Egg Intake and Dietary Quality among Overweight and Obese Mexican-American Postpartum Women

Despite their low cost and high nutrient density, the contribution of eggs to nutrient intake and dietary quality among Mexican-American postpartum women has not been evaluated. Nutrient intake and dietary quality, as assessed by the Healthy Eating Index 2010 (HEI-2010), were measured in habitually sedentary overweight/obese (body mass index (BMI) = 29.7 ± 3.5 kg/m2) Mexican-American postpartum women (28 ± 6 years) and compared between egg consumers (n = 82; any egg intake reported in at least one of three 24-h dietary recalls) and non-consumers (n = 57). Egg consumers had greater intake of energy (+808 kJ (193 kcal) or 14%; p = 0.033), protein (+9 g or 17%; p = 0.031), total fat (+9 g or 19%; p = 0.039), monounsaturated fat (+4 g or 24%; p = 0.020), and several micronutrients than non-consumers. Regarding HEI-2010 scores, egg consumers had a greater total protein foods score than non-consumers (4.7 ± 0.7 vs. 4.3 ± 1.0; p = 0.004), and trends for greater total fruit (2.4 ± 1.8 vs. 1.9 ± 1.7; p = 0.070) and the total composite HEI-2010 score (56.4 ± 12.6 vs. 52.3 ± 14.4; p = 0.082). Findings suggest that egg intake could contribute to greater nutrient intake and improved dietary quality among postpartum Mexican-American women. Because of greater energy intake among egg consumers, recommendations for overweight/obese individuals should include avoiding excessive energy intake and incorporating eggs to a nutrient-dense, fiber-rich dietary pattern.


Introduction
Hispanics, the largest minority group in the United States (U.S.) [1], have a higher prevalence of obesity and cardiometabolic disease risk factors relative to other ethnic groups, disproportionately increasing their risk for chronic conditions such as cardiovascular disease and diabetes [2,3]. Among women of reproductive age, excess weight gain during pregnancy and failure to lose weight postpartum have been associated with long-term obesity and further risk for chronic diseases [4]. This is of particular concern for postpartum Hispanic women due to higher pre-pregnancy obesity rates [5] and the presence of many contributors to excessive weight retention after childbirth [6].
Several dietary factors are essential for the prevention and management of chronic diseases. Studies have shown that a higher dietary quality is inversely related to chronic disease risk factors such as waist circumference, low density lipoprotein (LDL)-cholesterol, insulin and C-reactive protein (CRP) [7,8]. Despite the known benefits of consuming adequate diets, available surveillance data on

Measures
Trained bilingual research staff collected and processed all baseline sociodemographic, anthropometric and diet data prior to the randomization allocation. Standard procedures were used to measure in triplicate height, weight, and waist circumference.
Three unannounced 24-h recalls using a five-step, multiple-pass method were collected to assess baseline dietary intake data [35]. The dietary recalls were randomly collected during all seven days of the week, including two week days and one weekend day. The Nutrition Data System for Research (NDSR) software version 2009, developed by the Nutrition Coordinating Center (NCC), University of Minnesota, Minneapolis, MN, was used to analyze dietary data. Dietary variables of interest were estimates of total energy intake, amount and percentage of energy provided by macronutrients, and selected micronutrients. Egg intake was reported as servings per day, with one serving being equivalent to one large egg. Participants were classified as egg consumers if they reported any egg intake (including egg products) in at least one of the three 24-h dietary recalls (mean egg intake >0 servings/day).
Diet quality was assessed by calculating the HEI-2010, as described elsewhere [32]. Briefly, the HEI-2010 includes 12 components divided into adequacy components that should be included in the diet (total fruit, whole fruit, total vegetables, greens and beans, whole grains, dairy, total protein foods, seafood and plant proteins, and fatty acids) and moderation components that should be limited (refined grains, sodium, and empty calories). Individual components are scored from 0 to 5, 10, or 20 points; the total HEI-2010 score is calculated as the sum of all individual components, for a total of 100 possible points [36]. Maximum scores correspond to conformance to the dietary guidelines, reflecting higher consumption of adequacy components and lower consumption of moderation components. The scoring standards are assessed as food group and nutrients consumed per intake of 4184 kJ (1000 kcal), percentage of total energy intake, or a ratio, providing information on a density basis rather than absolute amounts [32]. The recommended approach to calculating HEI scores using NDSR was followed [37].

