials 2012;33:1238–44. Kruzel-Davila E, Wasser WG, Aviram S, Skorecki K. APOL1 nephropathy: from gene to mechanisms of kidney injury. Nephrol Dial Transplant 2015. [Epub ahead of print]. Shoham DA, Durazo-Arvizu R, Kramer H, et al. Sugary soda consumption and albuminuria: results from the National Health and Nutrition Examination Survey, 1999-2004. PLoS One 2008;3:e3431. Bomback AS, Derebail VK, Shoham DA, et al. Sugar-sweetened soda consumption, hyperuricemia, and kidney disease. Kidney Int 2010;77:609–16. Nakayama T, Kosugi T, Gersch M, et al. Dietary fructose causes tubulointerstitial injury in the normal rat kidney. Am J Physiol Renal Physiol 2010;298:F712–20.
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[102] Gersch MS, Mu W, Cirillo P, et al. Fructose, but not dextrose, accelerates the progression of chronic kidney disease. Am J Physiol Renal Physiol 2007;293:F1256–61. [103] Roncal Jimenez CA, Ishimoto T, Lanaspa MA, et al. Fructokinase activity mediates dehydration-induced renal injury. Kidney Int 2014;86:294–302. [104] Tawatsupa B, Lim LL, Kjellstrom T, et al. Association between occupational heat stress and kidney disease among 37,816 workers in the Thai Cohort Study (TCS). J Epidemiol 2012;22:251– 60. [105] Correa-Rotter R, Wesseling C, Johnson RJ. CKD of unknown origin in Central America: the case for a Mesoamerican nephropathy. Am J Kidney Dis 2014;63:506–20. [106] Ziebarth D, Healy-Haney N, Gnadt B, et al. A community-based family intervention program to improve obesity in Hispanic families. WMJ 2012;111:261–6. [107] Johnson RK, Appel LJ, Brands M, et al. Dietary sugars intake and cardiovascular health: a scientific statement from the American Heart Association. Circulation 2009;120:1011–20.
CLINICAL FOCUS: DIABETES REVIEW
Hispanic Americans living in the United States and their risk for obesity, diabetes and kidney disease: Genetic and environmental considerations
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Joseph M. Yracheta*1, Javier Alfonso*2, Miguel A. Lanaspa2,3, Carlos Roncal-Jimenez2,3, Sarah B Johnson2, Laura G. Sánchez-Lozada3,4 and Richard J. Johnson 2,3 1
Department of Pharmaceutics, School of Pharmacy, University of Washington, Seattle, WA, USA, 2Division of Renal Diseases and Hypertension, University of Colorado, Aurora, CO, USA, 3Colorado Research Partners LLC, Aurora, CO, USA, and 4Laboratory of Renal Physiopathology and Department of Nephrology, INC Ignacio Chavez, Mexico City, Mexico Abstract
Keywords
The Hispanic American, the largest minority population in the United States, is at increased risk for obesity, diabetes and end-stage renal disease. Here we review genetic and environmental factors that might account for their increased risk for these conditions. Whereas many environmental and genetic factors have important roles in driving the increased risk for obesity and kidney disease in this population, a case is made that excessive intake of sugary beverages is a contributory cause. Studies focusing on decreasing intake of sugary beverages among the Hispanic American could potentially reduce renal and cardiovascular complications in this population.
Hispanic American, diabetes, obesity, metabolic syndrome, chronic kidney disease, health disparities, sugar, fructose
Hispanic Americans are an ethnicity defined as Americans of Mexican, Cuban, Puerto Rican, Central American, or Southern American culture or origin. Hispanic Americans constitute the largest minority (16%) in the United States and are projected to account for one in three Americans by 2050 [1-4]. Hispanic Americans have some of the highest prevalence rates of obesity and diabetes in the United States, as well as increased frequency of chronic kidney disease (CKD), but interestingly have less coronary artery disease events and cardiovascular mortality [5-7]. Regional diversity is also present among Hispanic Americans based on origins (Cuban, Mexican, Puerto Rican, etc.) or environment that can lead to some variation in the frequency of diabetes and cardiovascular diseases [7-9]. Here we review the metabolic and cardiorenal status of the Hispanic American and discuss potential environmental and genetic mechanisms to account for these findings, with a special emphasis on the role of sugar intake.
