Defining the Public Health Threat of Dietary Supplement Fraud

Authors


Abstract

 Adverse health events resulting from dietary supplement fraud (DSF)—fraud conducted for economic gain using dietary supplements—have received increased recognition from agencies and industry. There is a growing awareness that this issue represents a significant public health threat. With increasing consumption of supplements, there are increasing consequences—good and bad—for food science and food safety. “Dietary supplements” are a special category of food that consists of finished products (for example, a vitamin D tablet) that contain 1 or more dietary ingredients. “Dietary ingredients” are the components of those finished products (for example, vitamin D added to a food product such as breakfast cereal). Due to a number of factors, potentially harmful dietary supplements reach—and often remain—in the market. DSF is a type of product fraud, as is food fraud, which is often classified by the U.S. Food and Drug Administration as Economically Motivated Adulteration (EMA). Since the adulterants are unconventional, DSF may represent an even greater public health threat than traditional dietary supplement safety issues (though it is important to note that adulteration is only one type of fraud). Criminology concepts such as situational crime prevention and the crime triangle deepen understanding of the relationship of fraud opportunity as it relates to fraudsters and established hurdles to fraud. The purpose of this research is to provide a comprehensive overview on the public health threat of DSF, and to focus on altering current intervention and response-based approaches that are prevention-based.

Practical Application

 Dietary supplement fraud, including the more defined subcategory of economically motivated adulteration, is a food protection threat that has not been defined or holistically addressed. One autonomous food protection category is food defense—protection from attack—which became a public and private priority after the terrorist attacks of September 11, 2001. There is growing awareness that attacks for economic gain is growing in awareness and regulatory focus to the point that product fraud may also become an autonomous concept. This research establishes a starting point for defining dietary supplement fraud and identifying the public health risks.

Introduction

This dietary supplement fraud (DSF) research builds on the food fraud research that has been conducted over the last 2 y (Spink and Moyer 2011, 2012; Moore and others 2012; Spink and others, Unpublished Report; Spink and Fejes 2012). DSF is fraud conducted for economic gain using dietary supplements. With more people consuming more supplements, there are growing consequences—good and bad—for food science and food safety. The European Union (EU) considers dietary supplements to be “food supplements.” The U.S. Food and Drug Administration (FDA) defines dietary supplements as a specific category of product separate from food or food additives and it is important to consider these together since they can interact, sometimes with drug-like effects, within the human body. “Dietary supplements” are a special category of food that consists of finished products (such as a vitamin D tablet) that contain one or more dietary ingredients. “Dietary ingredients” are the components of those finished products (for example, vitamin D added to products such as breakfast cereal). An important first step is defining the threat before evaluating scope, scale, detection methods, or even countermeasures (Spink 2012). The focus of this article is to provide insight into one aspect of the growing global and U.S. product fraud threat that is gaining attention from the Global Food Safety Initiative (GFSI), U.S. Pharmacopeia/Food Chemicals Codex, various World Health Organization (WHO) activities, International Standards Organization, the U.K. Food Standards Organization's Food Fraud Task Force, and the U.S. Food and Drug Administration. While existing product fraud initiatives have focused on food and drugs, little attention has been devoted to defining the public health threat of DSF or the steps needed to take a proactive approach toward prevention.

As with other types of product fraud, the methods to understand the threat, scope, and scale are just beginning to be defined. While current regulations target adulteration, stolen goods, or intellectual property rights violations, few integrated laws or regulations covering all types of product fraud exist (Fortin 2011). The behavioral sciences and criminology concepts have been applied in order to enhance understanding of the problem and encourage the seeking of countermeasures that not only detect, but also deter—strategically applying actions to detect and deter lead to prevention (Spink 2011).

The concept of food fraud has been characterized as “the deliberate and intentional substitution, addition, tampering, or misrepresentation of food, food ingredients, or food packaging; or false or misleading statements made about a product, for economic gain.” As an economically motivated, intentional act that can lead to adverse public health consequences such as food adulteration, food fraud may be considered more risky than traditional food safety threats because the contaminants are often unconventional (Spink and Moyer 2011). As awareness of food fraud and countermeasures continue to spread within industry and the regulatory arena, so does the need for a deeper exploration of related issues of concern.

The public health threat of DSF, a close cousin of food fraud, has not yet been defined. DSF increasingly has the potential to impact food safety since more and more food products include dietary supplements as ingredients and the use of supplements continues to increase. Consumers spend over $20 billion each year on dietary supplements. From 2004 to 2007, the dietary supplement industry grew from $22.5 billion to $23.7 billion (Natural Products Foundation 2012). The increasing popularity of dietary supplements emphasizes the increasing need to examine its association with fraud. As with food fraud, DSF is economically motivated, intentional, and has the potential to cause harm. DSF often begins with ingredient fraud, and then affects finished products that are adulterated and/or bear labels that cause the products to be misbranded. The impact of DSF on industry can be expensive, on regulatory agencies, frustrating, and on consumers, risky to dangerous.

Although many dietary supplements have a long history of providing good to exceptional health benefits for those who use them, some dietary supplements provide no health benefit at all. Furthermore, dangerous public health consequences associated with some dietary supplements have been well documented and will be discussed below. Traditionally, methods to combat DSF have focused on reactive, not proactive approaches. Reactive approaches, combined with a lack of understanding regarding DSF and the associated public health consequences, magnify the threat and make DSF all the more challenging to prevent. Like food fraud, DSF prevention is extremely interdisciplinary and as such, requires interagency, multidisciplinary approaches to increase effectiveness and minimize public health harm (Spink 2009).

This research is intended to define the public health threat of DSF, regulatory challenges, and the need for a cooperative strategy to move from an intervention and response approach toward a prevention-based approach. A thorough literature review of academic, industry, and government resources was conducted to support this research. This article is the first holistic, all-encompassing, interdisciplinary study on DSF.

Background

A notable large-scale incident of adverse public health events caused by dietary supplement use occurred in 1989 when an association between dietary supplements containing of L-tryptophan and an outbreak of Eosinophilia Myalgia Syndrome emerged. The Centers for Disease Control and Prevention (CDC) estimated that over 1500 people who had consumed the supplements subsequently experienced fatigue, shortness of breath, and other health effects. The CDC confirmed 38 deaths as a direct result of L-tryptophan consumption (FDA 2012e). Evidence revealed that the manufacturing company had taken cost-cutting shortcuts in the purification process. Work with genetically engineered bacteria had produced contaminated batches of L-tryptophan. Products made with the contaminated batches entered the market, and many people who used them experienced incurable, debilitating health effects. As a result of the outbreak, the U.S. Food and Drug Administration (FDA) banned over-the-counter sales of L-tryptophan in 1990 (NEMSN 2011).

In 2004, the FDA also issued a ban on dietary supplements with ephedrine alkaloid ingredients. One such supplement included the weight loss product marketed as Ephedra, which contained the active ingredient ephedrine. Ephedrine was associated with “an unreasonable risk of illness or injury” such as heart attacks and strokes (Nelson 2004). Ephedra caused adverse health effects in 155 individuals, and infamously contributed to the death of baseball athlete Steve Bechler (Nelson 2004). There is some speculation that ephedra-containing products were also involved in the sudden death of football player Korey Stringer in 2001 (Olney 2003). The manufacturer, Metabolife International, denied knowledge of any customer complaints regarding adverse health events. However, in 2007, it was revealed that the firm had deliberately concealed over 10000 adverse health complaints while they continued to market the product (Nelson 2004). These 2 major incidents emphasize the grave public health consequences that can occur as a direct result of marketing fraudulent dietary supplements.