Statistical Analysis
All statistical analyses were conducted with software IBM SPSS Statistics for Windows, version 21.0 (IBM Corp., Armonk, NY, USA). Descriptive characteristics of participants and dietary data are presented in text and tables as mean˘standard deviation (SD). Nutrient intake for carbohydrates, protein, fat, and saturated fat was expressed as percentages of total energy. We used independent groups t-tests to compare egg consumers and non-consumers on each of the nutrient intake measures, each HEI-2010 component, and the HEI-2010 total score.

Participant Characteristics
Participants were 139 women (28˘6 years old) self-identified as Mexican or Mexican-American (Table 1). Per study design, all participants were overweight or obese (mean BMI = 29.7˘3.5 kg/m 2 ) with mean waist and hip circumferences of 86˘9 cm and 106˘8 cm, respectively, and mean body fat of 38.6%˘4.6%. Based on dietary intake data from three dietary recalls, 57 women (41% of participants) were classified as egg non-consumers, whereas 82 women (59% of participants) were classified as egg consumers. There were no significant differences in age, BMI, waist or hip circumferences, or body fat percent between egg consumers and non-consumers.

Nutrient Intake
Intake of total energy, macronutrient, and select micronutrient intake data for egg consumers and non-consumers are displayed in Table 2. Relative to non-consumers, egg consumers had 14% greater energy intake (p = 0.033), associated with consuming 17% more protein (p = 0.031) and 19% more fat (p = 0.039). There were no significant differences between egg non-consumers and consumers in the absolute amount of saturated and polyunsaturated fat, including ω-3 fatty acids, but monounsaturated fat intake was 24% greater for egg consumers than non-consumers (p = 0.020). There were no significant differences between egg non-consumers and consumers in the proportion of energy provided by macronutrients (data not shown), with the exception of monounsaturated fat (10.5%˘2.4% of energy for non-consumers vs. 11.6%˘3.1% of energy for consumers; p = 0.026). As expected, egg consumers had greater intake of dietary cholesterol (109%; p < 0.0001) than non-consumers. Whereas there were no significant differences between groups in total or added sugars intake, egg consumers had greater intake of total fiber (22%; p = 0.035) and soluble fiber (29%; p = 0.017) relative to non-consumers.

Healthy Eating Index 2010
Estimated mean HEI-2010 individual component and total scores for egg non-consumers and consumers are presented in Table 3. There were no significant differences in adequacy component scores between groups, with the exception of the total protein foods score, which was greater in egg consumers than in non-consumers (p = 0.004). There was a non-significant trend for egg consumers to have a greater total fruit score relative to non-consumers (p = 0.070). There were no significant differences between groups in moderation component scores, although relative to non-consumers, there were trends for egg consumers to have a lower score (greater intake) for sodium (score of 4.5˘3.5 vs. 3.5˘3.0 out of 10; p = 0.074) and a greater score (lower intake) for empty calories (score of 8.8˘5.7 vs. 10.6˘5.3 out of 20; p = 0.059). The total composite HEI-2010 score did not differ significantly between groups, although was slightly greater for egg consumers (52˘14 vs. 56˘13 out of 100 points for egg non-consumers and consumers, respectively; p = 0.082).

