Introduction
Type 2 diabetes mellitus (T2DM) is a serious clinical and public health concern in the United States [
1,
2]. T2DM continues to be prevalent despite public health efforts to develop effective policies and interventions. In 2012, it is estimated that about 12.3% of U.S. adults age 20 years and older had diagnosed or undiagnosed diabetes [
3]. T2DM is associated with an increased risk of serious complications including cardiovascular disease (CVD) and is a primary risk factor for coronary heart disease (CHD) [
4]. It is estimated that at least 68% of people aged 65 years or older with T2DM die from CVD in the United States [
5]. Moreover, a recent meta-analysis by Einarson and colleagues (2017) examined the prevalence of CVD among adults (mean age 63.6 ± 6.9 years) with T2DM during the time period between 2007 and 2017 in multiple countries, including the United States [
6]. Results indicate that about 32.2% of individuals with T2DM were affected by overall CVD. CHD was found to be the most prevalent contributor of CVD mortality (about 21.2%) among individuals with T2DM [
6]. Moreover, an analysis of data from the 2009–2012 National Health and Examination Survey (NHANES) found that about 37% of U.S. adults age 20 years and older (51% of those age 65 years or older) had prediabetes. People with prediabetes had high fasting plasma glucose (FPG) or hemoglobin A1c (HbA1c) levels, but these blood values were not high enough yet for a diagnosis of T2DM [
3]. However, prediabetes increases the risk of developing T2DM, heart disease, and stroke in the future. Estimates from the Centers for Disease Control and Prevention (CDC) suggest that about 15–30% of people with prediabetes will develop T2DM within five years [
3]. Therefore, lifestyle interventions to improve diet are an important strategy to prevent T2DM and other adverse health outcomes, and optimize long-term health [
7].
The Healthy Eating Index-2010 (HEI-2010) is a measure of diet quality in relation to the 2010 Dietary Guidelines for Americans (DGA 2010) [
8]. The main objective of DGA 2010 is to promote healthy eating in the general population [
9]. The HEI-2010 score captures key nutrients and food groups that reflects current evidence on the dietary components that are healthful [
10]. Another popular tool used to measure dietary quality is the Alternate Healthy Eating Index-2010 (AHEI-2010), which is based on evidence-based recommendations that incorporates additional components that focus on foods and nutrients to predict the risk of chronic disease [
11,
12]. The most recent U.S. dietary guidelines (DGA 2015) have somewhat moved in the direction suggested by the AHEI [
9]. For instance, the HEI-2015 has included added sugars and saturated fats as two separate components instead of being combined into empty calories, which is one of the components in HEI-2010 [
13]. However, excessive calories from alcohol (part of empty calories) has been removed in the HEI-2015 whereas the AHEI-2010 includes alcohol as a separate component to assess dietary quality. With the exception of these minor changes, most of the HEI-2010 components are kept in HEI-2015 [
13]. The AHEI-2010 provides additional food and nutrient components that are neither found in HEI-2010 nor HEI-2015. Therefore, it is useful to utilize the HEI and AHEI indices to examine their association with health or disease outcomes, such as T2DM.
The HEI-2010 and AHEI-2010 are useful tools measure adherence to dietary guidelines and evidence-based recommendations. The HEI-2010 and AHEI-2010 are similar in some aspects. For example, both indices capture consumption of fruits, vegetables, whole grains, and sodium. However, the AHEI-2010 reflects a critique of the HEI-2010 where it provides dietary recommendations that better improve health risk factors, and it has shown to more strongly predict chronic disease risk (i.e., T2DM) and mortality [
11,
12]. The AHEI-2010 incorporates distinct features from the HEI-2010. For example, the AHEI-2010 pays more attention to fat quality (i.e., intakes of omega-3 fats and polyunsaturated fats), promotes intake of nuts and legumes, and considers moderate alcohol intake (Male: 0.5–2.0 drinks/day; Female: 0.5–1.5 drinks/day) as beneficial to health regardless of disease status (i.e., diabetes). In addition, the AHEI-2010 recommends to limit intake of red and processed meats and avoid added sugars (i.e., sugar-sweetened beverages and fruit juice) [
12]. Both HEI-2010 and AHEI-2010 complement one another in terms of evaluating essential foods groups and nutrients. Therefore, it is useful to utilize the HEI-2010 and AHEI-2010 as tools to assess dietary quality and examine their association with health markers and diabetes status.