Defining dietary supplements

Walmart is one major retailer that markets dietary supplements via the Internet. Their website makes it easy on consumers by categorizing products into multivitamins, vitamins A-Z, supplements, herbals, fish oils, weight loss supplements, glucose supplements, sports and performance supplements, bone and joint supplements, and minerals. Consumers may select a category from this virtual library or they can browse a list of “top trends in vitamins and supplements” (Walmart Stores Incorporated 2013). Other major retailers also offer consumers numerous categories of supplements for a range of health-related conditions, but the line between “dietary supplement” and “drug” can blur for uninformed consumers around the world.

The Codex Alimentarius Commission offers a definition of dietary supplements in its “Guidelines for Vitamin and Mineral Supplements.” The Guidelines, which are voluntary for all member states, indicate that:

Vitamin and mineral food supplements for the purpose of these guidelines derive their nutritional relevance primarily from the minerals and/or vitamins they contain. Vitamin and mineral food supplements are sources in concentrated forms of those nutrients alone or in combinations, marketed in forms such as capsules, tablets, powders, solutions, etc., that are designed to be taken in measured small-unit quantities but are not in a conventional food form and whose purpose is to supplement the intake of vitamins and/or minerals from the normal diet (CODEX 2005, 2007).

The Guidelines recommend further that all supplements contain ingredients that have been scientifically tested for purity, and should take into account standards set by the WHO and international pharmacopeias. Labeling guidelines specify that a supplement package should contain: (CODEX 2005, 2007)

  1. a list of ingredients expressed as percent values;
  2. an indication of the product's intended use;
  3. a warning to the consumer not to exceed the recommended value;
  4. a statement that the supplement should not replace regular food and meals;
  5. a statement that the product should be kept out of the reach of children.

In the EU, regulations focus on the safety and proper labeling of dietary supplements, which are considered foods and referred to as “food supplements.” When compared to the U.S. regulatory definition of “dietary supplement,” the EU refers to the exact same type of product, but simply utilizes slightly different terminology. Directive 2002/46/EC is the regulation that governs food supplements containing vitamins and minerals (EU 2002). The Directive establishes labeling requirements and maximum and minimum levels of ingredients added to food supplements. It also includes vitamin and mineral substances that are legally permitted additives based upon scientific credibility. If a substance is not included in this list, a manufacturer may apply for approval directly to the European Commission's European Food Safety Authority (EFSA) (EFSA 2012). The Federal Food, Drug, and Cosmetic Act (FD&C Act) defines a drug as, “articles intended for use in the diagnosis, cure, mitigation, treatment, or prevention of disease” and “articles (other than food) intended to affect the structure or any function of the body of man or other animals” (FDA 2002b). A dietary supplement, according to section 201(ff) is “a product taken by mouth that contains a dietary ingredient intended to supplement the diet” (FDA 2012b). The dietary ingredients in dietary supplements may include: vitamins, minerals, herbs, or other botanicals, amino acids, and substances such as enzymes, organ tissues, glandulars, and metabolites” (FDA 2012b). FDA requires preapproval of drugs before they reach the market via the New Drug Application (NDA) process or fulfilling the requirements of a “monograph” for a certain category of drugs. These monographs require over the counter drug ingredients to qualify as generally recognized as safe and effective, and not misbranded. Some OTC drugs are permitted to remain on the market pending an NDA approval until a monograph for its class of drugs is incorporated into regulation. If the intended use of the product qualifies it as a drug, it must comply with all drug-related requirements (FDA 2002b). FDA's labeling guidance webpage displays 16 titles of separate guidance documents that outline requirements for drugs. The titles include specifications for noncontraceptive estrogen drugs, discontinued labeling for listed drugs, geriatric drugs, topical acne drug products for over the counter human use, and “warnings and precautions, contraindications, and boxed warning section of labeling,” for example (FDA 2011b). In essence, drug preapproval and labeling is extremely strict and extremely complex. Likewise, the FDA's Dietary Supplement Labeling Guide explains dietary supplement labeling regulations. In general, a dietary supplement label must display (FDA 2005a):

  1. statement of identity (name of the dietary supplement),
  2. net quantity of contents (amount of the dietary supplement),
  3. nutrition labeling,
  4. ingredient list,
  5. name and place of business of the manufacturer, packer, or distributor.

Labeling laws become very specific regarding claims that describe a relationship between the product and a disease or a health-related condition. A health claim is associated with the effect a product has on the risk or prevention of a disease, such as “calcium may reduce the risk of osteoporosis,” and must be approved by FDA prior to use. A more general structure/function claim does not reference any disease, but characterizes the product and its intention regarding the structure or function of the body. An example would be, “helps to maintain memory function.” These claims do not require FDA preapproval. Any structure/function claim on a dietary supplement label must be accompanied by the word-for-word disclaimer, “this statement has not been evaluated by the Food and Drug Administration. This product is not intended to diagnose, treat, cure, or prevent any disease.” A manufacturer must notify FDA in writing of a structure/function claim within 30 d of marketing the product (FDA 2005b).

To further clarify the difference between a “drug” and a “dietary supplement,” it is important to note per section 201(g) of the FD&C Act, a dietary supplement is permitted to make truthful structure function claims without being considered a drug and if a label makes untruthful claims, it is not automatically considered to be a drug based on this factor only (21 USC §331 2008). The FDA has the burden to demonstrate that these claims are false or misleading. If a dietary supplement is not a drug, then no New Drug Approval (NDA) is required.

To assist industry and regulators, the U.S. Pharmacopeial Convention (USP) defines additional standards for assessing dietary supplement characteristics such as identity, strength, quality, and purity (USP 2012a). The USP standards are widely recognized as quality standards that restrict potential adulterants and contaminants in dietary supplements. In 2009, USP responded to the needs of the increasingly expanding world market for dietary supplements by publishing these standards in their documents.

The USP maintains more than 550 monographs in the DSC, and over 200 reference standards that serve as a foundation for dietary supplement manufacturing and testing. The USP also offers the USP Verified Mark, visible on more than 3 million product labels, for products that comply with the strict requirements of the USP's verification program (USP 2012b). At the USP Workshop on Intentional and Unintentional Adulteration of Food Ingredients and Dietary Supplements on September 26 to 27, 2013, in Rockville, Md., U.S.A., topics will include national and international perspectives on ingredient adulteration, establishing authenticity of dietary supplements, and current analytical approaches to detect adulteration in dietary supplements (USP 2012b).

Adulteration and misbranding

Within the Federal Food, Drug, and Cosmetic Act, the FDA defines an adulterated food as a food that “contains any poisonous or deleterious substances, such as chemical contaminants, which may ordinarily render it harmful to health” (FDA 2012c). In the FD&C Act, section 402(f), FDA specifies additional conditions that may deem a dietary supplement to be adulterated. A dietary supplement may be considered adulterated if it is or contains a dietary ingredient that may lead to “a significant or unreasonable risk of illness or injury” when utilized according to label directions or if the label lacks adequate directions for use. Additionally, a dietary supplement may be considered adulterated if it contains a dietary ingredient that has not been evaluated “to provide reasonable assurance” that indicates it does not present risk of illness or injury, it is determined to pose an imminent public health hazard, or it contains a dietary ingredient that under normal conditions of use would render it adulterated (21 USC §342 2007). Common adulterants include chemicals such as melamine, filth, and extraneous materials, and heavy metals in the form of arsenic, lead, and mercury (FDA 2012c). Heavy metals in dietary supplements are a well-known issue. One explanation is the increasing reliance on imported pharmaceutical excipients, ingredients, and dietary supplements. Until recently, no federal standards existed for permissible levels of heavy metals in dietary supplements. Also, responsibility for defining standards was at the discretion of dietary supplement manufacturers (DiStefano and Zaidi 2008).

