Medical pharmaceutical and device manufacturers are essential in making products that benefit patients, and collaboration between health care clinicians and the industry is necessary for the design and manufacture of these medical products. However, health care clinicians must recognize that their duties and the interests of the industry may at times diverge. Relationships with the industry, even seemingly minor ones, have the potential to shape the decisions made on behalf of patients. The marketing divisions of pharmaceutical and medical device firms view health care clinicians as targets of their efforts, and some of the interactions that occur between the industry and health care clinicians have the potential to alter decision making in ways that may not necessarily benefit patients. Health care clinicians have an ethical duty to recognize situations and marketing strategies that are designed to influence their choice of diagnostic and therapeutic options for their patients. At a minimum, health care clinicians should be aware of the techniques used to attempt to alter their behavior and guard against them.
The practice of medicine is an inherently moral activity, the foundation of which is a clinician-patient relationship grounded in trust. The pediatric health care clinician’s primary responsibility is to seek the best interest of his or her patient.1,2 All other interests remain secondary. Health care clinicians must conduct their professional responsibilities in a way that allows patients and the public to trust their actions and judgments.3 These professional duties include not only providing high-quality clinical care but also educating health care professionals in training and advancing the knowledge base of pediatric practice through the conduct of scientifically and ethically sound research.
Health care clinician interactions with the industry (commercial enterprises that manufacture products, such as drugs, devices, or nutritional products, for use in patient care) are, at least in some cases, essential to the promotion of these primary professional duties. Research designed and funded by the industry is essential to the development and improvement of diagnostic and therapeutic modalities critical to the delivery of quality health care to children. Industry funding is particularly important in the setting of inadequate government funding of medical research. The development of pharmaceutical products and medical devices essential to the care of patients requires interaction with physician experts and investigators at almost every point in the development and research process. Continued progress in drug and device development requires the interaction of physicians and the industry.
However, some clinician-industry interactions, even seemingly minor ones, may have the potential to undermine the health care clinician’s duty to seek the best interest of the patient.4,5 Both financial (honoraria, gifts, speakers’ fees, food, travel, lodging, and educational and research grants) and nonfinancial (deference, recognition, enhanced reputation, and publication opportunities) inducements have the potential to influence the decisions health care clinicians make on behalf of their patients and undermine trust in the patient–physician relationship.6–9 The primary challenge posed by interactions with the industry is not one of health care clinicians who are corrupt, but of well-intentioned health care clinicians who are subtly and subconsciously influenced to make decisions that may not represent the best choice for their patients.10–12 Health care clinicians may fail to recognize their vulnerability to the methods used by the industry to influence their behaviors and decisions.7 Although hospitals, academic institutions, professional societies, journal editors, and medical education providers all play a role in mediating the potential influence of clinician–industry relationships, this technical report will focus solely on the individual health care clinician, highlighting the ways in which an individual clinician can be subtly influenced by the industry and offering some suggestions to aid health care clinicians in navigating relationships with the industry while maintaining their primary responsibilities to patients and the public.
An Overview of Health Care Clinician Relationships With the Industry
Physicians and other health care clinicians have represented a primary target audience for pharmaceutical and medical device marketing. Studies have reported that an average of approximately $61 000 was spent per physician in the United States in 2004, and that amount has decreased between 2006 and 2010.13,14 In 2016, pharmaceutical companies spent $29.9 billion on marketing, of which $20.3 billion (68%) was directed toward health care clinicians in the form of prescriber detailing ($5.6 billion), free samples ($13.5 billion), direct physician payments related to specific drugs ($979 million), and disease education ($59 million).15 Data collected by the Centers for Medicare and Medicaid Services under the Open Payments program16 revealed that, in 2019, 615 000 physicians received payments or investment interests worth $3.6 billion (an average of $5854 per physician recipient), and 1194 teaching hospitals accepted payments totaling $2.63 billion. Payments are highest among the medical and surgical specialties and, although 90% of physicians who accepted payments between 2014 and 2018 received less than $10 000, 3.4% of physicians who accepted payments received more than $50 000.17 According to 2015 Open Payments data, approximately 40% of primary care pediatricians have received payments from the industry, most commonly for food and beverages, averaging $95 per physician; however, 559 nonspecialist pediatricians each received more than $10 000 during the year.18,19
