May 2020 Issue

CPE Monthly: Offal — Health Benefits of Organ Meat
By Ellen Ratliff, MS, RD
Today’s Dietitian
Vol. 22, No. 5, P. 44

Suggested CDR Learning Codes: 2020, 4063, 6030
Suggested CDR Performance Indicators: 8.3.6, 8.4.4, 9.3.3
CPE Level 2

Take this course and earn 2 CEUs on our Continuing Education Learning Library

Offal, more commonly known as organ meats or variety meats, refers to “the internal organs and entrails of a butchered animal, excluding muscle and bone.” This definition doesn’t specify particular organs or animal parts, as what’s considered edible varies by culture and region. However, offal generally is considered to include animal blood, bones and marrow, brain, chitterlings and intestine, fats and other trimmings, testicles, head meat, heart, kidneys, lips, liver, spleen, skin, thymus, pancreas, tail, tongue, and stomach.1 The consumption of offal is considered taboo in some cultures and highly valued in others.

Many are familiar with offal in the form of gourmet products such as foie gras (ie, duck or goose liver), pâté (ie, a paste, pie, or loaf that may contain liver), and sweetbread (ie, thymus or pancreas, most commonly from veal or lamb but also from beef or pork).

Many regions of the world have their own offal specialties. Scotland offers haggis (ie, sheep or calf heart, liver, and lungs mixed with suet, oatmeal, and seasonings boiled in a bag made from the animal’s stomach). Chopped liver is a dish in Jewish cultures; chitterlings/chitlins (ie, boiled and fried pig intestine) are popular in the southern United States, and Mexico makes menudo (ie, beef stomach or tripe).

Offal isn’t particularly popular in the United States, where it’s consumed mostly in the casings of sausages and hot dogs, traditionally made from intestines. For comparison, the top five consumers of offal in the world (in kilograms per capita) are Hong Kong, China (26.77); Mongolia (10.34); Serbia (9.41); Australia (7.96); and Belarus (7.77).2

This continuing education course examines current offal usage in the United States and internationally and examines benefits of, considerations for, and barriers to use in the US food market. It also offers recommendations for how RDs can apply this information to public health and private nutrition settings.

Organ meats have been a part of the human diet since the birth of cooking, which allowed otherwise indigestible animal parts to become edible and deliver a multitude of nutrients found in considerably higher amounts than in muscle tissue.

In more recent history, in the United States during World War II, former US President and US Food Administration Leader Herbert Hoover wrote in the magazine What’s New in Foods and Nutrition about the state of the American meat supply. Meat was considered as important to the war “as are tanks and aeroplanes.”3 The slogan “Food will win the war” was pioneered, and Meatless Mondays were started in an attempt to conserve resources as growing amounts of beef and pork, as well as butter and cheese, were shipped overseas to feed both American and Allied troops. With more meat heading overseas, rationing was instituted at home and smaller portions were seen on the plates of American households.

At the same time, meat was considered a staple in the American diet. Beef was especially valued, and its reduced presence left many with the feeling of not having had a proper meal, per some reports.3 With meat rationing, a black market developed in the meat trade, supplying rationed goods at exorbitant prices.

In 1940, the National Research Council assembled the Committee on Food Habits, led by anthropologist Margaret Mead, to examine American eating habits and their influences. The goal was to devise a way to persuade Americans to part with their favored cuts of meat in exchange for the parts often left on the slaughterhouse floor—hearts, livers, kidneys, and other organs.

Mead and the committee believed that to find the best way to encourage the public to eat organ meats, they first had to find out why they weren’t being used. Food and cultural identity are deeply intertwined, and most every culture in the world has at least some classical flavors or dishes unique to the population.

At the time, there was a socioeconomic stigma attached to organ meat consumption. Many Americans believed that organ meats were for the rural poor—and it was true that the rural poor did eat more organ meats than their urban- and suburban-dwelling peers. This stigma likely had a racial component as well. For example, chitterlings (“chitlins”), made from pork intestines, became a staple in the diets of African Americans during slavery, while wealthier, white slave owners dined on the choice hog meat.4

To help overcome the stigma associated with organ meat consumption, the committee encouraged the use of the term “variety meats” over “organ meats” and urged homemakers to incorporate them into meal planning to add variety to the diet. Fewer ration points were required for variety meats than for more premium cuts, making them a more economically sound choice.