Despite the regulations and standards, harmful levels of heavy metals such as arsenic, cadmium, lead, and mercury do occur in dietary supplements (FDA 2001a; Ergil and others 2002; Ernst 2002; Dolan and others 2003; Saper and others 2004; Levine and others 2005; Liu 2010; Mason 2010; Mandal and Mandal 2011; Micovic and others 2011; Montoro and others 2011; Posadzki and others 2012). A study published in the Journal of the American Medical Association stated that when researchers sampled commercially prepared Ayurvedic medicines obtained from websites, almost 21% contained detectable levels of lead, mercury, and/or arsenic. Several of these products manufactured in India had the potential to cause lead and/or mercury ingestions 100 to 10000 times greater than established limits (Saper and others 2008). Overexposure to mercury can cause permanent nervous system and kidney damage. Overexposure to arsenic may lead to discoloration of the skin or in extreme cases, death (OSHA 2012). Elevated blood lead levels are primarily a critical risk for young children, and can cause learning disabilities and behavioral problems (CDC 2012). Children 4 to 8 y old had the highest use of dietary supplements (48.5%) compared to other children under 18 y old, and children in families with higher incomes demonstrated higher levels of dietary supplement use (Picciano and others 2007). In sum, children taking adulterated dietary supplements contaminated with heavy metals can experience severe health effects. Misbranded dietary supplements have presented public health risks to consumers that were at least equal to, if not worse, than adulterated dietary supplements.

According to FDA, a misbranded dietary supplement bears labeling that is considered to be “false or misleading in any particular” (FDA 2012c). Examples of misbranding include labels that do not display required components in the English language, incomplete lists of ingredients, and false or misleading health claims. In 2011, federal regulators warned consumers that some dietary supplements sold online falsely claim to treat or cure sexually transmitted diseases (STDs) ranging from genital warts to HIV/AIDS (FDA 2011a). The FDA stated that only medicines available by prescription actually work for diagnosis and treatment of STDs. The FDA and Federal Trade Commission (FTC) threatened legal action for companies making and selling such products. At least 15 misbranded supplements were being sold for treatment of STDs. These federal agencies targeted specific brands such as Medavir, Herpaflor, and Viruxo. Ineffective treatments can endanger individuals taking them and also place sexual partners at risk (FDA 2011a). Some misbranding issues, such as inclusion of drug ingredients not listed on a label, represent even more serious public health issues as drug ingredients may interact with prescription medications. Furthermore, such deceptive marketing techniques used by fraudsters undercut firms that market their products legitimately.

The following example demonstrates the link between fraudulent advertising of a dietary supplement product and potential public health risk due to lack of accurate ingredient labeling. In August 2012, the U.S. District Court in Boise, Idaho, U.S.A., charged the owners of the online company Bodybuilding.com with misdemeanors for introduction and delivery for introduction of misbranded drugs into interstate commerce (DOJ 2012). The court also issued criminal fines in the amount of $8.1 million and up to 4 y probation for 2 of the 3 defendants. Court records show that the defendants admitted that they sold 5 misbranded dietary supplements that contained drug ingredients in the form of anabolic steroids. The 5 products were deemed misbranded because the firm promoted them as products intended to affect the structure or function of the body, that is, they were promoted as dietary supplement that build muscle mass (DOJ 2012).

As with U.S. consumers, increased popularity of dietary supplements among Canadian consumers has also subjected consumers to the public health risks of DSF. For example, in 2008, Canadian consumers were advised to avoid the body building dietary supplements 6-OXO (4-androstene-3,6,17-trione) and 1-AD (1-androstenediol), or any other supplements containing the ingredients 4-androstene-3,6,17-trione or 1-androstenediol. In a press release, Health Canada warned that seizures and blood clots in the brain could occur from use of these “unauthorized natural health products” (Health Canada 2008). In 2010, Health Canada warned consumers about the dietary supplement called Fat Burner nr 1, a product that was tested and found to contain 2 pharmaceutical ingredients that were not listed on the label. The ingredients included a component chemically similar to sibutramine (N,N- didesmethylsibutramine), which could no longer be legally sold in Canada due to an association with heart attacks and stroke. It also contained sildenafil, a prescription drug intended for use under medical supervision only. Sildenafil has been linked to low blood pressure and adverse cardiovascular effects (Health Canada 2010).

Popularity of dietary supplements

According to the CDC, dietary supplement use is common among adults in the United States and has increased. Approximately 40% of adults reported taking dietary supplements in 1988 to 1994. By 2006, that percentage increased to 50%. Multivitamins were the most commonly reported supplements used. A total of 61% of women aged 60 and older reported using calcium supplements. Also, use of vitamin D supplements increased for men and women in most age groups (Figure 1).

Figure 1.

Dietary supplement use in the United States has increased since the National Health and Nutrition Examination Survey (NHANES) III (1988 to 1994). Trends in the percentage of persons using dietary supplements, by gender for adults aged 20 and over: United States, 1988 to 2006 (CDC 2011b).

Note: Significant linear trend from 1988 to 1994 through years 2003 to 2006. Statistically significant difference for men compared with women for all time periods, P < 0.05 for comparison between genders within survey periods. Age adjusted by direct method to the year 2000 projected U.S. population (CDC 2011b).

The Council for Responsible Nutrition (CRN) characterized dietary supplement users as people who tend to make and maintain healthier overall lifestyle choices (including a balanced diet, routine medical care, adequate sleep, regular exercise, and healthy weight) compared to those who do not take supplements. The CRN also reported that approximately two-thirds of U.S. adults take dietary supplements for overall health and wellness or to balance nutritional deficiencies in their diets (CRN 2012). Researchers in Canada characterized supplement users and found that more females than males took supplements. They also found that the prevalence of supplement use was at its peak for women over age 50, and that increased use of supplements tended to be positively correlated with higher socioeconomic status. CRN's research results reflected similar findings on supplement use and socioeconomic status in the United States (Vatanparast and others 2010).

Supplements made from plant-derived ingredients are not unique to developed countries like the United States and Canada. Supplements have always existed as an integrated component in all countries and traditional cultures around the world, and have formed the basis for pharmaceutical preparations used today (Gurib-Fakim 2006). The WHO described the existence of such plant-derived treatments and other nondrug practices within Indian Ayurveda, Chinese and Tibetan traditional medicine, Unani, and Amazonian and African medicine systems (WHO 2007). “Traditional medicine is the sum total of knowledge, skills, and practices based on the theories, beliefs, and experiences indigenous to different cultures that are used to maintain health, as well as to prevent, diagnose, improve, or treat physical and mental illnesses,” according to WHO. It may also be referred to as “alternative medicine” or “complementary medicine” (WHO 2007). In developing countries, many people utilize traditional medicine for primary health care needs because they cannot afford to spend scarce financial resources on imported medicines. Many countries in Africa and Asia readily promote traditional medicines, which are inexpensive and locally available, within established public health programs (Gurib-Fakim 2006; Nweke and Sanders 2009). A multitude of supplements demonstrates positive health benefits that either prevent potential health conditions or assist in management of existing health conditions.

For people who do not have access to a variety of nutritional foods or fail to eat a nutritionally balanced diet on a regular basis, some dietary supplements make nutritional goals more attainable. Scientific evidence demonstrates that certain supplements demonstrate genuine health benefits and may be effective in managing some health issues. Calcium and vitamin D supplements assist in maintaining bone strength. Folic acid decreases the incidence of birth defects in newborns. Omega-3 fatty acid supplements may benefit heart disease patients (NIH 2011). Traditional and modern uses of Asian ginseng include improving the health of people recovering from an illness, boosting mental and physical performance, managing conditions such as erectile dysfunction, hepatitis C, and menopause discomfort, and moderating blood pressure. European elder tree supplements have been used for pain, swelling, infections, coughs and cold symptoms, and skin conditions. Feverfew herbs, native to Eastern Europe, have been used to relieve many conditions from insect bites to migraines, and even conditions such as toothaches. Studies have shown some promise that gingko, common in traditional Chinese medicine, can assist patients suffering from Alzheimer's disease (NIH 2008). Numerous other supplements have been used historically in traditional medicine and are still utilized today to relieve a wide range of health issues or assist in health prevention regimens.

