FDNJ

Introduction

Adolescents comprise about 13% of the US population equating to almost 43 million individuals. Adolescence is a critical stage of life and an intense period for growth and development as it is the period of transition from childhood to adulthood signified by sexual maturation and major physical and hormonal changes [1-3]. Adolescents generally gain over 40% of their adult weight and over 15% of their adult height during this period and require higher levels of energy, and macro- and micro-nutrients. The 2020–2025 Dietary Guidelines for Americans (DGA) identified that in addition to having lower diet quality than their younger counterparts, adolescents also have the greatest disparities between the recommended and current nutrient intakes and are at greater risk of nutrient inadequacy [4]. Inadequate intakes of micro-nutrients such as calcium, iron, magnesium, phosphorus, potassium, folate, vitamin B₆, vitamin B₁₂, choline, vitamin D among adolescents have been previously identified [5-7]. During adolescence inadequate dietary intakes can have serious health consequences including delayed growth, impaired cognitive function, sexual development disorders, endocrine dysfunction, and inadequate bone mass [8-11]. Yet nutrition in this group has been largely overlooked in global nutrition policy research [10].

Pork is one of the most widely consumed meats in the world, accounting for over a third of total global meat production [12]. In the US, pork ranks third in annual meat consumption after beef and chicken, and is about 25% of overall meat intake [13]. Approximately 52% American children and 59% American adults are pork consumers with a daily intake of 47 and 61 g pork, respectively [14]. Pork is an important source of high-quality protein and several priority micronutrients (Table 1) [14-16]. As reported in cross-sectional studies, intake of pork has been found to contribute significantly (more than 10%) to intakes of several nutrients, including protein, phosphorus, potassium, selenium, thiamine, riboflavin, niacin, vitamin B₆, and vitamin B₁₂ [17-19], and was associated with higher intakes and adequacies for several key micronutrients, including many under-consumed nutrients in children (age 2-18 years) and adults (age 19+ years) [14]. In a dietary modeling study using the USDA’s Healthy Dietary Patterns, removal of a serving of meat including pork was associated with a substantial decrease in several important nutrients including protein, iron, phosphorus, potassium, zinc, selenium, thiamine, riboflavin, niacin, vitamin B₆, vitamin B₁₂, and choline [20]. While the studies above have looked at the association of pork intake with nutrient intake and nutrient adequacy, none specifically examined adolescents (age 9-18 years).

Table 1: Nutrient composition of Pork* [14-16].

We hypothesized that since adolescents have higher nutrient requirements but have suboptimal intakes of several nutrients, intake of pork as nutrient rich source of a number of key nutrients would be associated with improved nutrient intakes and nutrient adequacy among consumers compared to non-consumers.

Therefore, the purpose of this study was to evaluate association of pork consumption with nutrient intake and the % below EAR/above AI specifically in adolescents using National Health and Nutrition Examination Survey (NHANES) 2011–2018 data [21], a robust and validated database/program of Centers for Disease Control and Prevention (CDC) that aims to assess the overall nutrition and health status of the American population. We also stratified the data by gender and age (9-13 years for young adolescents and 14-18 years for older adolescents) as these are specific age groups used for DRI and dietary guidelines [4,22].

Methods

Database: NHANES is an ongoing cross-sectional survey that uses a stratified multistage cluster sampling probability design to obtain a nationally representative non-institutionalized sample of the civilian US population. NHANES data are currently continuously collected and released every two years by the National Center for Health Statistics of the CDC. A detailed description of the subject recruitment, survey design, and data collection procedures are available online [21]. NHANES protocols are approved by the Ethics Review Board of National Center for Health Statistics and the present study was a secondary data analysis which lacked personal identifiers, therefore, was exempt from additional approvals by Institutional Review Boards. All participants provided a signed written informed consent. All data obtained from this study are publicly available at: http://www.cdc.gov/nchs/nhanes/.

Study Population: Data from children and adolescents aged 9-18 years (n = 6,154; population weighted N = 41,520,807) participating in NHANES cycles 2011-2012, 2013-2014, 20152016 and 2017-2018 were used. Data for those with incomplete or unreliable dietary recall as determined by NHANES staff, with missing day 1 dietary data and those pregnant and/or lactating were excluded from analyses. 