Discussion
This study assessed the contribution of eggs to dietary quality among an understudied group of the population, Mexican-American postpartum women, by comparing nutrient intake and HEI-2010 scores between egg-consumers and non-consumers. This report is of importance because there is limited information regarding contributors to nutrient intake and dietary quality among Mexican-American women of reproductive age. Study findings indicated that egg consumers had greater intakes of energy, protein, fat, monounsaturated fat, cholesterol, total and soluble fiber, vitamin D, riboflavin, vitamin B12, choline, sodium, potassium, and phosphorus, and a modestly higher HEI-2010 score than non-consumers. Similarly, in the only study of its kind conducted in a diverse sample of pregnant Hispanic women, egg consumers had higher intakes of several nutrients including protein, fat, vitamins K and E, cholesterol, total polyunsaturated fatty acids, and DHA [31]. Comparable information among postpartum women is lacking.
In the current study, a greater proportion of participants (59% or n = 82) reported consuming eggs than what has been reported for U.S. adults (19%) or Mexican-American adults (32%) using NHANES III data [30]. A majority of study participants (78%) were immigrants of Mexican origin who had been in the U.S. for 12˘7 years [34,38,39]. Several reports indicate that multiple factors that are part of the immigration experience, such as acculturation, generational status, and time in the U.S., are associated with lifestyle modifications often associated with less healthful dietary patterns in part due to immigrants' lack of familiarity with available foods in their new environment [40][41][42][43]. However, eggs are a low-cost common protein source in the Mexican diet, as evidenced by the high per capita consumption of eggs in Mexico compared to other countries [28], which may have made eggs a nutritious and familiar dietary choice among the generally low-socioeconomic status study participants [34,38,39]. Nevertheless, the possibility cannot be ruled out that the methodology used in the current study (three 24-h recalls) may have better allowed to capture individual instances of egg intake than using only one 24-h recall for NHANES.
In the current study, energy intake was greater for egg consumers than non-consumers. Considering that participants were overweight or obese, this increased energy intake could be of concern because it could potentially translate into long-term weight gain, even when mean total energy intake was lower than what has been reported among U.S. adult women (7543˘59 kJ/day (1803˘14 kcal/day) according to NHANES 2009-2010 data [44]). The greater energy intake among egg consumers could have been in part attributed to greater fat intake. Differences in fatty acid intake were due to greater monounsaturated fatty acids in the diet of egg consumers vs. non-consumers, which explains the greater, albeit non-significant, HEI-2010 fatty acid ratio score ((polyunsaturated fatty acids + monounsaturated fatty acids)/saturated fatty acids) for egg consumers. Although these differences cannot be solely attributed to the fatty acid contribution from eggs, it is noteworthy that roughly 50% of fatty acids in eggs are monounsaturated [45]. Regarding polyunsaturated fatty acids, fortified eggs can be an important dietary contributor to ω-3 fatty acids. A study including Mexican pregnant women reported that 20% of total DHA intake was supplied by eggs [27]. In a diverse sample of pregnant Hispanic women, a greater proportion of egg consumers than non-consumers had DHA consumption in the highest tertile of intake [31]. In the current study, differences in ω-3 fatty acid intake between egg non-consumers and consumers were not statistically significant. Although as expected in the current study egg consumers had greater dietary cholesterol than non-consumers, intake levels did not exceed current recommendations for cholesterol intake (300 mg/day) [46].
Adequate protein intake is crucial for women of reproductive age to maintain maternal and fetal tissue accretion during pregnancy and milk production during lactation [47][48][49]. In fact, a recent report [50] suggested that protein needs for pregnancy may be even higher than current dietary reference intake recommendations of 1.1 g/kg of body weight/day [46]. In the current study, both absolute protein intake and the HEI-2010 score for total protein foods were greater for egg consumers than non-consumers, although as previously reported the total protein HEI-2010 score was indicative of appropriate consumption of protein-containing foods for all participants [38]. Intake of animal protein was also greater for egg consumers than for non-consumers, although non-significantly different (data not shown). However, the high-quality nature of egg protein [24] may provide an additional nutritional advantage to women who incorporate eggs as part of their diet in the postpartum period.