Dietary supplement regulation

Impact of the dietary supplement and health education act (DSHEA)

FDA used to regulate dietary supplements as foods. However, the 1994 Dietary Supplement Health and Education Act (DSHEA) made dietary supplements a separate category of foods and established separate regulations for them (FDA 2012b). In actuality, DSHEA significantly weakened FDA's authority over dietary supplements and created opportunities for consumer deception, especially with regards to imported supplements. When it comes to regulatory action for dietary supplements, one article stated, “FDA can only bark, not bite” (Schardt 2003). DSHEA established that unlike prescription drugs, dietary supplements do not require premarket approval before entering the market. The Act determined that the responsibility for the safety and efficacy of products and accuracy of health claims on labels rested solely on firms, not FDA. Then, in 2007, FDA issued mandatory current good manufacturing practices (cGMPs) for dietary supplement manufacturers and distributors. The regulations emphasize dietary supplement identity, purity, quality, strength, and composition (FDA 2012b). Label information must conform to standards outlined in the FDA Final Rule 21 CFR 111, that is, all components of a label must display truthful information that is not misleading. The cGMPs became law in 2007, and require compliance for any firm (both foreign and domestic) that manufactures, labels, or holds dietary supplements intended for distribution in the U.S. market. The cGMPs also require the responsible U.S. firm to report any serious adverse events to FDA (FDA 2012a). To clarify, FDA has inspection and enforcement jurisdiction only for products manufactured in, or imported into, the United States (Zach and Bier 2009; Zach and others 2013).

In 2011, the Food Safety Modernization Act (FSMA) was signed into law. FSMA requires FDA to implement stricter regulatory procedures and enforcement policies intended to protect the safety of foods (and dietary supplements). These procedures and policies will have significant impact upon the dietary supplement industry in the United States and manufacturers and distributors that export dietary supplements to the U.S. market. FSMA outlines 2 primary areas that directly affect the dietary supplement industry. The first is that dietary supplement firms are exempt from hazard analysis and critical control requirements provided that they strictly adhere to the dietary supplement GMPs. Second, FSMA establishes new standards for new dietary ingredient (NDI) notification (Roller and others 2012).

In sum, the dietary supplement by FSMA as such (Roller and others 2012):

  1. FDA will be required to issue NDI draft guidance.
  2. FDA will have greater enforcement authority to require product recalls and suspend facility registrations; FDA will also be able to investigate and detain products.
  3. Facility registration procedures will be enhanced and FDA will have increased access to facilities and records.
  4. Specific requirements on foreign suppliers will be expanded.

Additional FSMA provisions will take years to develop into enforceable laws, but some are already in place. In 2012, FSMA required FDA to implement certain tasks such as developing guidance and rules for importers regarding foreign supplier verification, establishing an expedited review process for importers who have agreed to take part in a voluntary-qualified importer program, and notifying the industry of proposed rules regarding recordkeeping requirements for facilities that manufacture or handle “high”-risk foods. The dietary supplement industry may submit comments directly to FDA on these changes and may also communicate with government officials regarding the impact of the changes on their industry and consumers (Roller and others 2012).

However, until these changes are developed into enforceable law, within the current regulatory framework, FDA can only take action against a misbranded or adulterated product after it reaches the market. This regulatory dilemma allows such products to reach consumers and sometimes, the consequences prove to be disastrous.

Misbranding and adulteration impact Olympic athletes

“Nutrition for Athletes,” the International Olympic Committee (IOC) warns athletes that manufacturers sometimes produce dietary supplements in unhygienic conditions that lead to toxin contamination. Other supplements fail to include on the label the entire list of ingredients, preventing an athlete from knowing that a product contains banned substances missing from the label. The Commission states that the purity of dietary supplements cannot be guaranteed, and warns that some supplements can also cause athletes to fail a drug test (IOC 2003). An IOC-funded study found that some dietary supplements purchased from 13 different countries contained steroids and/or stimulant compounds prohibited by the IOC and the World Anti-Doping Agency (WADA). Of the 30 samples, 12 (40%) tested positive. Of those 12, 8 (66.7%) contained prohormones such as dehydroepiandrosterone (DHEA) and 4-androstenedione. Another 4 (33.3%) tested positive for stimulants listed as the herbal ingredients ma huang, guarana, and kola extracts, in addition to a combination of ephedrines and caffeine. The labels on 8 of the products failed to list any prohormones (van der Mewre and Grobbelaar 2004).

Labeling issues have caused some Olympic athletes to suffer the bitter repercussions of using supplements with WADA-banned substances. The Brazilian cyclist Flavia Oliveira purchased a dietary supplement called Hyperdrive 3.0 to combat fatigue caused by her asthma and allergy medications. She consequently tested positive for oxilofrine, a category of stimulants banned by WADA because they contain the drug sibutramine, an active ingredient. Months before Oliveira's test, the FDA warned the public that this product contained sibutramine, a drug ingredient known for dramatically increasing heart rate and blood pressure (USADA 2012). Despite her claim that she was unaware that the supplement contained sibutramine, Oliveira was disqualified and deemed ineligible to compete for 2 y (USADA 2010a). LaShawn Merritt, an American track and field athlete, tested positive for DHEA found in an ingestible sexual enhancement supplement called Extenz that he had purchased at a convenience store. As a result, he was ineligible to compete for 21 mo (USADA 2010b). The American swimmer Jessica Hardy tested positive for clenbuterol, an ingredient in a supplement called AdvoCare Argenine Extreme that she had used for 8 mo. Before taking the supplement, Hardy diligently reached out to the manufacturer who assured her of its purity. Despite her attempted diligence, she was deemed negligent and therefore ineligible to compete for a period of 1 y (USADA 2009).

The finest athletes in the world may lose a competition, prior medals, and points, or damage their entire career when they fail drug tests due to drug-tainted dietary supplements. Some, like the baseball athlete Steve Bechler, lost their lives. Adulterated dietary supplements, or misbranded supplements with labels that fail to describe honestly what a product contains, are not just Olympic issues though. They are an alarming global public health issue with the potential to damage the health and lives of many people around the world.

Discussion

A global issue

Despite the existence of an expansive, well-established global history of traditional medicine, the WHO asserts that “counterfeit, poor quality, or adulterated herbal products [dietary supplements] in international markets are serious safety threats.” Traditional medicine practices are widespread around the world but are not generally evaluated against any international standards or methods (WHO 2008). As such, the standards of manufacturers and distributors vary widely with respect to the quality, safety, and effectiveness of their ingredients and products.

The rapidly developing economy in Nigeria has created unprecedented opportunities for the sale of both legitimate and counterfeit medicines. Counterfeit and substandard medicines are acknowledged as a significant risk to public health (deKeiffer 2006; Liang 2006). In some areas, it is estimated that 90% of antimalarial medicines are inadequate or substandard (Spink and others, Unpublished Information). It is not known if ineffective malarial drugs cause parents to choose herbal treatments for their children, or if herbal treatments are chosen as a substitute for drugs. However, it is known that approximately 60% of children with elevated, malaria-induced fevers are treated at home with herbal medicines. A survey also found that 39% of Nigerians choose herbal medicines for cough, 62% for measles, and 38% for ear infections. In 2006, researchers tested 25 samples of Nigerian herbal remedies manufactured and sold in Nigeria. All samples contained elevated levels of heavy metals (iron, nickel, cadmium, copper, lead, selenium, and zinc) that exceeded recommended daily intake levels. Such levels were found to cause potentially harmful effects when taken as indicated. Inclusion of heavy metals in Nigerian herbal remedies could occur due to intentional addition for supposed therapeutic purposes, accidental inclusion during manufacturing with metal equipment, or polluted soil conditions (Obi and others 2006). Certain dietary supplements available for sale in Australia have demonstrated similar tendencies toward contamination with heavy metals.