A 2007 survey of US physicians revealed that 94% reported at least some relationship with the industry; 83% accepted gifts from the industry in the form of food or beverages in the workplace, 78% accepted drug samples, 28% accepted some kind of payment for consulting, speaking, serving on an advisory board, or enrolling patients in clinical trials, 26% took advantage of free or subsidized continuing medical education (CME) events, 15% accepted travel expenses to attend meetings, and 7% accepted gifts in the form of tickets to cultural or sporting events.20 In that same survey, pediatricians reported meeting with industry representatives an average of 8 times per month. In 2003, others had described similar levels of physician contact with the industry.21 In older surveys from 1988 and 1994, more than half of physicians named commercial sources, such as industry representatives, as the most influential source in deciding whether to prescribe a new drug.22–24 For example, a survey from 2000 revealed that nearly half of physicians reported eating food provided by pharmaceutical representatives, 48% reported providing drug samples to patients on a daily basis, and 76% of respondents reported that pharmaceutical representatives were, to some extent, a valuable source of information.25
Leaders in academic medicine are no less inclined to maintain industry relationships. In a 2007 survey of clinical department chairs, almost two-thirds of department chairs had some form of personal relationship with the industry, including having served as a consultant, a member of a scientific advisory board, a paid speaker, and/or an officer, founder, or member of the board of directors.26 Similarly, a 2020 study found that 80% of physicians serving as board or governing council members for 10 professional medical organizations had financial relationships with companies making drugs and devices during their time in leadership.27 In recent years, many academic institutions and hospitals and some private practices have restricted access between staff and industry representatives, at least at educational events.28–30 Although this has restricted 1 avenue for contact between the industry and health care clinicians, many points of contact remain.
In many cases, the goals of the industry and health care clinicians are aligned. Medical pharmaceutical and device manufacturers are essential in making products that benefit patients, and collaboration between physicians and the industry is necessary for the design and manufacture of these medical products.31–34 However, health care clinicians must recognize that their duties and the interests of the industry may at times diverge.35 One of the goals of the pharmaceutical and medical device and products industry is increasing company profits and shareholder value. Although those industries may be essential in providing important products for the management of medical conditions, their fiduciary responsibility lies elsewhere, and the interests of the individual patient and society have, from time to time, been subordinated to commercial interests.3,36–39
Health care clinicians represent a target audience for industry marketing efforts,40 and many of the interactions that occur between the industry and physicians (speaker’s fees, offers of ghost authorship, ill-defined consulting arrangements, gifts, and other marketing initiatives involving physicians) may not be necessary to accomplish the kind of collaborations that benefit patients.41 They do, however, serve a purpose important to the industry; physicians who receive payments for services rendered to the industry tend to prescribe more brand-name drugs than do their colleagues who do not receive such payments.42–47 Health care clinicians have an ethical duty to recognize the situations and marketing strategies that are designed to influence their choice of therapeutic options for their patients. At a minimum, health care clinicians should be aware of the methods used to attempt to affect their behavior and develop strategies to address them.
Facets of Product Promotion
The marketing or promotion of pharmaceutical products and medical devices extends well beyond easily recognized advertisements and visits from industry representatives. Product promotion may take subtle forms, including social opportunities, educational programs, research, and consultation. Health care clinicians must be vigilant in recognizing the broad array of activities designed to market medications and devices.
Promotion Through Industry Representatives
Many physicians believe visits from industry representatives include an educational component. In a 2009 survey of physicians, 76% reported their view that information from sales representatives was at least somewhat valuable, and 29% reported using information from representatives often or almost always when making decisions about whether to prescribe a new drug.25 Many of these interactions occur when industry representatives visit physician offices, but they also occur at professional meetings and education events that include exhibit halls and sponsor tables. Industry detailing may serve a role in accelerating the adoption of novel and useful therapies and technologies, given the slower spread of information about these products through the medical literature and accredited CME events. The intent of these visits, however, is not only to educate but also to promote products.