Several prospective studies have evaluated HEI-2010 and AHEI-2010 scores in relation to T2DM [
11‐
18]. Results from a recent meta-analysis of 15 cohort studies, with follow-up time ranging from 5 to ≥24 years, show that diets of the highest quality (compared highest vs. lowest quintile scores), as assessed by the HEI, AHEI, and DASH, are associated with a significant risk reduction for all-cause mortality, T2DM and other chronic diseases (i.e., cardiovascular disease, cancer) (
P < 0.05) [
18]. The meta-analysis included seven reported studies (six in the United States and one in Europe) on T2DM as the main disease outcome, with age ranging from 30 to 79 years, among individuals from different ethnic groups including Caucasian (European), non-Hispanic White, African American, Hispanic, and Asian. Of these studies, the main result indicates that diets that score highly on the HEI, AHEI, and DASH are associated with a significant reduction in the risk of T2DM (22%,
P < 0.05) [
18]. In these studies, the HEI-2010 (and HEI-2005) has been evaluated among individuals with chronic disease (including T2DM) with mixed results. Some studies have shown moderate inverse associations and some showed no association with regards to the HEI-2010 and T2DM risk [
12,
17]. However, the AHEI-2010 (and AHEI-2005) has demonstrated to be more strongly associated with chronic disease, including T2DM [
11,
12,
14,
15,
17]. McCullough and colleagues evaluated whether or not the AHEI-2005 would predict risk reduction for chronic disease (including CVD, cancer, or nontraumatic death) more effectively than the HEI-2005 [
11]. The study was conducted in the United States among females aged 30–75 years enrolled in the Nurses’ Health Study (NHS), and males aged 40–75 years participated in the Health Professional’s Follow-up Study (HPFS). The main result indicates that the AHEI-2005 was more effective in predicting chronic disease risk than the HEI-2005. The overall risk reduction with the AHEI-2005 (highest quintile compared to lowest quintile) was lower among men and women, with 11 and 3%, respectively [
11]. In 2012, Chiuve and colleagues used the NHS/HPFS datasets to assess the associations of the HEI-2005 and the AHEI-2010 with major chronic diseases, including T2DM [
12]. The main result indicates that the AHEI-2010 was more strongly associated with T2DM risk than the HEI-2005. Although both indices were significant, the association between HEI-2005 and T2DM risk was attenuated after adjustment for confounders [
12]. In 2015, Jacobs and colleagues compared associations of the HEI-2010, AHEI-2010, DASH, and Alternate Mediterranean Diet Score with T2DM risk [
17]. The study was conducted in the United States among men and women 45–75 years who participated in the Multiethnic Cohort Study. The main result indicates that the AHEI-2010 was associated with a 12% risk reduction of T2DM among white individuals. However, the HEI-2010 was not significantly associated with T2DM risk [
17].
While there is growing evidence from prospective studies that high scores on the HEI or AHEI (corresponds to healthy dietary pattern) are inversely associated risk reduction of chronic disease, it remains unclear on whether the HEI-2010 or AHEI-2010 is preferable as a tool for dietary assessment in people with T2DM. Therefore, an improved understanding of the relationships between dietary pattern and health outcomes will help identify the appropriate tool to assess dietary quality for diabetes management and subsequently, decrease the risk of CHD and other diabetes-related complications.
In this study, the authors hypothesized that the AHEI-2010 is more strongly associated with T2DM than the HEI-2010 dietary pattern. To the authors’ knowledge, this was the first study that compared the HEI-2010 and AHEI-2010 scores and their associations with diabetes status in a representative sample of U.S. adults. Moreover, there is limited understanding of the differences of individuals’ dietary behavior at different stages of disease development. For that reason, the authors defined diabetes status into three categories: nondiabetes, prediabetes, and diabetes (T2DM). The authors were interested in looking at differences in dietary quality, and how they are associated with the stages of disease development. Furthermore, few studies have investigated the relationship between dietary pattern and physiological health markers. A better understanding of the biological basis of health markers (i.e., lipid profile) in relation to diet may better explain the differences in metabolism of individuals with and without chronic disease. In addition, this may provide an insight to develop more effective treatments for diabetes.