Medical researchers in Australia acknowledged that lead poisoning due to Indian Ayurvedic supplements is a well-known health issue (Wijeratne and others 2010). The Australian Government's Therapeutic Goods Administration, responsible for the regulation of medicines and any products that make therapeutic health claims, warned the public about the associated risk of heavy metal poisoning due to use of Indian Ayurvedic and Chinese supplements. The report describes various reasons for the presence of heavy metals in traditional supplements, including the use of lead, mercury, and arsenic as primary ingredients. Additionally, lack of adequate sanitary controls during production can result in cross-contamination between herbal ingredients and contaminants not intended to come into contact with the ingredients (Therapeutic Goods Administration 2007). The prevalence of heavy metals in Ayurvedic supplements was examined further through a study conducted in the United States.

Researchers purchased 230 dietary supplements from websites selling Ayurvedic products and analyzed 193 of those products from 37 different manufacturers. They found that 20.7% of the supplements available for online purchase contained detectable levels of lead, mercury, and/or arsenic. Results showed that lead was the most common metal found in the samples. Three of the samples showed extremely elevated lead and mercury concentrations. Numerous supplements had the potential to cause lead and/or mercury ingestions 100 to 10000 times greater than acceptable limits. The authors noted that the practice of rasa shastra, which requires deliberate addition of metals such as cinnabar (mercuric sulfide), galena (lead sulfide), realgar (arsenic sulfide), and white arsenic (arsenic trioxide), were the likely reasons that explained the presence of heavy metals in the samples. While Ayurveda practitioners claim that properly prepared ingredients result in purified, nontoxic products, incidents of significant toxicity associated with certain Ayurvedic products have been well documented. Practitioners also believe that a long history of Ayurvedic use demonstrates proven safety and efficacy, and tend to blame irresponsible, economically focused manufacturers for their poor production methods that result in cross-contamination (Saper and others 2008). Supplements rooted in traditional Chinese medicine have also come under scrutiny for similar issues.

China is the largest producer of dietary supplements in the world, and sales have been on the rise for over 10 y in China. Expected growth of this market is estimated at 10% per year. There are approximately 3000 manufacturers of nutritional supplements in China, and 559 foreign brands of supplements are available for sale (Redfern Associates 2010). One survey found that most Chinese consumers actually prefer imported supplements over domestically produced supplements (Redfern Associates 2010). The global market for Chinese-produced dietary supplements is flourishing, but health issues associated with Chinese-made supplements have been well documented.

In 2001, the FDA warned consumers to immediately discontinue use of aristolochic acid and any products containing this herbal ingredient. FDA indicated that aristolochic acid, used in traditional medicines and dietary supplements, had caused permanent kidney damage or urinary tract cancer in several individuals. This consumer advisory was based upon knowledge that 2 individuals in the United States, 2 in the United Kingdom, and others in Belgium and France had suffered permanent kidney damage and/or disease after using supplements containing aristolochic acid (FDA 2001a). Researchers demonstrated that regular use of Chinese aristolochia herbs dramatically increased rates of renal diseases and urothelial carcinoma (Nortier and others 2000). In Belgium, 100 cases of renal disease occurred in individuals who had used weight loss supplements containing aristocholic acid. More than 70 individuals consequently required dialysis or kidney transplantation. Two individuals in the United Kingdom had also consumed similar products. Both developed end-stage renal failure requiring kidney transplants. Seven individuals in France experienced similar adverse health effects, and one developed urothelial carcinoma. Two individuals in the United States suffered end-stage renal disease from use of these products (FDA 2001b). Many harmful, even lethal, effects have occurred from the use of herbal products. Direct toxic effects of the herbs, contamination, and interactions with prescription drugs explain many of the adverse effects. Also, manufacturers may deliberately (and illegally) add heavy metals and drugs not listed on the label in order to produce specific results (Gagnier and others 2006). Deliberate addition of heavy metals and drugs to dietary supplements is considered Economically Motivated Adulteration (EMA) (Everstine and others 2013).

Defining DSF

EMA

In order to define the public health threat of DSF, it is important to consider its roots. Like food fraud, DSF is a type of EMA (FDA 2009a). While food fraud is the motivation, in the United States, the violation is often adulteration and specifically classified by FDA as EMA (though it is important to note that the fraud act may not involve adulteration) (Spink 2012). According to FDA, EMA is:

“The fraudulent, intentional substitution or addition of a substance in a product for the purpose of increasing the apparent value of the product or reducing the cost of its production, i.e., for economic gain. EMA includes dilution of products with increased quantities of an already-present substance (e.g., increasing inactive ingredients of a drug with a resulting reduction in strength of the finished product, or watering down of juice) to the extent that such dilution poses a known or possible health risk to consumers, as well as the addition or substitution of substances in order to mask dilution” (FDA 2009b).

Samples of supplements imported from China and Taiwan, in particular, have been economically adulterated in order to increase effectiveness and value. The adulterants have included drug ingredients no longer approved for human use, or drugs (that is, Cortisone or Viagra (Ergil and others 2002)) that can cause adverse reactions when taken in large amounts. Such drugs have the potential to interact with prescription drugs to produce adverse effects (FDA 2008). In 2007, FDA issued a warning to consumers and health care professionals about 6 products from China with names like Shanghai Ultra X and Strong Testis. The warning stated that the products, promoted for erectile dysfunction and sexual enhancement, were being sold as dietary supplements but contained undeclared active ingredients. FDA warned that the active ingredients had the potential to interact with nitrates found in legal prescription drugs (such as nitroglycerin) and cause blood pressure to fall to dangerous levels (FDA 2007). In order to define DSF further, it is important to define the nature of the risk.

Defining the risks

The food fraud risk concepts apply to DSF. Food fraud risks have been categorized as direct, indirect, and technical. Direct Food Fraud risks cause direct, immediate adverse health effects or fatalities. The adverse health effects of Indirect Food Fraud risks develop over time, such as long-term exposure to heavy metals. Technical Food Fraud risks may include issues of misbranding such as lack of a certain ingredient in a list of ingredients or lack of country of origin on a package. Regardless of what type of risk occurs in a food fraud or a DSF situation, the result may include adverse health events and recalled products (Spink and Moyer 2011). In order to deepen an understanding of DSF, it is important to distinguish how it differs from other related concepts.

Defining food protection

As with food fraud, the nature of DSF can be further understood through an explanation of the food protection concepts of food quality, food fraud, food safety, and food defense, which differ in terms of risk and intention. Food safety risks, to include biological contaminants such as Salmonella and Norovirus, are both unintentional and not meant to cause harm. Food quality risks are economically motivated, but as with food safety risks, public health harm is similarly unintentional. On the other hand, food defense risks, such as tampering or terrorism, are intentional and also meant to cause public health harm. Food fraud risks are also economically motivated, but the fraudster intends no public health harm. Adverse health events occur purely by accident in food fraud incidents (Spink and Moyer 2011). The Food Protection Matrix, created and published by Spink and Moyer, shows how these 4 concepts relate to each other. The Food Protection Matrix concepts have been adapted for the Dietary Supplement Protection Matrix, and are illustrated in Figure 2.

Figure 2.

Dietary supplement matrix (Spink and Moyer 2011).

Applying the concepts in the Food Risk Matrix to dietary supplements, it is important to note that specific motivations or causes, as well as effects, must be further explored. It is also important to note that the term “Dietary Supplement Defense” has not been defined in current literature. It is included here for demonstration purposes only. Table 1 explains through example the cause and effects of intentional or unintentional adulteration of a dietary supplement with lead. Table 1 is adapted from the chart “Risk Cause and Effects for the Food Disciplines” in Spink and Moyer's “Defining the Public Health Threat of Food Fraud” article that was previously published in the Journal of Food Science (Spink and Moyer 2011).