Pharmaceutical and industry detailers, like most people in sales, are generally friendly, intelligent, and outgoing. Their job is to persuade health care clinicians to use their products.48–50 To accomplish this persuasion, sales representatives are trained to learn as much as possible about the professional’s personal interests and life to establish a relationship that feels like a friendship.50 Sales representatives are often genuinely likable, which makes it difficult to refuse to talk with them.48
The detailer often uses data obtained through pharmacy registries to become familiar with the professional’s prescribing practices. Pharmacies collect this information and sell it to data mining companies, which then sell the reports to pharmaceutical companies.51 These data allow an industry detailer not only to identify high and low prescribers, but also to increase visits and focus their message to individual health care clinicians who are low prescribers, reinforce the behavior of high prescribers, and monitor the effect of certain approaches with a specific professional.48–53
Evidence from several older studies reveals that information provided by industry detailers may be biased and presented in a way that casts a favorable light on the drug or product being marketed to the health care clinician.53–56 Industry detailers are carefully trained to present medical information, and even characterize the clinician’s objections, in a way that supports their “pitch,” turning concerns into a reason the product should be preferred over others.49,52,53 Information is presented by using persuasion and sales methods that have been proven effective in changing behavior and influencing others.4,7,10,57,58 Health care clinicians are no less susceptible to these persuasive techniques than anyone else.51,59
Promotion in the Form of Education
CME opportunities encompass a broad range of activities, including those that are accredited (and therefore regulated and monitored for conflicts of interest) and those that are not. Health care clinicians (and the patients they serve) should be able to trust that ongoing education in the form of CME is unbiased and data-based. Yet, when educational events are industry-sponsored and unaccredited, biased information is frequently disseminated. Industry-sponsored educational offerings generally favor the class of product the sponsor produces, the specific product they produce, and the use of patented over generic products.52,60 In some cases, industry sponsors may determine the topic, select the speaker, develop curricula, or provide or edit the text used by speakers.
According to the Accreditation Council for Continuing Medical Education (ACCME), 10% of ACCME-accredited CME in the United States in 2016, accounting for 20% of learner interactions, were supported by commercial entities.60 Pharmaceutical and device manufacturers invest heavily in medical education and communication companies (MECCs), which are asked to develop CME programs, prelaunch and branding campaigns, and digital and print publications based on the specifications of the company that hired them.61–66 In 2016, 28% of the income of CME providers accredited by the ACCME was from commercial entities.60 Conferences and lectures organized by MECCs are often designed to fit the specifications of the industry sponsor and present the company’s product in a positive light while appearing neutral. This strategy may involve finding a speaker who is willing to deliver a lecture that has been prepared for him or her or simply identifying a recognized expert who already delivers a lecture that favorably portrays the company’s product. Because many professional societies will not allow funding to influence their programming directly, professional meetings are often accompanied by unofficial programming that occurs simultaneously and frequently includes a free meal while an expert lectures on a relevant topic. The programming is designed to deliver a message favorable to the company and its product. Because MECCs are often the official sponsors, the name of the company that funds the endeavor rarely appears on promotional materials.63,67
Pharmaceutical companies may influence educational content through even more subtle vehicles. Some companies offer grants to patient advocacy groups that allow the group to sponsor lectures and produce materials designed to educate health care clinicians and the general public not only about the condition in question but also about the company’s product that can be used to treat it.68,69 In some cases, advocacy groups have been used by the industry to influence public policy related to specific drugs, as well.70,71 Similarly, industry involvement with and participation in (sometimes directly and sometimes via physician experts) social media sites designed for health care clinicians may be used to communicate without revealing the promotional purpose.72 Finally, medical apps that are branded by the industry not only associate a brand with a useful tool, thus nurturing a favorable attitude toward the industry sponsor, but may also nudge a user toward the company’s products.73
Evidence indicates that industry-sponsored CME influences physician prescribing behavior. Conference funding by the industry has been shown to increase brand loyalty,74 and physician prescribing behavior has been shown to favor the specific product made by the company sponsoring a CME event, despite physicians’ claims that the event did not influence their prescribing behavior.75,76 As a result, the American Medical Association (AMA) Council on Ethical and Judicial Affairs has raised concerns that industry involvement in professional education threatens “the integrity of medicine’s educational function”77 and that “…industry funding for CME could have undesirable effects, including potentially biasing content toward funders’ products and influencing the overall range of topics covered.”78
Promotion Through Speaking Opportunities and Consultation