In the present study, egg-consumers had a greater intake of vitamin D compared to non-consumers. According to NHANES 2003-2006 data, eggs were ranked the third main source of vitamin D (after milk and fish/seafood), contributing with about 5% of vitamin D intake among adults in the United States [51]. This is important considering that it is estimated that between 40% and 80% of U.S. adults, depending on gender and age range, have inadequate vitamin D intake [52]. Furthermore, results from a meta-analysis study showed that low maternal vitamin D levels during pregnancy are associated with risk of preeclampsia, gestational diabetes, preterm birth and small-for-gestational age [53].
All participants in the current study had HEI-2010 scores suggesting intake of diets with low quality or in need for improvement (55˘14 relative to a maximum score of 100). A report using NHANES data suggested that at the population level HEI-2010 total score was 53 [54]. Furthermore, participants were not meeting intake recommendations for several nutrients, including fiber, Ca, vitamin E, vitamin C and folate. Egg consumers had a greater HEI-2010 score for total protein foods, and trends towards greater scores for total fruit and empty calories, and lower score for sodium. These differences resulted in a modestly greater total HEI-2010 score for egg consumers.
The main risk associated with egg consumption in the U.S. is salmonellosis, mainly due to consumption of raw or undercooked eggs [55]. The risk is particularly important during pregnancy since salmonellosis may be transmitted to the fetus, increasing the risk of preterm delivery and intrauterine death [55,56]. In a study about food safety, most pregnant women were aware about recommendations to avoid raw eggs; however, they still reported consumption of eggs with runny yolk (35%) and cookie dough containing raw eggs (40%), indicating the need to improve instructions given to this target group [57]. Nevertheless, the potential benefits associated with their high nutritional quality outweigh risks as long as eggs are properly cooked before consumption.
Prior reports from the current study have documented that participants included a large proportion of women living under disadvantaged socio-economic conditions in neighborhoods with limited food access [34,38,39]. In general, Hispanic households have been documented to have greater food insecurity rates than the general population [58]. Thus, an additional benefit of egg intake for the target population in the current study as well as other Hispanic subgroups is associated with their low cost. In general, the cost of foods is directly associated with protein but inversely associated with carbohydrate content [59]. In contrast, relative to other animal sources of protein, eggs are an inexpensive nutrient-dense, high-protein, low-carbohydrate food [24,59]. According to the Nutrient Rich Foods Index, developed as an effort to aid consumers select nutritious food choices under financial constraints, eggs are a low cost source of protein, vitamin A, vitamin B12, riboflavin, calcium and zinc, providing excellent nutritional value for the money [60].
An important limitation of the current report is that dietary assessment was conducted using three 24-h dietary recalls, a method subject to intake underreporting, particularly among women and Hispanic individuals [61,62], as indicated by the relatively low energy intake observed in the current study. Although this limitation was addressed by calculating the HEI-2010 scores on an energy-density basis when assessing dietary quality [32], differences observed in individual nutrient intakes between egg consumers and non-consumers, particularly macronutrients, are likely a result of absolute energy intake and not solely due to egg consumption. Moreover, data from 24-h dietary recalls may not be the best indicator of habitual food consumption, including eggs.

Conclusions
The current report suggests that Mexican-American women who consumed eggs had greater nutrient intake and higher dietary quality than non-consumers. Whereas these data do not indicate that egg intake directly improves dietary quality, it could potentially be an indicator of a healthier dietary pattern. Despite the greater energy intake observed among egg consumers, the low cost and high nutritional quality of eggs make them an ideal protein source that is likely to provide greater benefit than risk to the target population, especially if dietary recommendations focus on consuming eggs as part of a dietary pattern that also includes nutrient-dense and fiber-rich foods and maintaining a healthy body weight.