Increased prevalence of obesity and diabetes yet lower prevalence of cardiovascular disease: The Hispanic paradox The Hispanic American is currently at increased risk for obesity and metabolic syndrome compared to non-Hispanic
History Received 11 November 2014 Accepted 17 February 2015 Published online 7 March 2015
Whites (Table 1) [5,6,10-14]. Obesity is especially prevalent in female Hispanic Americans with 44% obese compared to 32% in non-Hispanic Whites. This is accompanied by an increased prevalence rate for metabolic syndrome [13], fatty liver [14], and diabetes [10]. Obesity and diabetes are common in Hispanic Americans in adolescence [14,15], with type 2 diabetes occurring four times more in Hispanic American adolescents compared to non-Hispanic Whites [16]. Diabetes is almost twice as common (12%) in adults as compared to the non-Hispanic White (7%), and is especially common in Mexican Americans where it occurs at an earlier age than in non-Hispanic Whites [15]. Interestingly, Cuban Americans have a lower frequency of diabetes compared to Mexican or Puerto Rican Americans [17]. Despite the higher prevalence of obesity and metabolic syndrome, the prevalence of hypertension tends to be equivalent or slightly lower to that observed in the non-Hispanic White [18-20]. An exception is the Caribbean Hispanic, who has a greater prevalence of hypertension [21,22], possibly related to the greater African heritage compared to Mexican Americans [23]. Despite similar rates of hypertension, the incidence of stroke is greater in the Hispanic Americans, especially in those under the age of 60 [24]. Nevertheless, stroke mortality is lower in Hispanic Americans (although these differences do not appear in some regions) [25,26].
Correspondence: Richard J Johnson, MD, Division of Renal Diseases and Hypertension, University of Colorado, 12700 East 19th Ave, Room 7015, Aurora, CO 80045, USA. E-mail: [email protected] *These authors contributed equally to this work. 2015 Informa UK Ltd.
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Table 1. Increased obesity, diabetes and CKD in the Hispanic American.
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Obesity prevalence, males (BMI > 30, ‡ 18 yrs), (2007–2010) Obesity prevalence, females (BMI > 30, ‡ 18 yrs), (2007–2010 Metabolic syndrome IDF criteria, men, age > 20, adjusteda Metabolic syndrome, IDF criteria, women, age > 20 yrsa Metabolic syndrome, NCEP criteria, men, age > 20, adjusteda Metabolic syndrome, NCEP criteria, women, age > 20 yrsa Nonalcoholic fatty liver disease (Dallas Heart Study) Diabetes prevalence, (‡ 18 yrs), 2010 Hypertension prevalence, (‡ 18 yrs), 2007–2010 % of Hypertensive subjects with BP controlled (age adjusted) Chronic kidney disease (Stages 1 to 5, NHANES, 1999–2004)a Heart failure prevalence, 2008, (%)
ESRD, Incidence, 2001, cases/million ESRD, Incidence, 2011, cases/million Coronary artery disease and strokes, deaths/100k, 2009 Stroke, deaths/100k in 2006 CAD deaths/100k in 2006
Hispanic (%)
Non-Hispanic White (%)
Ref.
35 44 51 46 40 44 45 12 28 34 19 2
33 32 42 34 35 32 33 7 29 53 16 3
[10] [10] [13] [13] [13] [13] [14] [10] [10] [10] [6] [11]
Hispanic (Rate)
Non-Hispanic White (Rate)
Ref.
600 536 86 34 106
283 286 118 44 137
[5] [5] [10] [12] [12]
a
Mexican Americans. Abbreviations: BMI = Body mass index; BP = Blood pressure; CAD = Coronary artery disease; CKD = Chronic kidney disease; ESRD = End-stage renal disease; IDF = International Diabetes Federation; NCEP = National Cholesterol Education Program; NHANES = National Health and Nutrition Examination Survey.