Physician educators, particularly those identified by the industry as “key opinion leaders,” may play an important role in industry marketing. Industry-sponsored speakers’ bureaus are one vehicle by which the industry enlists influential physicians to deliver lectures with a message that is favorable to the sponsor. Many less obvious mechanisms also exist, however. Industry detailers may be tasked with identifying “thought leaders” who appear to have a favorable attitude toward the company’s products as potential recruits for consulting and speaking engagements.49,50 The most desired speakers are those who are subtle and tactful in their promotion of the company’s product.50 Key opinion leaders are carefully engaged, often using a gradual approach beginning with a single lecture accompanied by an honorarium for a local talk. There may be no attempt to influence the content. If the speaker delivers a talk that appears favorable to the company message, he or she will be offered other opportunities and perhaps subtly encouraged to tailor his or her comments in a direction that is favorable to the company’s product. Speakers who advocate for a company product may be offered lucrative national speaking opportunities.48 Physicians invited to participate in speakers’ bureaus are carefully monitored and not asked to continue unless their message is favorable to the company.79,80 These “thought leaders” are recruited not only because of their impact on other health care clinicians but also because the use of the company’s products by these speakers is likely to increase.50 Speakers may be influenced to use the product because of the sense of obligation for the “gift” of the opportunity provided, the sense of loyalty and commitment to the company they now have a relationship with, and the opportunity for company representatives to spend time with these physicians talking about their product and its many potential uses.79,81
Physician speakers have 2 important advantages over pharmaceutical employees. First, they are respected clinicians who do not appear to have a direct connection with the company and its product. Second, physicians can suggest the use of the company product for off-label indications, something industry employees could not do legally through formal marketing efforts.56,82,83 This strategy occurred with the drug Neurontin (gabapentin), a drug approved only for a narrow indication in the treatment of epilepsy. Using a variety of strategic methods involving sponsoring small research projects to suggest possible off-label uses of the drug, preparation of these articles, ghost-written review articles, and commentaries suggesting various off-label uses for the drug, and speaking engagements, the company nurtured a group of opinion leaders to promote the use of the drug for a wide range of conditions, including migraine, chronic pain, bipolar disorder, restless leg syndrome, and others for which there was little to no evidence of efficacy.48,59,84 The industry uses similar techniques to expand the use of drugs to conditions previously not considered abnormal, such as nongrowth hormone deficiency short stature.83 Other examples of “drugs in search of a disease” include those sometimes suggested for menopause, sleep disorders, the level of cholesterol requiring treatment, prehypertension, social anxiety disorder, and erectile dysfunction.83,85,86 Although each of these conditions can be severe and debilitating, the industry has encouraged drug treatment of a significantly expanded number of patients by altering the clinical definition of what constitutes normal and what “requires” treatment. This even appears to extend to the overdiagnosis of cow milk protein allergy and the use of specialized infant formula products.87,88 Most recently, expansion of the use of opioids for pain management was largely driven by the marketing efforts of pharmaceutical representatives, who sought to expand the market for opioids beyond a few limited situations.52,53,89
As discussed previously, consulting opportunities are also frequently used as subtle marketing devices by the industry. In 2009, the Institute of Medicine (IOM [now the National Academy of Medicine]) recognized the need to distinguish between consulting, in which a physician offers objective technical advice on scientific issues, products in development, and research study design, and those activities that more closely resemble promotional or marketing support.90 Although consulting in the former sense serves an important purpose, the distinction is often blurred because physicians who serve as consultants have established a relationship with a sponsor, benefit from that relationship, and will find themselves in a position in which they will almost certainly be subject to subtle marketing from company contacts.
Physicians hired as consultants may not realize that they may be used to market a drug and that they themselves are the target of marketing efforts.3,48,59,84 In the case of Neurontin, prescriptions for the drug increased 70% among physicians attending dinner meetings directed at physicians who had been paid to attend, either as a CME opportunity or as “consultants.”84 Company documents released during litigation have provided evidence that industry sponsors who combine educational programs with social events and meals generate a significant return on their investment in terms of increased prescriptions, both from physicians participating in those events as attendees and from speakers.91
Promotion Through Research
Federal funding for research in the United States has decreased in recent years whereas industry-sponsored funding of research has increased substantially.92 Industry-sponsored research plays a critical role in advancing child health, both in the creation of new products and in support of pediatric labeling of US Food and Drug Administration-approved therapeutic products. Because the majority of research funding for drugs, vaccines, and devices for children is provided by the industry, pediatrician involvement in industry-sponsored studies is necessary and unavoidable, and most physicians undertake their role in these projects with integrity. Nonetheless, it is important that physicians be aware of some potential concerns in working with industry sponsors.
The industry may use research as a means of promoting their products, through the use of peer-reviewed journal articles,56 review articles and editorials written by experts with industry ties, and consensus and guideline statements developed by panels consisting mostly of members with ties to industry.93,94 Choudhry and colleagues found that 87% of authors of clinical practice guidelines had some form of interaction with the pharmaceutical industry, 58% had received financial support, and 38% had been employed or paid as a consultant by a pharmaceutical company.95 Most of these authors had a relationship with a company that manufactured a product referred to in the guideline.