The main objectives of this study were three-fold: 1) To determine whether there were relationships between two measures of dietary quality, the HEI-2010 and AHEI-2010 and diabetes status (nondiabetes, prediabetes, T2DM); 2) To examine the relationships between the HEI-2010 and AHEI-2010 and health markers (including biomarkers); 3) To determine the strength of the relationships between the HEI-2010 and AHEI-2010 with diabetes status while controlling for health markers, lifestyle and demographic factors. All analyses were based on data from the 2007–2010 National Health and Nutrition Examination Survey (NHANES).
Discussion
The results of present study were not consistent with the results of earlier cross-sectional studies that compared the HEI and AHEI scores in relation to T2DM. The main result of this study was that the AHEI-2010 did not to perform better than the HEI-2010 in terms of its relationship with diabetes status. This was in contrast with the results of a cross-sectional study by Huffman and colleagues that examined the relationship between the HEI-2005 and the AHEI-2005 scores and 10-year predicted CHD risk in Cuban Americans with and without T2DM [
40]. The authors performed hierarchical linear regression models and used diabetes status as one of the covariates to predict CHD risk. They found that for every unit increase in the AHEI-2005 score, there was a 0.24-point reduction in the 10-year CHD risk score among participants with T2DM. However, they did not find a significant association between HEI-2005 score and CHD risk among participants without T2DM [
40]. Another similar study by Huffman and colleagues assessed the relationships of the HEI-2005 and AHEI-2005 among Haitian Americans (HA) and African Americans (AA) with and without T2DM [
41]. They found that the HEI-2005 score was significantly higher among individuals with diabetes (T2DM) compared to nondiabetes after controlling for age, gender, ethnicity, and education. However, the difference in AHEI-2005 scores among individuals with diabetes and nondiabetes was not significant [
41].
There are several possible ways to interpret the apparent inconsistencies between the results of these earlier cross-sectional studies and the present study. First, this study used total the HEI and AHEI scores based on the 2010 dietary guidelines and evidence-based recommendations rather than the 2005 guidelines. Second, this study and the earlier studies focused on different outcomes. This study used logistic regression to examine diabetes status as the dependent variable and the HEI-2010 and AHEI-2010 scores as the independent variables. Third, this study used differences in the HEI-2010 and AHEI-2010 by diabetes status and did not further assess the health risks of individuals with diabetes (T2DM). The AHEI-2010 is based on current knowledge of dietary factors that mainly contribute to CVD (i.e., myocardial infarction, angina, stroke, transient ischemic attack, and revascularization) [
11,
12]. T2DM is associated with increased risk of CVD and is an independent risk factor for CHD [
4,
40]. This may indicate that the AHEI-2010 would be more applicable among diabetic individuals with pre-existing CVD conditions.
Some prospective studies have found significant inverse associations between the HEI-2010 and AHEI-2010 scores and risk of T2DM [
11,
14‐
17]. The association was found to be stronger for the AHEI-2010 than for the HEI-2010 in relation to T2DM. These studies found that greater adherence to the AHEI-2010 dietary pattern was associated with 23–36% risk reduction in T2DM [
14,
17]. However, the present study did not confirm earlier findings of significant association of the HEI-2010 nor the AHEI-2010 in relation to T2DM. A possible reason could be differences in how diet was assessed (i.e., 24-h recall vs. FFQ) to calculate the HEI-2010 and AHEI-2010 scores. This study used a single 24-h dietary recall to calculate the HEI-2010 and AHEI-2010 scores. Therefore, measuring dietary quality based on one or even two days of intake may not serve as a good predictor of chronic disease (i.e., diabetes) that takes years to develop. However, assessing dietary quality based on habitual or usual intake may serve as a better predictor. It might be possible to find a significant relationship with diabetes status if the HEI-2010 and AHEI-2010 scores were calculated based on the FFQ since it is designed to evaluate usual dietary intake. NHANES uses the 24-h recall rather than the FFQ to capture food intake. This study attempted to replicate the methods from previous studies that used the 24-h dietary recalls to compute the HEI-2010 and AHEI-2010 scores from NHANES [
7,
25,
26,
42,
43]. NHANES is currently considered to be the best source of valid and reliable data on dietary intake.
