Nutritional Effects of Removing a Serving of Meat or Poultry from Healthy Dietary Patterns—A Dietary Modeling Study

Meat and poultry are nutrient-dense sources of protein and typically are recommended as part of an overall healthy diet. The objective was to assess the nutritional impact of removing a serving of meat/poultry in Healthy Dietary Patterns (HDPs) using a similar approach to that used by the USDA for Dietary Guidelines for Americans. Composites of minimally processed and further processed meat and poultry were developed and their nutrient profiles were used to accomplish modeling by removing nutrients of each meat and poultry composite from the HDPs. The removal of a 3 oz (85 g) serving of meat or poultry resulted in decreases (10% or more from baseline) in protein and several key micronutrients including iron, phosphorus, potassium, zinc, selenium, thiamine, riboflavin, niacin, vitamin B6, vitamin B12, and choline as well as cholesterol and sodium in the HDPs, and the decreases were consistent for most nutrients with the removal of either minimally processed (fresh) or further processed meat or poultry and even after adjusting for changes in calories. In conclusion, the results of this dietary modeling study show that the removal of a meat and poultry serving from HDPs resulted in decreases in protein and several key nutrients.


Introduction
Meat, including poultry, is a major component of the US diet and is a predominant source of dietary protein [1]. Dietary Guidelines for Americans (DGA) 2020-2025 [2] and MyPlate [3] recommend the consumption of lean meat and poultry as part of an overall healthy diet. In the U.S., meat comprises a significant portion of the normal diet, contributing more than 15% to daily energy intake, 40% to daily protein intake, and 20% to daily fat intake [4], and over 70% of adults consume red meat or poultry with a mean intake of 14-15 lean oz equivalents (eq)/week [5].
Meat is a dense source of nutrients such as protein, iron, zinc, and B vitamins [6,7]. Animal-sourced protein foods, because of their higher protein quality, are more efficient sources of dietary protein than plant protein foods. Consumption of meat has been criticized from ethical, environmental, and health perspectives in scientific and popular media. However, the meat foods evaluated in these studies as well as the terminology used to describe meat foods in nutrition research has been inconsistent and varies in different studies [8,9]. Meat is generally defined as beef, veal, pork, lamb, and game meat; and poultry is defined as chicken, turkey, Cornish hens, duck, goose, quail, and pheasant (game birds) by USDA [10]. Cured meat (frankfurters, sausages, corned beef, cured ham, and luncheon meat that are made from beef, pork, or poultry) is usually considered a separate food category [10]. While red meat and processed meat have been associated with a variety of chronic diseases in observational studies [11][12][13], minimally processed meat and poultry were not associated with chronic disease risk or related mortality [14,15].
To help guide individuals in healthy eating, the USDA developed Healthy Food Patterns and released them as part of DGA 2015-2020 [16] and updated them as Healthy Dietary Patterns for release as part of DGA 2020-2025 [2]. These patterns include the characteristics of healthy eating with details on how to follow the DGA guidance within caloric needs, and these can be used by all individuals for meal planning. Three Healthy Dietary Patterns are developed: (1) The Healthy U.S.-Style Dietary Pattern (USP), which is the primary dietary pattern of the USDA based on food types and the proportions Americans typically consume; (2) The Healthy Mediterranean-Style Dietary Pattern (MSP) which more closely reflects Mediterranean-style diets that are associated with positive health outcomes in studies; and (3) the Healthy Vegetarian Dietary Pattern (VDP) to more closely reflect the eating patterns of vegetarians. These Healthy Dietary Patterns are based on the types and proportions of foods Americans of all ages, genders, races, and ethnicities typically consume, but in nutrient-dense forms, and appropriate amounts and servings of lean meat, poultry, and eggs are included as part of protein foods in USP and MSP. DGA 2020DGA -2025 also suggest that a healthy dietary pattern is associated with beneficial outcomes for all-cause mortality, cardiovascular disease, overweight and obesity, type 2 diabetes, bone health, and certain types of cancer (i.e., breast and colorectal).
However, there is a strong push among scientific advocacy groups and policy makers to limit animal-sourced food products in the diet primarily due to environmental concerns [17][18][19][20][21][22]. Therefore, the aim of this analysis was to examine the potential unintended consequences of limiting meat and poultry by modeling the effect of removing a serving of meat and poultry on nutrient profiles of the healthy dietary patterns identified in the Dietary Guidelines for Americans, 2020-2025, and to assess whether the modeled changes lead to meaningful changes in intake.