Estimates of Dietary Intake: Dietary intake data were obtained from 24-hour dietary recall interviews that were administered using an automated, multiple-pass (AMPM) method [23]. Intakes of calcium, iron, magnesium, phosphorus, potassium, selenium, sodium, zinc, vitamin A, thiamin, riboflavin, niacin, folate, vitamin B₆, vitamin B₁₂, vitamin C, vitamin D, vitamin E and choline from foods were obtained from the total nutrient intake files for each NHANES cycle [24]. Intakes from dietary supplement intakes were not included in the present analysis. Two days of dietary recalls were collected on most subjects; the first day dietary recall was collected in person in the mobile examination center while the second recall (3 to 10 days later) was collected via the telephone. Usual nutrient intakes and the distribution of intakes were estimated using the National Cancer Institute (NCI) method [25] and the percentage of the population below the Estimated Average Requirement (EAR) or above the Adequate Intake (AI) was determined using the cut-point method (except for iron where the probability method was used) for pork consumers and nonconsumers separately [26].

Estimates of Pork Intakes: Food and Nutrition Database for Dietary Studies (FNDDS) food codes were used to identify pork containing items [24]. Over three thousand FNDDS food codes included pork such as bologna, sausages, ham, chops, roasts, bacon, salami, hot dogs, scrapple, specific pork cuts, steaks, ground pork, kabob, and in numerous mixed dishes. When pork items were used as “ingredients” of the survey foods, the FNDDS food codes were identified, and recipe calculations were performed using the survey-specific USDA Food Patterns Equivalents database (FPED) which also includes the Food Patterns Equivalents Ingredient Database (FPID) [27]. The FPID descriptions were examined to determine proportion of pork: 100% if entirely pork, 50% or 33% if the description indicated one or two other meat types in addition to pork. For some FNDDS food codes that contained ingredients with missing FPID the food code ingredient profile was modified either by using food code from another NHANES cycle or by using another ingredient code with a similar description. With pork content of pork containing food codes identified, pork intake was summed across all sources of pork consumed during the recall days. Consumers of pork were defined as those individuals consuming any amount of any pork item on either of the two days of dietary recall and those who did not consume any pork on either of the two days of dietary recalls were defined as non-consumers.

Statistics: All analyses were performed using SAS 9.4 (SAS Institute, Cary, NC, USA) software and the data were adjusted for the complex sampling design of NHANES, using appropriate survey weights, strata, and primary sampling units. Data were analyzed separately for those aged 9-18, 9-13 and 14-18 years for sexes combined and for males and females aged 9-18 years aligning with age groups defined by DGA. Data are presented as mean ± standard error of means. Differences in demographics between consumers and non-consumers were determined through regression analyses. Differences in nutrient intakes and the % below EAR/above AI were determined using Z-statistics. For presentation purposes the percentage difference in nutrient intakes between consumers and non-consumers were calculated; additionally, we present the differences in % below the EAR/above AI as percentage unit differences (% units).

Results

About 53% of adolescents aged 9-18 years were consumers of pork. There were no overall differences (P>0.05) in demographic characteristics of consumers and non-consumers except that a greater percentage (P<0.05) of pork consumers were male (5.2% units more) and current smokers (1.3% units more) compared to non-consumers (Table 2).

Table 2: Demographics associated with pork consumption in adolescents aged 9–18 years.

The mean intake of pork was 53.6 ± 2.9 g/day (32.9 ± 1.4 and 131 ± 8 g/day for the 50^th and 90^th percentile of intakes, respectively) among consumers. Mean per capita intake of total pork intake was 19.6 ± 1.2 g/d while fresh pork intake was 6.39± 0.57 g/d and processed pork intake was 13.2 ± 0.9 g/d. Pork intake has not changed over the last 18 years (β = -0.44 ± 0.23 g/cycle; P_linear cycle trend = 0.0536). Pork consumers compared to non-consumers had 10% higher intakes of energy, 17% higher intakes of protein, 6% higher intake of carbohydrate, 14% higher intakes of fat, 14% higher intakes of saturated fat and 4% higher intake of percent calories from saturated fat (Table 3).