Table 1. Risk cause and effects for the food disciplines (adapted from (Spink and Moyer 2011))
  Cause and Public health 
Risk typeExamplemotivation risk typeSecondary effect
Dietary Supplement QualityAccidental inclusion of leadPoor quality controlProduct cannot be soldDietary supplement safetyReduced brand integrity or public health incident
Dietary Supplement FraudIntentional inclusion of lead to increase raw ingredient weightEconomic gainLead poisoningDietary supplement safetyPublic reaction and industry-wide lower prices of this and related products
Dietary Supplement SafetyUnintentional contamination with leadPoor sanitation during manufacturingLead poisoningDietary supplement safetyDamage to industry, recalled product, public mistrust
Dietary Supplement DefenseIntentional contamination with leadRevenge on manufacturer or brand via consumer harmLead poisoningDietary supplement defenseAdulterated product, damage to brand and industry, public mistrust

Criminology and the behavioral sciences

Before shifting focus from intervention and response to prevention, it is important to identify the root causes of DSF. They are based on an inherent fraud opportunity that is not only unique to the product and supply chain, but also to the fraudster. Each fraudster has a unique opportunity based on a particular business environment. A fraudster who is a distributor sales representative that sells directly to retailers has a different opportunity than the owner of a dietary supplement packaging manufacturing facility. A fraudster who manufactures bulk powdered active ingredients has a different fraud opportunity than a fraudster who prints packaging labels. All these details lead to an extremely complex task to try to predict the probability of DSF.

While the specific type of fraud incident may have never occurred before and may never occur again, the underlying fraud opportunities are the same. Therefore, predicting the exact type of fraud or adulterant may be almost impossible, but identifying the fraud opportunity is often very intuitive. The “bad guy” action usually makes sense from the original perspective. In criminology, this is called Rational Choice Theory. The criminal is making what they believe is a rational choice that will lead to a greater benefit than risk. Another theory that applies to understanding and reducing fraud opportunity is Situational Crime Prevention. An especially valuable tool in that theory is the crime triangle.

The use of the crime triangle allows the fraud opportunity to be deconstructed into base factors. Often, the vulnerabilities are identified only after a specific DSF incident has been identified. It cannot be underemphasized how important the rapid detection systems are to try to identify the incidents. That said, rapid detection of a near infinite number of adulterants is not efficient.

In order to be efficient, the detection and deterrence countermeasures should be combined with other business actions to reduce the fraud opportunity and support the goal of prevention. It is an important nuance, and to clarify, deterrence is a focus on persuading the criminal to not act or to change their nature, whereas prevention is more holistic and focused on the overall situation. That holistic, all-encompassing insight is complex, but possible using the crime triangle.

The crime triangle is composed of 3 legs: a victim who is cheated, a fraudster committing the act, and the guardian or hurdle gaps (see Figure 3). While there are competent guardians and hurdles, the fraudsters continue to evolve. The countermeasures are a chess match. The crime triangle was originally developed for crime but has been adapted to product fraud, and is directly applicable to DSF.

Figure 3.

The crime triangle (Spink and Moyer 2011).

Responding to DSF

As stated above, the FDA expects the dietary supplement industry to adhere to cGMPs that focus on dietary supplement identity, purity, quality, strength, and composition (FDA 2012a). The FDA also expects the industry to develop labels that display truthful information that is not misleading in any way (FDA 2012a). However, negligent or unscrupulous manufacturers and distributors skirt these requirements and cause public health harm via their fraudulent dietary supplements. Fraudulent dietary supplements, whether they are misbranded or adulterated on an intentional or unintentional basis, can and do affect public health. Additionally, such products undercut legitimate manufacturers and distributors who painstakingly follow the rules. Incidents of blatant DSF occur in the United States, and are often intimately linked to complex international distribution networks. Officials have prosecuted several cases of fraud by dietary supplement distributors in the United States, but the issue is still rampant today.

In 2009, a Michigan business owner pleaded guilty to repackaging, selling, marketing, and distributing “unapproved new drugs” and misbranded drugs over the Internet for a total profit of $11.9 million (DOJ 2009). Federal law prohibits dietary supplement labels from making drug-type health claims that purport to treat, cure, or prevent disease. Making such claims renders a product an unapproved drug under the FD&C Act. Advertising materials on the company's website stated that the products had been proven via clinical trials to effectively treat and prevent diabetes, irritable bowel syndrome, gout, high cholesterol, high blood pressure, heartburn, and diarrhea. In reality, the company had conducted no such trials. Furthermore, no experts had established the safety and effectiveness of the supplements when used according to label directions. FDA considered the dietary supplements to be new drugs, and since they did not preapprove any of the products, they were also considered unapproved drugs. In addition to using a model to pose as a doctor on the website and posting false testimonials about the products, the company used mirror image technology to disguise certain aspects of the website. FDA accessed several of the websites from a FDA network computer, but received a “sanitized” version with claims that appeared compliant. When they accessed the websites from a computer with no traceable Internet provider address, drug-type claims appeared (DOJ 2009, 2010a). It appears that the fraudsters set up their own specific websites to provide fake web content to government-located computers by identifying the users by “.gov” or other identifying details.

In 2010, a prisoner in California was serving a 10-y federal prison sentence for Medicare fraud that had earned him $14 million. While incarcerated, a court prosecuted him for distributing misbranded sexual enhancement drugs called “Vitalex.” The drugs, which masqueraded as dietary supplements intended for natural sexual enhancement, displayed labels that represented them as “herbal sexual enhancement supplements” and “all-natural” alternatives to prescription sexual enhancement drugs. The supplements contained acetildenafil, an analog of sildenafil that is used to make Viagra. Acetildenafil is an unregulated drug known to cause adverse health reactions and in some cases, death. His daughter assisted in the operation by purchasing ingredients in China and shipping them to the United States. Even after FDA seized violative products and packaging from their home, the business continued online. The man and his daughter each received charges of introducing a misbranded drug into interstate commerce. The court issued each of them a maximum 1-y prison sentence (FDA 2010a).

In 2010, officials charged a Pennsylvania woman with illegally importing 4 million weight loss pills that contained a controlled drug substance, unapproved drugs, and a possible carcinogenic ingredient. The products contained sibutramine, linked to side effects such as nausea, vomiting, increased blood pressure, heart attacks, and strokes. Many of the products she sold also included rimonabant (an unapproved drug), phenytoin (a seizure medication), and phenolphthalein (recognized as a probable carcinogen) (DOJ 2010b). The woman obtained the supplements from a manufacturer in China. She pled guilty to mail fraud, smuggling illegal products, and distributing a controlled substance. The woman distributed the drugs in full knowledge that they contained the controlled substance and failed to comply with FDA drug regulations. She smuggled the pills via the mail system and labeled incoming packages as “gifts” in order to evade import duties (FDA 2010b). Her co-conspirators in China sent the packages to multiple addresses to deliberately deceive U.S. Customs officials (DOJ 2010b), then she deliberately deceived customers by telling them that the illegal diet pills contained only natural ingredients made in Japan. She also stated to customers that the FDA warnings about these pills were untrue (FDA 2010b). She was sentenced to a total of 3 mo in prison for importing and distributing the violative pills and was ordered to pay a $5000 fine, undergo 3 y of supervised release with 9 mo of home detention, surrender $250000, and pay a special assessment of $1800 (DOJ 2011). Cases such as these demonstrate that the issue of direct to consumer online marketing magnifies the public health threat of DSF.