Materials and Methods
To achieve the objective of this study, four different minimally and further processed meat and poultry composites were developed using a total of 397 food codes in 10 food categories [10] using a similar modeling approach as that used by the USDA. The foods were grouped into minimally processed and further processed foods, and further into meat (beef and pork) and poultry (chicken and turkey). These groups are consistent with the meat science classification of meat products [23]. Minimally processed meat and poultry items include raw, uncooked products that have not been significantly altered compositionally and contain no added ingredients, but may have been reduced in size by fabrication, mincing, grinding, and/or a meat recovery system. Further processed meat and poultry items include those that undergo a transformation beyond minimal processing, contain approved ingredients, and may be subject to a preservation or processing step(s) including salting, curing, fermentation, thermal processing (smoking and cooking), batter/breading, or other processes to enhance sensory, quality, and safety attributes. One or two representative food codes were selected in each category, similar to the approach used by the USDA, and proportions of different foods in a category were based on their population-weighted consumptions for NHANES 2017-2018 participants (n = 7036; age 2+ years) [24]. The meat composite used in USDA's Healthy Dietary Patterns [25] was also used as an additional meat option. The following composites were developed and further details are provided in   [26]. Nutrient profile for ground beef (FDC ID 173113, Beef, ground, 97% lean meat /3% fat, patty, cooked, pan-broiled) was obtained using USDA Food Data Central [27]. Nutrient profiles for meat and poultry composites were computed by adding the nutrients of component foods in the proportions as described above and are presented in Table 2. . Dietary modeling was accomplished by removing nutrients of a 3 oz (85 g) serving of each meat and poultry composite from the Healthy Dietary Patterns (USP and MSP), and modified nutrient profiles were created using Microsoft Excel (Version 2019, Microsoft, Inc., Redmond, WA, USA). Additional modeling approaches were conducted where calories and nutrients were increased from the rest of the diet to match the baseline calories, thus providing an isocaloric removal of meat and poultry servings (i.e., showing the impact of removing meat and poultry and allowing the remaining diet to increase to meet the planned calorie level). To accomplish this, each nutrient value after removal of the meat and poultry composite was multiplied by the baseline calories and divided by the modified calories (Isocaloric nutrient value = {(baseline nutrient value − composite nutrient value) ÷ (baseline calorie value − composite calorie value)} × baseline calorie value). Basically, all the foods in the existing dietary pattern are increased proportionally to the number of calories of meat removed. A change of 10% or more in nutrients due to dietary modeling analyses of Healthy Dietary Patterns was used as an indicator of meaningful differences.