Table 3: Intake of energy, macronutrients and diet quality among adolescents aged 9–18 years non-consumers and consumers of pork.

Adolescent (age 9-18 years) consumers of pork had ≥10% higher (P<0.05) usual intakes of  copper, phosphorus, selenium, zinc, thiamine, niacin, vitamin B₆, vitamin B₁₂, vitamin D, potassium and choline; in addition, pork consumers had a 5% (but <10%) higher intake of calcium, iron, magnesium and riboflavin (Table 4). A lower proportion (P<0.05) of pork consumers had intakes below EAR  for calcium (-9% units), copper (-7% units), iron (-3% units), magnesium (-6% units), phosphorus (-16% units), zinc (-13% units), thiamine (-5% units), riboflavin (-3% units) and vitamin B₁₂ (-3% units), and higher proportion (P<0.05) were above AI for potassium (10% units) and choline (5% units) than non-consumers (Table 4). However, pork consumers also had 17% higher (P<0.05) intakes of sodium than non-consumers while virtually all of adolescent population, irrespective of their pork consumption, had sodium intakes above the AI (Table 4).

Table 4: Usual nutrient intakes and percentage of population below EAR or above AI among adolescents aged 9-18 years non-consumers and consumers of pork.

When we stratified data for adolescents age 9-18 years by gender, both adolescent male (M) and female (F) pork consumers had ≥10% higher (P<0.05) intakes of phosphorus, selenium, zinc, thiamine, sodium and choline (Table 5). In addition, adolescent male and female pork consumers had ≥5% higher intakes of calcium, copper, magnesium, riboflavin, niacin, vitamin B₆, and potassium. A lower (P<0.05) proportion of both adolescent male (M) and female (F) pork consumers had intakes below EAR  for copper (-5% units M, -8% units F), phosphorus (-10% units M, -18% units F), zinc (-9% units M, -17% units F) and riboflavin (-2% units M, -4% units F); and a higher proportion (P<0.05) were above AI for potassium (8% units M, 11% units F) and choline (6% units M, 4% units F) compared to respective non-consumers (Table 5). Female adolescent consumers additionally had higher (P<0.05) intakes of iron (7%), vitamin A (11%), vitamin B₁₂ (15%) and vitamin D (17%); and a lower (P<0.05) proportion had intakes below EAR for iron (-5% units), magnesium (-7% units), vitamin A (-9% units), thiamine (-6% units) and vitamin B₁₂ (-4% units); and a higher proportion (P<0.05) were above AI for sodium (1% units). A lower (P<0.05) proportion (-9% units) of male consumers were also below EAR for calcium (Table 5).

Table 5: Usual nutrient intakes and percentage of population below EAR or above AI among adolescents aged 9-18 years non-consumers and consumers of pork by gender.

When we stratified results for adolescents by age groups, pork consumers of both adolescents aged 9-13 years (YA) and 1418 years (OA) had ≥ 10% higher (P<0.05) intakes of  copper, phosphorus, selenium, zinc, thiamine, niacin, vitamin B₆, potassium, sodium and choline. (Table 6). In addition, pork consumers of both adolescents aged 9-13 years and 14-18 years had ≥ 5% higher (P<0.05) intakes of calcium, magnesium, riboflavin, and vitamin B₁₂. A lower (P<0.05) proportion of adolescent pork consumers (both YA and OA) were below EAR for calcium (-10% units YA, -9% units OA), copper (-4% units YA, -11% units OA), iron (-6% units OA), magnesium (-10% units YA), phosphorus (-15% units YA, -16% units OA), zinc (-12% units YA, -15% units OA), vitamin A (-8% units YA), thiamine (-8% units OA), riboflavin (-5% units OA) and vitamin B₁₂ (-4% units OA); and a higher proportion (P<0.05) were above AI for potassium (12% units YA, 8% units OA), choline (9% units YA) and sodium (1% units OA), compared to respective non-consumers (Table 6).

Table 6: Usual nutrient intakes and percentage of population below EAR or above AI among adolescent non-consumers and consumers of pork by age groups.