Additionally, there is inconsistency in modeling decisions and specification when examining the association between diet and disease (i.e., T2DM). In epidemiology, some studies attempt to specify models that are parsimonious while other studies control for a large number of variables. When variables are intercorrelated (as socioeconomic and demographic characteristics often are), this can lead to multicollinearity if multiple variables are entered into the model. In the present study, the AHEI-2010 score did not provide any improvement over the HEI-2010 in terms of predicting or explaining T2DM (and prediabetes) after adjusting for potential covariates. A possible reason is the interrelationships among the covariates that are included in the multivariate models (i.e., health markers and lifestyle characteristics). For instance, smoking status was significantly associated with physical activity, body size (as measured by WC), and presence of comorbidities (as measured by total comorbidity score). Also, dietary quality (using the total HEI-2010 and AHEI-2010 scores) seemed to be related to the other predictors, which makes it difficult to construct a definitive model that determines the effect of dietary quality alone in relation to diabetes status. The predicted probabilities suggest that the models specified for only the HEI-2010 and AHEI-2010 scores (total and sub-components) classified the least percentage of the sample correctly (about 52% correct classification) with respect to diabetes status compared to the other factors (i.e., sociodemographics, health markers). Classification of diabetes status did not improve when adding more variables to the models possibly because of the interrelationships among the variables. In addition, the percentage of false negative (i.e., when results indicate a person does not have the disease but actually does have the disease) increases when adding more variables to the models. Therefore, the true predictive value of dietary quality (using HEI-2010 and AHEI-2010) is not observed in relation to diabetes status. Diet is a complex exposure variable. There are numerous factors that influence diet, which in turn can have an impact on disease development (i.e., T2DM). This calls for more consistency in model specification, and maybe alternative approaches, to examine the relationship between diet and disease.
Both the HEI-2010 and AHEI-2010 scores indicated that U.S. adults need improvement in dietary pattern (mean total HEI-2010 score = 47.3 ± 0.4; mean total AHEI-2010 score = 38.2 ± 0.4). Adults with diabetes appeared to have more healthful dietary patterns (as shown by higher total scores) compared to adults with prediabetes and nondiabetes. It is likely that participants with diabetes are receiving more regular health care than other groups. Participants with diabetes (diagnosed) with regular doctor visits are more closely followed and receive nutrition counseling and are taught self-management skills to improve their health.
The HEI-2010 and AHEI-2010 individual food and nutrient component scores are clinically important because they can provide more insight about dietary quality, which would allow more flexibility to tailor dietary intervention among individuals with diabetes. This study found statistically significant differences in the sub-component HEI-2010 and AHEI-2010 scores across diabetes status (Tables
2 and
3). Some of the food and nutrient groups in the HEI-2010 and AHEI-2010 were aligned with one another in terms of protein and carbohydrate intake. For example, adults with diabetes had the highest intake of total protein foods (corresponding to highest score) in the HEI-2010 (Table
2), which was consistent with their having the highest intake of red and/or processed meat (corresponding to lowest score) in the AHEI-2010 (Table
3). Similarly, adults with diabetes had the lowest intake of empty calories (corresponding to highest score) in the HEI-2010 (Table
2), which was consistent with their having the lowest intakes of alcohol (corresponding to lowest score) and sugar-sweetened beverages and fruit juice (corresponding to highest score) in the AHEI-2010 (Table
3). In terms of clinical relevance, it seems that adults with diabetes are consuming food groups that are higher in protein and lower in carbohydrates and fats than other groups.
A possible explanation is that individuals with T2DM receive regular care and are counseled to avoid consuming excessive carbohydrates. As part of diabetes self-management, they are being taught to monitor their carbohydrate intake through carbohydrate counting, or “carb counting,” which is a meal planning technique for managing blood glucose levels in balance with medication or insulin intake and physical activity [
31]. In addition, individuals with T2DM are more likely to consume a low-fat diet as recommended by the American Diabetes Association (ADA) and American Heart Association [
31,
44]. As a result, the decrease in carbohydrate or fat intakes involves a compensatory increase in protein intake.