Discussion
The results of this dietary modeling analysis show that the removal of a serving of meat or poultry resulted in decreases (10% or more from baseline) in protein and several key micronutrients including iron, phosphorus, potassium, zinc, selenium, thiamine, riboflavin, niacin, vitamin B 6 , vitamin B 12 , and choline as well as cholesterol and sodium in the Healthy Dietary Patterns. It is interesting to note that the decreases were consistent for most nutrients with the removal of either minimally processed or further processed meat or poultry and even after adjusting for the decreases in calories associated with removing meat/poultry servings.
Minimally processed meat used in our study included lean beef steaks and lean pork chops; minimally processed poultry included chicken breasts, drumsticks, and turkey; further processed meat included battered/fried beef steaks, breaded pork chops, spareribs, deli ham, pork bacon, beef hot dogs, and pork sausages; and further processed poultry included grilled and rotisserie chicken breasts, chicken nuggets, deli turkey, turkey bacon, chicken hot dogs, and turkey sausages (see Table 1). Beef is a staple food in the Western diet and is an important source of high-quality protein and several key micronutrients including highly bioavailable iron, zinc, and B vitamins in the American diet [6,7,28,29]. We recently reported that beef also contributes significant amounts of several key micronutrients such as zinc, iron, vitamin B 12 , vitamin B 6 , and choline in the diets of American adults [30]. Pork is one of the most widely consumed meats in the world and accounts for over 30% of global meat production and intake. Pork is a nutrient-rich source of high-quality protein and select nutrients such as potassium, phosphorus, zinc, selenium, thiamin, riboflavin, niacin, and vitamins B 6 and B 12 [31,32]. Poultry meat is also high in protein and B-group vitamins (mainly thiamin, vitamin B 6 , and pantothenic acid), and minerals (like iron, zinc, and copper) [33,34].
In the present analysis, removal of a 3 oz (85 g) serving of minimally processed meat from the Healthy Dietary Patterns resulted in ≥10% decreases from baseline in protein, iron, phosphorus, potassium, zinc, selenium, thiamine, riboflavin, niacin, vitamin B 6 , vitamin B 12 , and choline. Similarly, removal of a 3 oz (85 g) serving of minimally processed poultry also resulted in ≥10% decreases in protein, phosphorus, selenium, niacin, vitamin B 6 and choline. Although there was a consequent small decrease in energy with the removal of meat or poultry from healthy dietary patterns, the decrease was less than 10% from baseline. Interestingly, the decreases in protein, zinc, selenium, niacin, vitamin B 6 , vitamin B 12 , and choline from the removal of meat; and protein, selenium, niacin, vitamin B 6 , and choline from the removal of poultry remained ≥10% from baseline when the decrease in energy was adjusted (isocaloric scenario) by adding back energy/nutrients from the rest of the healthy dietary pattern. This suggests that the meat and poultry are more nutrient-dense foods than other foods in the Healthy Dietary Patterns. Indeed, minimally processed meat or poultry provides about three times more protein, four times more zinc (for meat only), three to four times more selenium, three to four times more niacin, three to four times more vitamin B 6 , and two to three times more choline than Healthy Dietary Patterns on a per 100 kcal basis. However, meat and poultry also provide over four times more cholesterol, 70% more saturated fat (for meat only), and about three times more sodium.
While lean and fresh/unprocessed meat and poultry are recommended as part of healthy diets [2,3] and are not associated with adverse health outcomes [14,15], intake of processed meat has been reported to be associated with risk for several chronic disease outcomes in scientific research [11][12][13]. On a per 3 oz (85 g) serving basis, further processed meat or poultry provide more calories, less protein and other key micronutrients, and more saturated fat and sodium than their minimally processed counterparts. DGA 2020-2025 has identified saturated fat and sodium as nutrients to limit, as their current intake is more than recommended based on their suspected role in chronic disease outcomes [2]. Additionally, heme iron, N-nitroso compounds in processed meat, as well as heterocyclic aromatic amines and polycyclic aromatic hydrocarbons formed during high-temperature processing are also considered, by some, as potential carcinogens in processed meat [35]. However, the removal of further processed meat and poultry such as ground beef, fried steaks, pork chops, spareribs, chicken nuggets, cold cuts, bacon, frankfurters, and sausages, also resulted in ≥10% decreases in protein, selenium, and choline. In a recently published analysis of NHANES 2001-2018, we reported that beef including processed and ground beef contributed to the intake of protein and several key micronutrients [30]. In an earlier analysis of NHANES, intake of lunch meat (deli, cold cuts, or cured meat) did not adversely affect diet quality or physiological parameters in children and adults [36]. Although there is some evidence that high meat consumption (especially red and processed meat) may increase the risk for some types of chronic disease [37], meat (fresh and lean meat) can be an important source of nutrients, especially for people with limited availability of foods.
There has been a consistent ongoing discussion and increasing concerns about the environmental impact of animal-sourced foods and policymakers are increasingly concerned with the environmental consequences of meat consumption in addition to the effect on human health. Some studies show that meat production results in anthropogenic greenhouse gas emissions including CO 2 , methane, and nitrous oxide and is the single most important source of methane [17,18]. Consequently, there has been a strong push to limit or eliminate animal-based foods to minimize environmental impacts [19][20][21][22]. However, such recommendations do not account for their potential effect on food availability and nutrient intake. While removing or limiting animal foods from the diet may help lower greenhouse gas emissions, nutritional inadequacies may occur as potential trade-offs. Thus, recommending limiting animal-sourced foods could have potential unintended consequences [38][39][40]. Our results clearly show that the removal of a serving of meat or poultry could cause decreases in protein and several key nutrients in the Healthy Dietary Patterns.
While we used USDA's dietary modeling approach for menu modeling of Healthy Dietary Patterns, there are some key aspects to consider when interpreting our results. Firstly, the representative foods for different meat or poultry composites were selected in each category using USDA's approach, and proportions of different food in a category were based on their population-weighted consumptions using the most recent nationally representative database (NHANES 2017-2018). However, our results are dependent on foods selected in our meat and poultry composites and changes in the items selected for each composite may impact modeling results. Additionally, the results presented here are based on dietary modeling to evaluate the maximum effect of removing meat and/or poultry and may not reflect actual individual dietary behavior; however, such dietary modeling offers a technique to test the potential nutritional impact of dietary guidance. Finally, our results may not apply to non-US cultures as dietary recommendations and current dietary patterns may be different.

Conclusions
In conclusion, the results of this dietary modeling study show that the removal of a meat and poultry serving from Healthy Dietary Patterns resulted in decreases in protein and several key nutrients associated with meat intake like iron, zinc, and vitamin B 12 but also phosphorus, potassium, selenium, thiamine, riboflavin, niacin, vitamin B 6 , and choline with considerable consistency in results whether removing minimally processed or further processed meat and poultry. The results also provide insight into the nutritional consequences of removing meat and poultry from Healthy Dietary Patterns and identifies nutrient amounts that may need to be replaced by other foods.
Author Contributions: S.A.: participated in project conception, research design, overall research plan, analysis and interpretation of the data, manuscript preparation; K.R.M.: reviewed and classified meat and poultry items; V.L.F.III: participated in project conception, research design, overall research plan, analysis and interpretation of the data, manuscript preparation; All authors have read and agreed to the published version of the manuscript.

Funding:
The study and the writing of the manuscript were supported by Beef Checkoff and the Foundation for Meat and Poultry Research and Education.
Institutional Review Board Statement: Not applicable.
Conflicts of Interest: S.A. as Principal of NutriScience LLC performs nutrition science consulting for various food and beverage companies and related entities; K.R.M. is an employee of Foundation for Meat and Poultry Research and Education; V.L.F.III as Senior Vice President of Nutrition Impact, LLC performs consulting and database analyses for various food and beverage companies and related entities.