Another reason Americans seldom ate organ meat was that they were largely unfamiliar with it. The population wasn’t accustomed to eating it and generally didn’t know what it tasted like or how to prepare it. The committee believed it could remedy this quickly by familiarizing homemakers with the nutritional value of organ meats and by publishing recipes through the popular press, recommending that the fullest possible use be made of leaflets, booklets, posters, and nutrition films to spread its message.5

Over time, community groups held cooking classes to help consumers learn to cook with organ meats, publishers released cookbooks, and the stigma began to fade. The process, however, was too slow, and the war came to an end before lasting changes could take place. Americans soon replaced their chopped liver with pork chops and once again turned up their noses at the “good, abundant, highly nutritious” organ meats, as promoted in a 1943 Life magazine article.6

Current Trends
Because the definition of offal varies across cultures, it’s difficult to accurately estimate consumption levels. Offal sometimes is included with muscle meat in national production and consumption statistics. Red meat typically is considered the muscle and edible offal of cattle, sheep, deer, goats, and, sometimes, pigs. However, what qualifies as “edible” varies in different regions of the globe.

According to 2013 figures from the Food and Agriculture Organization of the United Nations, the United States ranks 171st in the world (out of 175 countries), with about 0.44 kg (0.97 lbs) of offal consumed per capita, primarily from sausages and hot dogs.2

State and federal agencies contribute billions of dollars each year in subsidies to the meat industry that help maintain meat at a relatively stable and affordable rate. With such a large meat market, but such a small offal market, the United States exports significant amounts of unwanted animal organs, with about 150,000 tons of cow offal sent overseas in the first half of 2016 alone.7

One group that supports consumption of organ meat is the Paleo diet community, which stresses the high protein content and nutrient density offal offers. For example, in her book Paleo Principles, Sarah Ballantyne, PhD, recommends eating organ meat (preferably grass-fed) at least twice (but ideally four or five times) per week and offers several recipes and tips about how to cook offal and incorporate it more often in meals, such as meatloaf, that may be similar to what families already prepare at home.1

Paleo dieters generally eat fewer processed foods, with an emphasis on animal protein, nuts and seeds, fresh produce, and starchy tubers, although there are many types and subsets of the Paleo diet that may incorporate dairy products, vegan options, or other deviations.

Benefits of Offal
Offal is nutrient dense and contains highly bioavailable protein and a balanced profile of amino acids and micronutrients including iron, zinc, selenium, and vitamins A, D, and B12. The specific composition of the organ meat varies depending on several factors, such as animal species and composition of the animals’ feed.8 Offal tends to be higher in iron and vitamin B12 than is lean muscle meat and contains considerable amounts of essential amino and fatty acids (see table).

Click to enlarge

Alpha-Lipoic Acid
Alpha-lipoic acid (ALA) is an antioxidant and naturally occurring fatty acid that can be made in the mitochondria of the body and is found in a variety of foods including organ meats, spinach, tomato, broccoli, and yeast. Beef kidneys and hearts contain the highest amounts of ALA among animal food sources. A 100-g serving of beef kidneys contains 264 mcg lipoyllysine (the protein-bound form of ALA), the same amount as is in about 3/8 cup raw spinach.9 In nature, lipoic acid is found as lipoyllysine, but it’s not protein bound in supplements, where it’s usually found as a mix of R- and S-lipoic acids or as R-ALA on its own at various dosages. Levels in food and in the body tend to be much lower than amounts found in supplements.

Because the body can make its own ALA, there’s no recommended intake level from diet and no evidence for a specific dose. However, in research studies, standard dosages of 300 to 600 mg per day of ALA tend to be used, but larger doses of as much as 1,800 mg and even 2,400 mg have been used with low risk of toxicity and are considered relatively safe. Most commonly reported side effects were nausea, itchiness, and appetite suppression.10

CVDs, such as atherosclerosis and hypertension, can develop due to an overwhelming amount of reactive oxygen and nitrogen species causing mitochondrial damage during the aging process. ALA has been studied extensively for its role in energy metabolism and protection from mitochondrial dysfunction induced by free radicals. Although the body can produce enough ALA to scavenge reactive oxygen species and enhance antioxidants such as glutathione and vitamins C and E in younger adults, levels of ALA decline significantly with age, which may lead to endothelial dysfunction.11

Furthermore, older adults become more susceptible to age-related diseases such as Alzheimer’s and Parkinson’s as body processes slow down. Even in the absence of a neurological disease that affects brain function, most older adults experience some degree of cognitive decline, which is linked to increased oxidative stress and mitochondrial damage. ALA, as an antioxidant, has been posited to help prevent and treat cognitive decline and neurological disorders.