Furthermore, the incidence of cardiovascular events (myocardial infarction) and prevalence of heart failure, as well as cardiovascular mortality, are lower in the Hispanic American compared to the non-Hispanic White (Table 1) [10,27,28]. The observation that certain risk factors such as obesity and diabetes are more common, yet cardiovascular events and mortality are lower, has been called the Hispanic Paradox [29-32]. To date no environmental factors have been identified that can adequately explain this paradox [32]. Interestingly, a similar pattern is evident among Native Americans [33,34], suggesting that this may be due to Native American genetic polymorphisms that may have carried over to this subgroup of Hispanic Americans. Hypertension also appears to be less prevalent than would be expected based on the increased frequency of obesity and metabolic syndrome, but overall stroke prevalence is higher among Mexican Americans compared to non-Hispanic Whites [35]. This may relate to the relatively poor health care of the Hispanic American and the fact that only one-third of Hispanic Americans with hypertension have their blood pressure adequately controlled (Table 1) [10]. An exception may be the Caribbean Hispanic American, who has a greater black heritage and also has a higher prevalence of hypertension than other Hispanic American groups [36]. Hypertension is much more frequent in the African American than other groups in the United States, and likely has genetic origins. It is known, for example, that early studies of the Bantu documented high prevalence of hypertension and kidney disease [37-39]. CKD may also be increased in the Hispanic American compared to non-Hispanic Whites, although there remains some controversy, especially related to Hispanic American subgroups [2]. CKD is especially common among the Hispanic poor [40]. Hispanic Americans with CKD have higher rates of self-reported diabetes, a higher prevalence of
hypertension, less use of drugs that inhibit the renin angiotensin system, and lower mean eGFR than non-Hispanic Whites or African Americans with CKD [41]. This likely accounts for the consistent finding that both diabetics and nondiabetic Hispanic Americans with CKD show a more rapid progression to end-stage renal disease (ESRD) than non-Hispanic Whites, despite a lower risk for cardiovascular events and mortality [31,42].
Environmental and genetic factors driving obesity and diabetes Obesity, metabolic syndrome, fatty liver and diabetes are commonly observed together and can be considered a cluster of signs with a common underlying pathway [43-45]. One of the central underlying pathophysiological pathways that link these disorders is the development of insulin resistance [46,47]. The observation that many animals store fat by increasing fat in the adipose tissue, liver and serum coupled with the development of insulin resistance suggests it is a physiological mechanism for fat storage that eventually breaks down, resulting in type 2 diabetes [45]. Hence, grouping these conditions together may be useful from the standpoint of understanding etiology. Environmental factors that may contribute to the increased frequency of obesity and metabolic syndrome in the Hispanic American The Hispanic American falls into a disadvantaged minority that suffers from many environmental factors that could contribute to the increased frequency of obesity. These include a lower socioeconomic status with higher rates of poverty, lower rates of education, less overall diet quality, higher rates of sedentary activity, community effects that include not only
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Table 2. Demographic and behavioral characteristics of Hispanic Americans and non-Hispanic Whites. Hispanic (%) Social/economic Did not complete high school (‡ 25 yrs), 2011a Poverty level (‡ 18 yrs), 2011a Unemployed (age 18–64), 2011a No health insurance, (age 18–64), 2010a Preterm births (%), 2010a Habits Smoking, age ‡ 18 yrs, 2009–2010a Self-reported alcohol use, moderate or heavy (2004–2008)b Heavy (> 1 drink/d) soft drinks, 2005 (NYC data)c Percent calories from soft drinks, age ‡ 20, 2005–2008d ‡ 25% Total intake from added sugars (NHANES 2005–2008)e
505
Non-Hispanic White (%)
38 16 12 41 12
7 12 8 16 11
23 13 49 8 12
26 23 18 5 9
Data obtained from aCenters for Disease Control Health Disparities and Inequalities Report – United States, 2013 [10]. From the National Health Statistics Report (2004–2008) [51]. c From the 2005 New York City Community Health Survey [52]. d From the Centers for Disease Control and Prevention National Center for Health Statistics (2005–2008) [53]. e From the National Health and Nutrition Examination Survey (NHANES, 2005–2008) [54].