High protein diets such as the Atkins, South Beach, and Paleo diets are recommended weight reduction methods because protein reduces hunger, improves satiety, and increases thermogenesis [
45]. Also, when combined with a reduction in calories, high protein diets enhance weight reduction while maintaining lean muscle mass [
45]. Several studies have shown the benefits of a modest increase in dietary protein intake among individuals with diabetes with normal renal function [
46‐
48]. Higher dietary protein consumption has a favorable effect on CVD risk factors among individuals with T2DM. It is associated with reduction in HbA1c, total serum cholesterol, LDL cholesterol, triglycerides, blood pressure, and C-reactive protein. It is also associated with an increase in HDL cholesterol [
46‐
48]. In clinical practice, T2DM patients affected by overweight and obesity and have normal renal function are often advised to increase absolute protein intake to 1.5–2 g/kg of body weight (or 20–30% of total caloric intake) during weight reduction [
45]. However, the ADA recommends that dietary protein not exceed between 1 and 1.5 g/kg of body weight (or 15–20% of total caloric intake) [
31]. Despite the potential health benefits, high protein intake may have adverse long-term effects on renal function in individuals with diabetes (as well as in healthy individuals).
The present study demonstrated that adults with diabetes consumed less sugar and alcohol compared to adults with prediabetes and nondiabetes. The HEI-2010 and AHEI-2010 differ in how they assess the intakes of sugar and alcohol in the diet. In HEI-2010, sugar and alcohol intake were summed and counted as empty calories. Empty calories are composed of all calories from solid fats, added sugars, and alcohol intake beyond a moderate level (more than 13 g /1000 cal). In the AHEI-2010, sugar and alcohol are considered to be separate categories. Additionally, AHEI-2010 considers moderate alcohol intake (Male: 0.5–2.0 drinks/day; Female: 0.5–1.5 drinks/day) as part of a healthful dietary pattern. This means that individuals with moderate alcohol intake received higher scores than non-drinkers (10 points versus 2.5 points). This method of scoring severely penalized nondrinkers, especially for individuals with diabetes. In this sample, the percentage of individuals with alcohol component scores above 2.5 points (drinkers) was approximately 7.7% for individuals with nondiabetes, 7.9% for individuals with prediabetes, and 1.0% for individuals with diabetes. This is likely to be due to the nutrition education and counseling that is typically provided to individuals diagnosed with diabetes (T2DM). As part of diabetes self-management, the ADA recommends that individuals with diabetes (both type 1 and type 2) reduce or minimize alcohol consumption [
31], because alcohol intake (especially on an empty stomach) lowers blood glucose and causes hypoglycemia. In addition, many alcoholic beverages contain added sugars, which can lead to excess calories and elevated triglycerides, increasing the risk of heart disease [
31]. In this sample, adults with diabetes seemed to minimize alcohol or not drink it at all, which is consistent with diabetes self-management. This suggests that the HEI-2010 may be a better tool for assessing diet quality than the AHEI-2010 for individuals with T2DM.
The present study found a significant linear trend between HEI-2010 and AHEI-2010 quartiles and some of the health markers (Tables
4 and
5). For example, there was a significant decrease in BMI, WC, and triglycerides with increasing total HEI-2010 and AHEI-2010 scores (Tables
4 and
5). These findings are also clinically important because these health markers are negatively influenced by consuming a healthy diet (i.e., whole grains, fruits, vegetables, nuts and legumes). In clinical practice, individuals (especially for diabetes) are often advised to make dietary changes, and compliance to a healthful dietary pattern can lead to improvement in anthropometric or metabolic outcomes. However, there was no difference in CRP levels across HEI-2010 and AHEI-2010 quartiles, which makes the clinical relevance of this health marker to be less clear. Contrary to the present study, previous studies have shown significant inverse association between CRP levels and dietary patterns [
51,
52]. Smidowicz and Regula (2015) conducted a systematic review on the role of diet in reducing inflammation and thereby decreasing the risk of chronic disease [
52]. The review focused on the effects of several dietary patterns (i.e., Mediterranean diet, DASH diet, low-fat vs. low-carbohydrate) in relation to inflammatory markers (CRP and IL-6) [
52]. Based on the review of the research, the authors concluded that it is difficult to determine which dietary pattern is optimal for reducing inflammation. The relationship between inflammation and diet is complex since inflammatory response is often triggered by the cumulative effect of dietary and other factors [
52].