Few studies to date have examined the neuroprotective potential effect of ALA in humans. Animal studies have shown that ALA improves memory, and in vivo and in vitro studies have investigated ALA’s antioxidant, antiapoptotic, and anti-inflammatory properties. According to Molz and Schröder, there’s evidence that lipoic acid can reverse loss of neurotransmitters, their receptors, and their responsiveness, which could underlie why it’s been shown to have a positive effect on cognitive function.12

ALA also has been studied as a dietary supplement that can be incorporated into current pharmaceutical treatments and therapies for chronic disease. There’s good evidence supporting its benefit for diabetic neuropathy, which suggests that the strongest benefit for common complications of type 2 diabetes may derive from combining drug therapies with ALA.13

ALA also is used in carbohydrate metabolism. A 2018 meta-analysis looked at the effect of supplemental lipoic acid on glycemic control in those with insulin resistance. Lipoic acid administration was found to lower fasting blood glucose, lower fasting insulin levels, and lower hemoglobin A1c levels.14

ALA has been marketed as an over-the-counter weight loss aid to consumers for many years. There may be some truth to that claim. A 2018 meta-analysis found that supplementation of lipoic acid in those who are overweight or obese had significant, although modest, weight loss even without restricting caloric intake and the effect was greater in those with higher BMI.15

Organ meat can be rich in the mineral selenium, an essential trace element found to modify epigenetic markers. Inadequate selenium status is linked to higher mortality risk, impaired ability to fight infection, and mental decline. Higher selenium status or selenium supplementation in those who are deficient has been shown to exert antiviral effects, reduce the risk of developing signs and symptoms of autoimmune thyroid disease (such as Hashimoto’s thyroiditis or Graves’ disease), and be essential for optimal male and female reproductive health.16-18

Selenoproteins contain selenium as selenocysteine. The importance of selenium for maintaining optimal health is due in part to the functions exerted by the selenoprotein family, which includes glutathione peroxidases. Glutathione acts as an antioxidant, and selenoproteins have been found to have an important role in regulating thyroid hormone metabolism, as well as in skeletal muscle regeneration, cell maintenance, immune responses, and oxidative and calcium homeostasis.19

Much research links glutathione peroxidase-1 (GPx-1) to cancer growth and risk. In population studies, inadequate selenium intake is associated with an increased risk of developing cancer because selenium is a part of these glutathione compounds. GPx-1 activity is highly affected by selenium status. Several studies have shown decreased cancer risk following selenium supplementation, especially in those who were most deficient.20 Supplementation was shown to augment GPx-1 genetic expression (and possibly the other selenoproteins). Increasing expression of GPx-1 can decrease amounts of reactive oxygen species, resulting in preserved vascular function and reduced potential for carcinogenesis.

Seafoods, organ meats, and Brazil nuts are among the richest food sources of selenium. Muscle and organ meats have a more reliable and consistent level of selenium because of homeostatic mechanisms present in the organisms, whereas plant sources can vary widely by soil content, as is the case with nuts.21 A 100-g serving of beef liver contains 42 mcg selenium, about the same as is in four Brazil nuts.9

The Recommended Dietary Allowance of selenium ranges from 20 to 70 mcg per day depending on age, gender, and life stage. Tolerable Upper Intake Levels have been set at 400 mcg per day for adults.22

Vitamin B6
Organ meat is a good source of vitamin B6. Vitamin B6 is involved in more than 100 reactions in the body, executing myriad functions. It plays a role in cognitive development by creating neurotransmitters and helping regulate homocysteine, elevated levels of which are associated with cognitive decline and dementia. Vitamin B6 also has functions in gluconeogenesis, glycogenolysis, immune function, and hemoglobin formation.23