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b
socioeconomic factors and education, but also access to physical features such as parks and recreational facilities (the “built environment”) [48-50]. In addition, inadequate health coverage, language barriers with the health care community, different social mores, a relative lack of Hispanic American physicians, and health care provider bias may also impair health care delivery that may lead to health care disparities (Table 2) [10,51-54]. Many of these environmental factors, such as low socioeconomic status and poor education, are thought to influence obesity by increasing the likelihood for sedentary behavior and intake of diets of poor quality [48]. However, during the early twentieth century the risk for obesity and diabetes was the highest among the rich and educated, with the reversal of this pattern occurring in the mid-twentieth century [55]. Thus, there has been a socioeconomic reversal in the relationship of obesity and diabetes in the last century. One potential mechanism could be changing dietary habits, such as an increased intake in poor-quality foods among the poor, such as higher intake of fast foods, and foods high in fat or sugar [56,57]. Of these, intake of added sugars (sucrose and high fructose corn syrup) has recently emerged as a major risk factor for accounting not only for this paradox but also for the increased frequency of obesity and diabetes in Hispanic Americans today. Intake of added sugars as a mechanism to account for the socioeconomic risk factor reversal and the risk for obesity and diabetes Emerson was one of the first to show a strong epidemiological linkage of sugar intake with the development of diabetes [58]. In his seminal work performed in the early 1920s, he found that it was the wealthy and more educated population in New York City that were at risk for diabetes, and he linked this with the intake of sugar, which was less affordable to the poor at that time in history [58]. Over the last century sugar became less expensive, and today intake is greatest among the poor and less educated [56]. Today 25% of Americans are drinking more than one soft drink per day, and 5% are drinking more than four 12-ounce beverages [53]. In turn, multiple studies have confirmed that intake of sugar-
sweetened beverages is strongly associated with the development of obesity and diabetes [59-61]. Hispanic Americans ingest almost twice the percent daily calories from soft drinks compared to non-Hispanic Whites [53]. In a study performed in New York City, the intake of at least one soft drink per day was observed in almost half (49%) of Hispanic Americans and was nearly three times greater than that observed in non-Hispanic Whites; intake also correlated with physical inactivity and BMI in women (Table 2) [52]. Furthermore, intake of soft drinks is the highest in Hispanic Americans who are poor [52,56]; similarly diabetes is also more common among Hispanic Americans who are poor [15,62]. Intake of sugar and soft drinks has also been associated with beta islet cell dysfunction in adolescent Hispanic Americans [63]. One might argue that focusing on added sugars ignores the role of other dietary components that may also influence the risk for obesity, including the role of saturated and trans fats, a low intake in dairy products, high glycemic carbohydrates, and the intake of fast foods. Indeed, the role of these other types of foods should not be discounted. Nevertheless, there are reasons sugar comes to the top of the list as a risk factor for obesity and diabetes in the Hispanic American. First, between 1982–1984 and 1999–2006 the rate of obesity and diabetes increased significantly in the Hispanic American, yet during the same time the intake of total fat, saturated fat and protein decreased whereas that of carbohydrates (including sugar) increased [64]. The increased frequency of obesity and diabetes occurred despite falling levels of poverty and increasing levels of education [64]. Second, a study of Hispanic women attending a prenatal clinic showed that the risk for having an infant with obesity was markedly enhanced if the mother ingested more than two soft drinks per week (4.7-fold) or had at least two sweets per week (11-fold) during pregnancy, whereas no relationship was observed with intake of saturated fat, fast foods, fruits, vegetables, alcohol or exercise [65]. Another study reported that 3-year old Hispanic children had higher intakes of sugar-sweetened beverages, fast food, and lower dairy (1% milk or skim milk) and saturated fat intake compared to non-Hispanic Whites, suggesting that intake of saturated fats cannot explain the increased risk for
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Fructose metabolism Fructose Fat, glucose ATP depletion Uric acid
Systemic effects
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↓ No and vasoconstriction decreased adiponectin insulin resistance
Renal effects
Decreased fat oxidation increased lipogenesis increased glucose production
↑ Oxidative stress inflammation vasoconstriction glomerular hypertension direct tubular effects
Chronic kidney disease
Type 2 diabetes fatty liver obesity
Figure 1. Mechanism for how fructose may cause insulin resistance and kidney disease.