Industry-sponsored research has, in some cases, been tied to serious deviations from accepted research standards and flawed reporting of the risks and benefits of study drugs with a bias in favor of the industry product under investigation. These include manipulation of study entry criteria and selection of study populations, manipulation of drug dosages to favor a company product, selective use of data, nonpublication or delayed publication of trials that did not show a result in favor of the product in question, underreporting, biased reporting, selective reporting of results, nonreporting of adverse events, deviations from accepted standards for data analysis in a way that leads to biased results, and biased and selective descriptions of findings and conclusions.3,59,96–109 Industry funding of studies greatly increases the chances of proindustry results.110–114 In some cases, reanalysis of full datasets by independent investigators has revealed published findings from an industry-sponsored study to be dangerously misleading.106 In more egregious cases, postmarketing evidence of risk has been suppressed.89
Industry sponsors may also practice publication planning, which involves strategies to alter the medical literature to encourage health care clinicians to use and prescribe their products. Management of sponsored clinical trials can include sponsor involvement at nearly every step of the process, including research design, data analysis, data interpretation, writing, and publication of results. An industry sponsor of a multicenter trial may control the data and restrict access to the entire dataset to all but company statisticians, decreasing transparency and increasing the possibility of “data mining.” These company statisticians may not be included as named authors.115 Industry sponsors may use MECCs to ghost author articles and commentaries for publication, following the company’s specifications for framing and writing, and then assist in getting the manuscripts published in high-impact journals.84,115–118
The industry may also sponsor the publication of studies after the approval of a product. These publications have become known as “seeding trials,” and their purpose is often not to advance science, but to influence potential prescribers or users, sometimes referred to as “marketing in the guise of science.”82,119,120 The intent of these studies and publications is to familiarize health care clinicians with their products,121 encourage health care clinicians to use the company product rather than a competing product or generic version, and, in some cases, suggest new applications of the product that are not covered by the current approval and that represent applications for which the company cannot legally advertise. Not uncommonly, the industry may follow a “publications strategy” in which they design and fund seeding trials to explore the use of a drug for off-label uses (eg, the use of an antiepileptic agent approved for narrow indications would be the subject of small trials using the medication for other seizure disorders, chronic pain, bipolar disorder, migraine, etc).59 These trials seek to influence more than the readers of the study, however. They may also be intended to influence the “opinion leaders” whom the company has selected and approached to participate in the studies as named authors. These research and authorship opportunities are frequently accompanied by salary support or payments and sometimes offer additional paid speaking and “consulting” opportunities to disseminate the results suggested by these trials (presumably the off-label use of a company product).119,120
Ghost authorship is another technique used by the industry that enlists physicians to serve as “authors” of clinical trials, review articles, or editorials that have been written by scientists or medical writers working for the sponsor.115–118,122 Biomedical companies may ghost author papers as part of an organized marketing strategy.123 A company will invite carefully selected academic leaders to serve as authors on a paper that has been written either by employees of the company or by a hired medical education company. The actual employee who authored the paper will either not be credited with authorship or will appear among the list of names, whereas the ghost authors occupy the first and last author positions.124 Although some of these authors may have been involved at some level in the conduct of the trial (enrolling participants, for example), statistical analysis is often performed by company statisticians, with little opportunity for the outside “authors” to analyze the full raw dataset themselves.99 In some cases, a payment is made for being named as an author. Even without payment, however, the opportunity to author a paper, especially one that appears in a high-profile journal, is incentive enough in a field in which the number and location of publications heavily influence an academic physician’s opportunities for retention, promotion, salary, and enhanced stature and reputation among peers.