Vitamin B6 has been discussed as playing a direct role in CVD and high blood pressure because of its role in maintaining normal levels of homocysteine. Coronary heart disease (CHD) is one of the major causes of mortality in the world. Manylarge-scale studies, such as the Coronary Health Improvement Project, show an inverse relationship between vitamin B6 intake and CHD risk.24 Although the exact reasons for the reduced risk with increased intake are unclear, one proposed reason is that vitamin B6 can lower blood levels of homocysteine. Vitamin B6 is a required cofactor for the conversion of homocysteine to the amino acid cysteine, and elevated homocysteine levels correlate with heightened atherosclerosis risk.25

Vitamin B6 also has received attention for its role as an antioxidant and in immunomodulation and gene expression. Numerous studies implicate vitamin B6 in inflammation and inflammation-related chronic diseases such as cancer. Current evidence from population studies supports the possible role of vitamin B6 to reduce cancer risk and the bioactive form of vitamin B6, pyridoxal-5’-phosphate, as a potential biomarker for cancer screening. Systematic reviews show that high dietary intake of vitamin B6 was significantly linked to lower incidence of all cancers and especially gastrointestinal tumors.26 This association is much weaker with supplemental vitamin B6 rather than through dietary intake from food.

Vitamin B6 deficiency is the most common nutrient deficiency among Americans, affecting about 10% of the population, according to a 2012 report from the Centers for Disease Control and Prevention.27

Decreased Food Waste
Meat production is costly, and global demand has increased in recent years. The world’s total meat supply, which was 71 million tons in 1961, increased to an estimated 318 million tons in 2017.2 Per capita consumption more than doubled over that same time period and rose twice as fast in the developing world, with predictions that global consumption will again double by 2050.28

As sustainable agriculture becomes an increasingly pressing issue in food production, animals slaughtered for their more popular cuts could be put to further use by incorporating organ meats into processed foods, ingredients, and ready-to-eat meals.

Over the past decade, the trend of eating “nose to tail” to decrease food waste and make more sustainable food choices has become a movement. In general, the public is more interested in and educated about where their food comes from. Some consumers appreciate knowing that although an animal may have been killed for its meat, at least every part of the animal was used rather than having parts of it go to waste. As such, ethical eating can be broadened to include not just following a vegan diet but also responsible sourcing and efficient use of resources.

According to the USDA Food Standards and Labeling Policy of 2005, US producers can use cattle head meat and weasand (ie, gullet, throat) in foods and label them as beef.8 Likewise, per USDA regulations, hot dogs may contain as much as 85% organ meat.29

Most offal consumed in the United States is incorporated into minced beef, hot dogs, and sausages. Almost all other edible offal is exported, with as much as 60% going to Asia, where organ meat consumption is higher.8

Recently, some researchers have attempted to produce shelf-stable supplements of powdered offal in capsule form for fighting malnutrition and using powdered meat to create 3-D-printed food.30,31

The National Aeronautics and Space Administration is involved in 3-D food printing, too. In 2013, the agency awarded a contract to develop a 3-D-printed food system for astronauts. One hope is that future 3-D food prints could make processed foods more nutritious and that future printers could provide exact dosages of vitamins, supplements, drugs, and foods customized to the unique needs of each user.32

Risks and Hazards of Offal
There are possible risks and hazards to consider when making the choice of whether or not to consume offal.

Mad cow disease, also known as bovine spongiform encephalopathy (BSE), affects the brain and spinal cord of cattle. The disease can spread to humans through proteins called prions found in contaminated brains and spinal cords and cause a rare, noncontagious brain disease called variant Creutzfeldt-Jakob disease.

As of August 1997, brain meat from high-risk cattle and cattle with signs of BSE aren’t allowed to enter the United States as cattle feed, and this was extended in April 2009 to include any animal feed, including pet food. The FDA works to keep the food supply to humans safe by making sure cattle feed is safe and that cows remain healthy.30 Only four people in the United States have ever been found to be affected by BSE; they most likely became infected when living or traveling outside of the country. Likewise, just five cows in the United States have been found to have BSE, most recently in July 2013, and four of these were of an atypical type, meaning that they developed it spontaneously in later life, rather than typically (ie, by consuming contaminated feed).33

The USDA is involved with BSE prevention as well, making sure high-risk cows and cow products in the United States and from other countries aren’t used as food for people. Inspectors from the USDA’s Food Safety and Inspection Service bar from the food supply any cattle that display symptoms of neurological disease, central nervous system disorders, or other disability and prevent slaughter practices that might increase risk of disease transmission. The USDA also has a program in place to detect signs of BSE in the United States in groups where BSE is more likely to be found.34

Therefore, commercially available organ meat should be safe to eat and free of BSE if raised in the United States.