obesity in this population [66]. Importantly, however, there is evidence that Hispanic Americans are ingesting lower amounts of dietary omega-3 polyunsaturated fatty acids, which have been shown to provide some cardioprotective benefits [67]. Scientific studies suggest that added sugars may increase the risk of diabetes and obesity due to both the fructose content (present in both sucrose and the sweetener, high fructose corn syrup) and the high glycemic content [68-70]. Experimental studies document that the fructose is not simply a caloric source, but activates a side-chain reaction (the AMP deaminase-uric acid-mitochondrial oxidative stress pathway) that results in gluconeogenesis, an increase in fat synthesis, and a decrease in fat oxidation (Figure 1) [71-73]. Fructose also stimulates leptin resistance in animals leading to overnutrition, resulting in excessive energy intake and a decrease in energy expenditure [74,75]. Sucrose and fructose intake in animals can also induce islet dysfunction [76,77]. Thus, although the importance of socioeconomic and cultural factors cannot be discounted, there is increasing evidence that added sugars, such as high fructose corn syrup and sucrose, may be important factors driving the increased risk for obesity and metabolic syndrome in the Hispanic American. Role of genetic mechanisms in obesity and diabetes Although sugar intake and poor food selection may lead to overnutrition and metabolic syndrome, genetic mechanisms are also contributory and may involve environmental–genetic interactions [78]. The genetic profile of the Hispanic American is heterogeneous, with conventional wisdom assuming that Caribbean Hispanic Americans have a higher frequency of African American genetic polymorphisms and MexicanAmericans and Central and South Americans having a higher Native American ancestry [23,79]. Although this general trend holds, recent studies have identified some unexpected patterns of tri-racial admixture and gender biased admixture in several Latin American populations [9]. Among different
Hispanic subgroups, Puerto Rican have a more balanced triracial group (African American, non-Hispanic White, and Hispanic), Mexicans are skewed toward Native American ancestry whereas Cuban Hispanics are skewed toward European ancestry [9]. Thus, the genetics of the Hispanic peoples may be difficult to interpret based on reported studies given the diversity in underlying populations. Despite these concerns, studies of Mexican Americans have identified several genetic polymorphisms associated with obesity (FTO [80,81]), diabetes (ENPP1 [82,83], SLC16A11 [84] and TMPRSS6 [85]), fatty liver (PNPLA3) [86], and eGFR (Loci 20q11 [87]). Although the Hispanic American has a marked increased frequency of nonalcoholic fatty liver, the frequency in the Cuban Hispanic is less, likely because of higher admixture with African American genes (particularly polymorphisms in PNPLA3), which are associated with lower frequencies of hepatic steatosis [88,89]. Epigenetic mechanisms may also play a role in the increased frequency of obesity and diabetes. Although the original focus was on the effects of low birth weight on later adult life (fetal programming), differences in the frequency of premature births are relatively minor between Hispanic Americans and non-Hispanic Whites (Table 2). More recently emphasis has been placed on the relationships of diets rich in sugars and fat during pregnancy [90,91] and/or of maternal obesity itself on the future development of obesity and diabetes in the progeny, including potential effects of diet on the gut microbiome [92].