Despite the differences in construction of these indices to assess diet, both the HEI-2010 and AHEI-2010 have similar components of a healthful dietary pattern. Overall, the pillars of a healthy diet include higher intakes of fruits, vegetables, whole grains, nuts, legumes, unsaturated fats (i.e., PUFA), and lower intakes of sodium, sugar (i.e., sugar-sweetened beverages) and red and processed meats [
49]. Currently, the DGA 2015 does not recommend adherence to a single diet plan to achieve healthy eating patterns, but recommends instead that individuals consume specific food groups that are healthful [
50]. Similarly, the ADA recommends that individuals with diabetes consume from various food groups that are high in fiber (i.e., whole grains, vegetables) and avoid foods and/or beverages that contain added sugars to meet metabolic goals such as glucose, HbA1c, lipid levels, and blood pressure [
31].
Strengths and limitations
Strengths of this study include the use of a large, nationally representative sample of U.S. adults with reliable estimates of dietary intake. Therefore, the findings are generalizable and have implications for the development of effective policies to improve health and/or disease outcomes. NHANES is the only national survey that currently provides complete dietary intake through utilizing the AMPM to screen 24-h dietary recalls that are valid and reliable. NHANES has a long history of collecting nutrition data (since the 1960s) and continues to incorporate improvements to refine their dietary methodology.
However, this study also has some limitations: First, NHANES is a cross-sectional study design and therefore, the results cannot support causal inferences about the relationships between HEI-2010 and AHEI-2010 and diabetes status. Second, this study used a single 24-h dietary recall to calculate the HEI-2010 and AHEI-2010 scores, which may not reflect individuals’ habitual or usual intake. In addition, the 24-h recall may be subject to measurement error because it relies on participants’ ability to recall and accurately self-report dietary intake, which may lead to under- or over- reporting. Lastly, NHANES does not explicitly collect information on the type of diabetes (i.e., T1DM or gestational), which may lead to misclassification. However, this study used the available information in NHANES to construct a diabetes classification variable based on using a combination of self-reported and laboratory measured attributes to minimize misclassification.
Conclusion
In conclusion, HEI-2010 and AHEI-2010 were used as predictors of T2DM, and neither was significant, either alone or in combination with sociodemographic characteristics, health markers, and lifestyle behaviors. However, there were some significant differences in the means of the sub-component HEI-2010 and AHEI-2010 scores by diabetes status. In addition, there were significant positive relationships between the HEI-2010 and AHEI-2010 scores and health markers. Individuals with higher total HEI-2010 and AHEI-2010 scores had better health marker values compared to those with lower diet quality scores. Although total HEI-2010 and AHEI-2010 were not significant predictors of T2DM as expected, the role of diet should not be dismissed as a potential factor in the development of T2DM. There are factors that point to a role of diet in the development of T2DM: the significant differences in means of health markers across HEI-2010 and AHEI-2010 scores, and the significant differences in means of health markers (i.e., BMI, WC, total cholesterol, HDL, LDL, TG, insulin, blood pressure, comorbidity score) by diabetes status. These findings indicate that diet has some influence on T2DM development, leading to the conclusion that better tools are needed to assess dietary intake in persons with diabetes and to better understand the role of diet in T2DM risk.
The main finding of the present study is that diet alone did not have strong predictive ability with respect to T2DM. Neither the HEI-2010 nor the AHEI-2010 performed better than sociodemographics alone as predictors of T2DM. Some sociodemographic characteristics are likely to be associated with genetic differences. This study was not able to assess the impact of genetics, but there has been some recent research investigating the role of genetic factors in the development of T2DM, but this area of inquiry is still in its early stages [
53,
54]. In addition, the HEI-2010 and AHEI-2010 were not specifically designed as tools to assess dietary quality in diabetics. Future research is needed to develop an index based on relevant dietary components that contribute to T2DM. This will provide better utility for dietary assessment in adults with diabetes in clinical and community settings.