The dietary supplement supply chain

Direct-to-consumer marketing

Approximately 74% of adults utilize the Internet, and 61% have searched for health or medical information online (CDC 2011a). Additionally, 49% have reviewed a website for information about a particular medical issue (Baker and others 2003; Cohen and Adams 2011). The popularity of Internet use for health/medical information opens the door for any and all dietary supplement advertising. Use of the Internet to sell supplements directly to consumers removes barriers that may otherwise dissuade a consumer from purchasing the product. When a consumer purchases a supplement from an Internet site, no physician or pharmacist can intervene in order to warn the consumer of potential side effects or drug interactions. The consumer makes decisions based upon the information available on the website. Internet marketing may be especially effective for health/medical issues associated with embarrassment or shame such as sexual dysfunction and obesity. A consumer afflicted with such conditions may wish to avoid the embarrassment of a consultation with a doctor or pharmacist, so instead, discreetly purchases the product online from the safety of his or her own home. However, a consumer may not be able to distinguish truth from deception given that supplement marketing techniques adeptly disguise truthfulness.

An Internet search for the term “weight loss supplements” produced 28400000 hits. The very first website that appears is http://weightlosssupplements.net/ (Google 2011). The website introduces a man named “Mike,” a former employee of an anonymous supplement firm, who discloses “What Weight Loss Supplement Companies Don't Want You to Know.” According to Mike, weight loss supplements really do work and most weight loss supplement companies “suck.” The top 10 weight loss supplements discussed on the website range from $39.95 (for 2 separate products, weight and amount of capsules not disclosed) to $69.95 for a 60-capsule bottle (WeightLossSupplements.Net 2011). Mike instructs potential customers, “don't believe everything you read.” Other examples of direct to consumer online marketing may seem more legitimate.

In April 2011, the FTC asked federal courts to stop 10 online operations using fake information to market acai berry weight loss products. FTC declared that the websites offer information that seems to originate from legitimate news-gathering sources. However, the sites endorse other websites that promote sales of acai berry as a weight loss supplement. The sites display logos of well-known news outlets such as ABC, Fox News, CNN, and USA Today, followed by fictional testimonials about the product. The Director of FTC, David Vladeck, stated that, “almost everything about these sites is fake. The weight loss results, the so-called investigations, the reporters, the consumer testimonials, and the attempt to portray an objective, journalistic endeavor.” The FTC requested that courts order the companies to provide refunds to consumers who purchased the supplements. The FTC had originally received consumer complaints alleging that the complainants paid between $70 and $100 for the deceptive weight-loss products, which then triggered the investigation. Other claims made by companies selling acai supplements centered on using the products as colon cleansers for cancer prevention. The outcome of the cases is pending (FTC 2011). Although many distributors choose to market imported dietary supplements directly to consumers, many utilize gray markets.

Gray markets

Imported supplements also enter the United States via gray markets. Black markets facilitate the sales of stolen or counterfeit goods, while gray markets (either foreign or domestic) enable genuine products to be sold illegally. Products on the gray market are sold through unauthorized distribution channels that a manufacturer or trademark owner has not approved (Berman 2004). Even if a firm takes every precaution to prevent issues from occurring with a dietary supplement manufactured abroad, the legitimacy of supply chains can still be compromised. Gray markets represent a formidable challenge to industry and regulators, and according to one publication, are “a disease to be eradicated” (Antia and others 2004).

Current DSF intervention and response

The response to the case regarding the drug-laced diet pills from Japan involved a cooperative effort by the FDA, the Postal Inspection Service, and Immigration and Customs Enforcement Homeland Security Investigations (DOJ 2011). The majority of the regulations that pertain to dietary supplements fall under FDA, but U.S. Customs regulate the flow of all imported products, and the Postal Inspection Service investigates and provides evidence for cases of mail fraud. The U.S. Postal Service delivers mail to nearly 151 million locations in the United States, and as of 2010, has a total revenue of $67 billion (USPS 2012). Other agencies also share responsibility for DSF monitoring and enforcement.

The FTC regulates advertising and investigates any associated consumer fraud issues. On the local and state levels, health department inspectors encounter misbranded and adulterated dietary supplements during routine inspections and may pursue regulatory action such as embargo and destruction. Despite the efforts of all these regulatory agencies, fraudulent dietary supplements still enter the United States in huge quantities. Many reach unsuspecting consumers.

FDA and U.S. customs import procedures, intervention, and response

It is estimated that only 1% of food entering into the United States undergoes inspection. The United States has over 300 ports of entry, and inspectors are responsible for screening approximately 20 million imports of products under its jurisdiction (Nucci and others 2008). FDA's authority over imports falls under Section 801 of the FD&C Act. In 2002, the Public Health Security and Bioterrorism Preparedness and Response Act enhanced these regulations by establishing that facilities responsible for manufacturing, processing, packing, or holding food for the U.S. market must be registered with the FDA, and that firms must provide prior notice of importation to authorities (Closs and McGarrell 2004; Voss and others 2009; Speier and others 2012). Under the Act, FDA may utilize administrative detention authority and mark refused materials in order to deter reimportation (Nucci and others 2008).

Firms must adhere to these import procedures with full knowledge that FDA has the authority to refuse entry if a product appears to be adulterated or misbranded. FDA may detain a product with or without physical inspection based upon previous history or other information that suggests that the product is violative. When a shipment arrives, the Custom Agency's Automated Commercial System (ACS) notifies FDA through FDA's Operational and Administrative System for Import Support (OASIS). Then, FDA makes decisions about disposition based upon physical inspection/examination or examination of samples. The Agency considers factors such as type of product, FDA priorities, and prior history of the importer. In the event that FDA declines inspection of a shipment, they inform the Customs Agency, which then allows the shipment to enter. If FDA suspects a health threat exists, FDA can request that the Customs Agency hold the shipment for 24 h. The shipment is then subject to analysis and refusal. Officials notify the importer, who then must take steps such as conducting lab analysis to prove that the shipment does not violate regulations. If the shipment is still violative, customs officials will pursue destruction or export the shipment out of the country (Nucci and others 2008). Imported products found to be violative can appear on FDA's Inspection Refusal Report (IRR) if the agency decides to refuse admission. An example entry for the imported dietary supplement, Safi Blood Purifier, is shown in Figure 4.

Figure 4.

Safi blood purifier import refusal report (FDA 2002a).

This entry shows that on March 8, 2002, FDA identified Safi Blood Purifier, manufactured by Shamsheer Traders of Karachi, Pakistan, as an unapproved drug. FDA deemed the product to be violative because it “appears to be a new drug without an approved new drug application” (FDA 2002a). Additionally, FDA did not make this decision based on sample analysis, indicated by “no,” so it may be speculated that FDA decided that Safi is an unapproved drug based on labeling alone or prior violative history of the product or manufacturer.

State and local level intervention and response

State and local health departments also have a certain level of authority regarding enforcement of FDA laws that pertain to misbranding and adulteration. For example, the New Jersey Dept. of Health (NJDOH) enforces such laws under N.J.S.A. 24, Food and Drugs. Title 24 states that “no person shall distribute or sell, or manufacture for distribution or sale, or have in his possession with intent to sell, any food, drug, cosmetic, or device which under any of the provisions of this subtitle is adulterated or misbranded” (State of New Jersey 2012). The regulation also states that an agent of the state or local health department, upon finding a suspected misbranded, adulterated, or fraudulent product, has the authority to take a sample of the product and embargo the remaining inventory. The regulation states that a warning accompanies an embargo, notifying a firm that removal or sale of embargoed items without permission by the agent, a health department inspector, or the court, is unlawful. The inspector may also condemn any food found to be violative of any provision of the regulation and oversee destruction, “in such a manner as to make it impossible to be thereafter used for human food (State of New Jersey 2012).

Incidents of fraud and public health threats associated with dietary supplements are an underrecognized public health issue. Traditionally, intervention and response tactics have been employed to combat DSF that has lead to public health incidents or that have the potential to cause public health harm. However, the logical progression is from an intervention and response approach toward a prevention approach (Spink and Moyer 2011).