CKD in the Hispanic American The increased incidence of ESRD in Hispanic Americans relates in part to the higher frequency of diabetes in this population compared to non-Hispanic Whites [93], and is significantly less than that observed in African Americans and Hawaiians/Pacific Islanders (Figure 2). One study showed that Cuban Americans had higher serum creatinine levels
Hispanic American and obesity
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Incidence of ESRD, 2011 (USRDS)
Frequency per million
2500
2368
1500
452
517
280
0
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White
African Native Hispanic American American American
1.0 1.7 (1.1–2.6) 4.6 (2.5–8.3)
Shown is the odds ratio (OR) for CKD, defined as an estimated creatinine clearance < 60 mL/min/1.73 m2. The OR was adjusted for demographic, clinical, and socioeconomic factors (including known predictors of chronic kidney disease). From [94]. Abbreviation: CKD = Chronic kidney disease.
940
1000
500
Table 3. Rates of chronic kidney disease in Hispanic Americans based on the Hispanic Health and Nutrition Examination Survey (HHANES). Hispanic subgroup OR (adjusted) Mexican American Puerto Ricans Cuban Americans
2000
507
Pacific lslander
Figure 2. Age- and sex-adjusted incidence of ESRD, 2011 [5]. Abbreviation: ESRD = End-stage renal disease.
than Puerto Rican Americans or Mexican Americans across gender and age with an odd ratio of 4.6 (2.5–8.3) predicting CKD [94]. The higher prevalence rate of CKD in the African Americans has been shown to be due in part to the presence of specific polymorphisms in the apolipoprotein L1 (APOL1) gene, and similar linkage has been found in Hispanic Americans who may have as much as 20 to 30% of their genes of African ancestry [95,96]. If one looks at CKD rates in different subgroups of Hispanics, the rate of CKD is highest in Cuban Americans and Puerto Ricans compared to Mexican Americans (Table 3) [94]. Further studies such as the Hispanic Chronic Renal Insufficiency Cohort study should provide a better assessment [97]. This is especially important as it may be possible in the future to target treatments aimed at the APOL1 polymorphisms that increase the risk for kidney disease [98]. These discrepancies across Hispanic subgroups may point to the environmental mechanisms that play a role in the CKD. Sugar-sweetened beverage intake, for example, is associated with increased risk for kidney disease in some [99,100] but not all studies [99], and administration of fructose to laboratory animals can cause tubular injury and accelerate CKD (Figure 1) [101,102]. In addition, recent studies have identified a potential role for heat and dehydration in inducing CKD in animals [103], raising the possibility that manual labor in hot environments such as the South may also emerge as a risk factor, similar to what has been shown in Thailand, Nicaragua, and Sri Lanka [104,105].
control of hypertension and diabetes, the expression of the APOL1 polymorphisms in certain individuals, and from environmental factors including unhealthy diets rich in sugar and hot climate predisposing to dehydration. The physician needs to be cognizant of the challenges in taking care of the Hispanic American, especially the challenges related to their higher frequency of poor health care coverage, language and sociocultural barriers, and health care provider bias. Interventions need to involve coordinated efforts to educate healthy food selection (including inclusion of healthy traditional foods), to increase physical activity, to provide counseling, and to improve community access to parks and recreational facilities. Using such approaches, some success has been achieved [106]. In addition, reducing intake of added sugars should also be of benefit, with a goal to limiting it to 10% of overall energy intake [107]. Reversing the epidemics of obesity, diabetes and hypertension will require a multipronged approach that includes education on healthy diets and hydration, improving health care delivery, treatment adherence, and programs to help prevent obesity.
Declaration of interest R Johnson, CA Roncal-Jimenez, MA Lanaspa and LG Sánchez-Lozada hold shares in Colorado Research Partners, who are trying to develop fructose inhibitors. R Johnson and MA Lanaspa are listed as inventors on patent applications for the University of Colorado. R Johnson is also on the scientific board for Amway and holds stock in XORT. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.
References Recommendations for the health care practitioner In summary, the Hispanic American has characteristics similar to the Native American in having a higher prevalence of obesity, diabetes and CKD compared to non-Hispanic Whites, while having a lower risk for cardiovascular events and mortality. Both genetic and epigenetic factors contribute to the increased risk for diabetes and obesity. Environmental factors, especially the intake of sugar-sweetened beverages, are also important. The increased prevalence of CKD also results in part from the increased frequency of diabetes, the poorer
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