Excess Vitamin A and Iron
Pregnant women should be cautious about eating offal, as it tends to contain high amounts of vitamin A, excess amounts of which have been associated with birth defects and abnormalities of the eyes, skull, lungs, and heart. The National Institutes of Health has recommended a Tolerable Upper Intake Level of 10,000 IU per day for all adults.35 For reference, 3 oz of beef liver contains about 22,000 IU.9

A common misconception about liver consumption is that the liver acts as a processing and storage site for toxins.

The liver, however, is more of a filter than it is a sponge. Its job is to process and convert potentially toxic byproducts into more water-soluble forms that can be excreted. It doesn’t store them indefinitely; rather, it stores a variety of nutrients that helps it perform its duties, such as detoxification. These nutrients include vitamin B12; the fat-soluble vitamins A, D, and K; and minerals such as iron and copper.1

So, while clients may be worried about ingestion of toxins when consuming liver, the biggest risk comes from consuming potentially excessive amounts of vitamin A, or possibly iron in those who have an iron overload disorder such as hemochromatosis, in which excess iron is stored in the body’s organs. Too much iron can lead to liver disease, heart problems, and diabetes. Those with hemochromatosis should reduce but not entirely avoid consumption of red meat (and organ meats).

In the body, most vitamin A is kept in the form of retinyl esters, but the body can’t use these esters until they’re broken down into all-trans-retinol, bound to retinol-binding proteins, and enter the bloodstream.36 Excessive intakes of preformed vitamin A can be deadly or lead to less serious side effects such as nausea, anorexia, hair loss, and dry skin. For a generally healthy person worried about excessive vitamin A consumption from organ meats, they should make sure that a variety of organs are consumed and try to keep portion size in mind. Blending liver with other organs or with ground muscle meat also will lower overall vitamin A intake per portion.

Gout is a common type of arthritis caused by high levels of uric acid in the blood, which can cause joints to become swollen and painful. Purines in the diet form uric acid in the body. Patients diagnosed with gout often are advised to moderate their intake of purine-rich foods, such as alcohol, seafood, dairy, and red meat.37 Organ meat, which is high in purines, may still be consumed, but in restricted portions. Individuals with gout should limit consumption of fish, meat, and poultry to 4 to 6 oz (114 to 170 g) per day. Organ meats would be included in this category. Similar amounts of purines are found in organ meat and muscle meat. Beef intestine contains 88 mg purines per 100 g, compared with 90 mg in sirloin. Pork heart contains 119 mg, compared with 120 mg in pork tenderloin.38

Influence on Cholesterol
Organ meat contains more cholesterol than does muscle meat. Four ounces (113 g) of raw beef liver contains 311 mg cholesterol, while beef kidney contains 464 mg and beef brain contains 3,401 mg. By comparison, 4 oz of ground beef contains only 68 to 88 mg.9

Despite the fact the 2015–2020 Dietary Guidelines for Americans no longer recommend limiting dietary cholesterol, many health care providers continue to advise patients to limit their intake of cholesterol. Thus, many may be reluctant to consume organ meat.39

Putting It Into Practice
Organ meats can be a healthful addition for anyone looking to add more variety to the flavor and nutrient content of their diets. They’re at least as affordable as muscle meat and can contain beneficial nutrients, such as protein, essential fatty acids, vitamin B6, vitamin B12, iron, and selenium, in equal or greater amounts than their muscle-based cousins.

Organ meats’ strong and unique flavors can be a hurdle for some clients, so RDs might advise those who want to incorporate them in their diet to start with more mildly flavored offal, such as tongue and heart, to help them adjust to its unfamiliar flavors. They also can combine organ meat with ground beef or pork, grinding liver and kidneys to include in a meat sauce. RDs also might recommend cookbooks to help clients learn how to prepare organ meats, including Odd Bits: How to Cook the Rest of the Animal by Jennifer McLagan and The Whole Beast: Nose to Tail Eating by Fergus Henderson.