DSF prevention

DSF prevention is extremely interdisciplinary and complex. The prevention philosophy is very different from the traditional sciences that are engaged. Criminology and the behavioral sciences are rarely included in the disciplines of food safety, food quality, food defense, and food fraud. Expanding a perspective to the new disciplines is effective for individual investigators and for organizations.

Establish a base of knowledge

The issue of DSF is a challenging one that calls for nontraditional approaches that focus on prevention. As discussed, numerous imported supplements contain carcinogenic (cancer-causing) heavy metals and/or harmful drug ingredients not listed on the label. Fraudsters deliberately deceive consumers by concealing critical warnings about adverse health effects or advertising products with inflated health claims. Regulatory authorities must educate themselves and staff members on this vital issue and how they can become proactively involved. Publications available online can assist in creating an overall “big picture” and offer valuable guidance on frontline issues such as dietary supplement labeling. Regulatory authorities such as local health departments may not have the financial means to conduct lab testing of products suspected to be contaminated with lead or drug adulterants. However, they can remove a product from the market because the label is not in compliance and the product is considered misbranded and/or appears on FDA Import Refusal/Alert. Knowing what a compliant label looks like, determining the difference between legal claims and drug-type claims, and reviewing the legality and scope of regulatory powers can empower state and local regulatory agencies to feel confident that their actions pertaining to misbranded supplements will stand up in a court of law.

Facilitate interagency cooperation and communication

Traditionally, regulatory authorities may only have contact with law enforcement and courts when faced with uncooperative individuals or businesses. However, in order to create formidable deterrents that disrupt DSF, regulatory agencies must practice cooperation and communication with law enforcement and other agencies/departments including regulatory agencies in other countries and international nongovernmental organizations (NGOs) on a routine basis. Other laws that a business may be violating should be considered, and the respective agency should be contacted and offered as much information as possible. Information sharing should be encouraged, especially when particular incidents cross jurisdictional lines, such as a firm importing fraudulent dietary supplements through the mail system and also deceiving consumers through online marketing of their products. In this case, it would be prudent to contact postal authorities and consumer protection agencies for follow-up, as this may also help to build a stronger case against a violative business. Such information sharing can help to achieve mutual objectives that aim to prevent DSF. When possible, regulatory agencies should welcome opportunities for joint inspections/investigations. Joint inspections help to educate each authority involved on the responsibilities and enforcement powers of the other authority. Also, joint efforts allow for the sharing of expertise and valuable resources. Finally, joint investigations send a strong message to criminals that their actions will not be tolerated, and that interagency loopholes that they may be accustomed to taking advantage of no longer exist.

Focus on reducing the fraud opportunity

Disrupting a fraudulent dietary supplement operation requires “outside the box thinking.” The fraudsters are clandestine, stealthy, well informed, and very creative at circumventing detection or inspection hurdles. The persistence of the fraudster is why the concept is an “opportunity” rather than framed as a public health and economic threat. Prevention should focus on the motivation of the fraudster. Just because regulatory agencies remove fraudulent products from retail stores does not mean that the supply chain shuts down. Regulatory agencies should focus on prevention by conducting full traceback and traceforward activities to determine where the product has been bought and sold. A business should provide invoices with their supplier information to demonstrate legitimacy of a suspected product. If a product is fraudulent, regulatory authorities should follow up with an investigation of the supplier(s). Regulatory authorities should require the business to issue written notices to their customers that the implicated product(s) has been recalled, and that they should return it for a refund. The investigation should not stop at “how” the product was made and the system breached, but “why” did the fraudster perceive a fraud opportunity in the first place. Once fraudulent products are identified, regulatory authorities must work together with FDA or their counterparts in other states to identify and share information that will assist in cutting off or disrupting fraudulent supply chains. Customs authorities should be apprised and provided with written information on fraudulent suppliers and products so that they can take steps to stop importation at the border.

Strengthen adverse event reporting requirements

Public health adverse events or potentially harmful products associated with dietary supplements should be required to be reported to FDA via the Reportable Food Registry (RFR). Currently, industry is required to use the RFR to report when there is a reasonable probability that an article of food can lead to adverse health consequences. However, RFR requirements do not apply to dietary supplements at this time. The RFR is advantageous in that it assists FDA to identify and follow patterns as well as focus on higher priority inspections. Manufacturers, as well as any firm involved in the distribution chain, should utilize the RFR to report when there is an issue or a recall on dietary supplements. Doing so protects the integrity of the firm and its products, increases the speed with which hazardous products can be withdrawn from the market, and limits damage to public health (FDA 2012d).

Conclusion

Dietary supplements continue to increase in popularity among consumers who seek nutritional enhancement and natural alternatives to prescription drugs. With more people consuming more supplements, there are growing consequences—good and bad—for food science and food safety. Dietary supplements are a special category of food that, unlike food additives, are not added to food products, but are stand alone products intended to supplement the diet. Current definitions clearly distinguish dietary supplements from both food and drugs and establish that dietary supplements are a unique category of consumer products with unique challenges (“dietary ingredients,” such as vitamin D added to breakfast cereals, are components of dietary supplements). However, loopholes in the regulatory structure allow fraudsters the opportunity to profit immensely from DSF. The scope and breadth of DSF is global and although the motivation for DSF is economic, unintentional public health adverse events such as heavy metal poisoning or drug interactions can and do occur. Effective measures to combat DSF require understanding of what it is, why it occurs, who is involved, and how it can be prevented.

DSF differs from both food fraud and fraud associated with prescription drugs. Though DSF overlaps with both in some ways, it is clearly unique. DSF is similar to food fraud in that the motivation is economic, and the consequences can harm the health of consumers. Fraudsters add active ingredients to dietary supplements in order to increase effectiveness, and therefore customer satisfaction with the finished products. However, since unscrupulous manufacturers and distributors deliberately leave active ingredients off the labels to avoid regulatory complications, consumers remain unaware of what the products contain. As a result, they are unaware of potential public health and other consequences. Olympic athletes have suffered the consequences of unknowingly consuming tainted dietary supplements, then being disqualified from competitions. Other consumers have experienced severe health effects such as lowered blood pressure, kidney damage, heart-related complications, or have lost their lives. Fraudsters are focused on taking advantage of regulatory loopholes for their own economic profit, but do not consider or do not care about the public health consequences of their activities.

After the Dietary Supplement Health and Education Act (DSHEA) removed regulatory preapproval requirements, dietary supplements flooded the market and savvy fraudsters took advantage of opportunities to promote health benefits without strict oversight of their marketing activities. As a result, misbranded and adulterated products reach consumers. While legitimate manufacturers and distributors follow strict current quality and safety restrictions such as current Good Manufacturing Procedures, fraudsters facilitate movement of their products across international borders and through the Internet. Such operations are a direct threat to public health and further magnify the issue as fraudsters continually evade regulatory hurdles and established quality controls.

Current approaches to combating DSF follow intervention or response procedures. Fraudulent dietary supplements sold to consumers have led to public health events, then a reactive regulatory response. Cases of DSF that have been handled in court represent an intervention and response approach that occurs long after consumers have already been affected. Such procedures do not cut off supply chains, do not effectively prevent such incidents from reoccurring time and time again, and do not protect public health. Developing understanding of DSF and related criminology concepts such as the crime triangle offer promise for understanding motivations for DSF and for developing effective, prevention-based approaches.

Next Steps

Progression toward prevention-based approaches to DSF depends upon further in-depth examination of the current regulatory structure, a greater understanding of fraudster operations (especially across international borders), and collaboration among the industry and regulatory agencies. Additionally, consumer education regarding avoidance of fraudulent dietary supplements will assist in restricting public health harm. Much additional research is required in this area.