On her blog, The Paleo Mom, Ballantyne offers tips on how to increase offal consumption.40 She explains that the flavor of ground beef heart is similar to that of ground beef and can be used in place of ground beef in any recipe. Liver, which has a stronger flavor, can be ground and mixed with other ground meats to help dilute its potent taste. Bone broth also is considered offal and can be used in soups or as the cooking liquid for rice or other grains. While there are no scientific studies that support the commonly purported medical benefits of bone broth, its consumption does support the nose-to-tail movement. Pork rinds, which are sold in convenience stores and supermarkets, are offal as well, and many clients likely are familiar with pâté as part of an hors d’oeuvres tray at a party. RDs can advise clients to experiment with a variety of organs from different species, as each has its own unique flavor.

For those who want the health benefits of organ meats but don’t enjoy the taste, desiccated and encapsulated organs are available as supplements. These are sometimes more expensive than consuming whole food offal and lack the protein that its food form contains. One popular product is Beef Liver Capsules from Vital Proteins. Ancestral Supplements also offers organ supplements including liver, heart, thyroid, pancreas, spleen, thymus, trachea, bone marrow, brain, kidney, prostate, adrenals, intestines and tripe, gallbladder, and lung from grass-fed beef. Consumers should look for products with third-party quality testing to ensure they’re consuming a safe supplement free from contamination and has a label that accurately reflects its contents.

Nutrition professionals can make offal consumption easy by incorporating organ meats into ready-to-eat meals, combating commonly held beliefs such as socioeconomic biases and unfounded health risks, and disseminating information on the environmental and nutritional benefits of offal usage. RDs have the opportunity to help clients and patients include more of this powerhouse category of oft-neglected food into their daily lives. If your mission includes a “food first” platform, consider the humble piece of organ meat—an excellent protein rich in B vitamins; fat-soluble vitamins such as A, D, E, and K; and minerals including iron, magnesium, selenium, and zinc.

— Ellen Ratliff, MS, RD, is a Michigan-based clinical dietitian and nutrition writer.

Learning Objectives

After completing this continuing education course, nutrition professionals should be better able to:
1. Distinguish the potential benefits of organ meat consumption.
2. Assess populations for whom organ meat may not be appropriate.
3. Evaluate possible barriers to increasing organ meat consumption.

CPE Monthly Examination

1. Which of the following patients should limit their consumption of liver due to its high levels of vitamin A?
a. A 37-year-old male with gout
b. A 69-year-old female with hyperlipidemia
c. A 26-year-old female who’s 31 weeks pregnant
d. A 9-year-old male with asthma

2. What question did anthropologist Margaret Mead and the Committee on Food Habits aim to answer?
a. What were American consumers’ favorite organ meats?
b. What nutrients are organ meats rich in?
c. Why weren’t consumers eating more organ meats?
d. Why should consumers eat more organ meats?

3. According to the accompanying table, organ meats generally contain more of which nutrients?
a. Protein, iron, zinc
b. Zinc, vitamin A, vitamin D
c. Magnesium, riboflavin, vitamin A
d. Iron, riboflavin, vitamin B12

4. Research suggests that supplemental alpha-lipoic acid may be beneficial for what medical condition?
a. Diabetes
b. Irritable bowel syndrome
c. Autism
d. Depression

5. Cookbooks and cooking demos are examples of interventions that can help combat which of the following barriers to increasing organ meat consumption?
a. Racial stigma
b. Familiarity of use
c. Higher cost
d. Short supply

6. Which of the following cattle-based diseases is often cited as a major risk of consuming calf brain?
a. Scrapie
b. Avian influenza
c. Bovine spongiform encephalopathy
d. Campylobacteriosis

7. A patient with gout may need to limit organ meat consumption because offal is a source of which of the following nutrients?
a. Iron
b. Alpha-lipoic acid
c. Selenium
d. Purine

8. According to the Centers for Disease Control and Prevention, which of the following nutrients of concern is most lacking from Americans’ diets and also can be found in organ meats?
a. Vitamin B6
b. Vitamin D
c. Iodine
d. Iron

9. According to the accompanying table, organ meats contain about how much iron per equal portion of muscle meat?
a. Half as much as muscle meat.
b. As much as muscle meat.
c. Twice as much as muscle meat.
d. Organ meats don’t contain iron.

10. What region of the world consumes the most organ meat per capita?
a. Australia
b. Hong Kong, China
c. United States
d. Mongolia


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