The Power and Psychology of Persuasion
Health care clinicians believe they remain unaffected and uninfluenced by pharmaceutical marketing and detailing techniques,125–128 despite the fact that multiple studies demonstrate that these techniques have significant effects on prescribing behaviors and requests for formulary changes.129–140
Health care clinicians may fail to recognize their vulnerability to both financial and nonfinancial forms of persuasion. Although health care clinicians believe that they can distinguish between accurate and inaccurate information presented by industry representatives, the data suggest otherwise.141–143 Contact with industry representatives has been shown to change physician behavior in terms of pharmaceutical choices and requests for formulary changes.23,129,132,139,144–146 For historical context, in a 1992 study, Orlowski and Wateska tracked prescriptions at their hospital for 2 drugs during the 22 months before and 17 months after an all-expenses-paid symposium held at a resort and attended by physicians on staff at the hospital.134 Although physicians who attended the symposia reported that their attendance did not alter their prescribing patterns, the use of both drugs increased after the symposia (whereas national usage rates remained unchanged). On the other hand, implementation of policies at academic medical centers restricting access to pharmaceutical detailing is associated with a reduction in prescribing many detailed drugs.137
Despite their own sense of invulnerability to persuasive techniques, physicians do consider other physicians to be vulnerable.125 This phenomenon is what social scientists refer to as the “bias blind spot.”147 As a general rule, individuals underestimate the degree to which they are influenced by cognitive and motivational bias and overestimate the degree to which others are influenced by the same things.147 In one survey of 397 members of the American College of Obstetricians and Gynecologists (ACOG), respondents were significantly more likely to believe that other physicians would be influenced by free food, the gift of an anatomic teaching model, or paid consultancies than they themselves would. In that survey, 80%, 88%, and 64% reported that they would absolutely not or probably not be influenced to prescribe a drug after acceptance of lunch, an anatomic model, or a paid consultancy, respectively. On the other hand, only 57%, 64%, and 38% of these respondents believed that the average physician would absolutely not or probably not be influenced to prescribe a drug after receipt of these items.148 Similarly, only 7% of authors of clinical practice guidelines believed that their relationships with the industry influenced the guidelines they developed, whereas 19% of authors believed that their colleagues’ recommendations were influenced by industry relationships.95 Interestingly, educating individuals about their biases does not eliminate those biases, although it further increases their belief that others are biased.7,147–150 Denial and rationalization are both strategies that assist in maintaining a personal sense of objectivity and assuage thoughts of conflict of interest or guilt.7
An extensive literature exists on the psychology of persuasion and the techniques that are effective in persuading humans to change their behavior or make a certain decision. In his book, Influence: The Psychology of Persuasion, Cialdini summarizes this literature and describes 6 basic categories of effective persuasive techniques.57 These techniques are widely effective, regardless of the target’s education or occupation,151 and clearly map the techniques commonly used by the industry and industry representatives discussed previously:
Commitment and Consistency. The human brain seeks consistency, and consistency requires honoring one’s commitments. Any behavior at odds with previously made commitments or previously expressed stances feels uncomfortable. Industry representatives are trained to get health care clinicians to make a verbal commitment to use their products. For example, by getting the health care clinician to verbally agree that he or she seeks a product that optimizes the care of patients and spares them side effects, an industry representative can then suggest that any health care clinician wanting to spare a patient unwanted side effects would prescribe the company’s product because it has a lower side effect profile than competing products (at least according to the company’s marketing materials). An industry representative may then attempt to obtain a commitment by asking the health care clinician if he or she will try the company product on the next 5 or 10 patients. The need for consistency then takes over. For example, once the health care clinician has tried the drug on 5 patients, he or she is more likely to continue to use the drug.7
Social Proof. In many situations, humans look to others to validate their own decisions and behavior. When told that almost all of the physicians in the region are now using drug A to treat disease B, a health care clinician will be hard-pressed not to join the group in prescribing drug A.131 Social proof is also the basis for industry reliance on physicians to encourage the use of a company product among other physicians, a technique known as peer advocacy, through the use of speaking engagements, social media, research and review papers, and consultation opportunities.124
Liking. The social science literature clearly shows that humans tend to be more responsive and receptive to individuals who are friendly, likeable, and attractive. Familiarity increases the likelihood of developing a relationship and rapport.7 Furthermore, most individuals tend to like people even more when they associate them with events at which food is served.57 Techniques that employ flattery, demonstrations of respect and deference, humor, food, gifts, and opportunities are particularly effective and make the recipient more receptive to the message being delivered. A savvy industry representative will seek to identify something he or she has in common with the health care clinician, leveraging that shared experience to nurture a more friendly relationship.
Appeals to Authority. Humans have a strong tendency to defer to those in positions of authority. The use of opinion leaders and experts to give lectures supporting the use of a product is just one example of this. Industry representatives are often quick to point out that a certain expert at a prestigious university prescribes their drug for his or her patients. This may be even further refined to include mention of an expert at the target health care clinician’s home institution.
Scarcity. Scarcity induces a sense that something is valuable and limited and leads individuals to act quickly lest the opportunity vanish. Opportunities to engage in consulting and speaking opportunities fall into this category. For many individuals, such an offer is not only flattering, but a “rare” opportunity that must be grasped before it disappears or goes to someone else.
Reciprocation. Reciprocity is a deeply ingrained cultural norm to return the kindnesses of others. A sense of obligation to reciprocate accompanies the receipt of any favor, gift, or kindness. Gifts can take many forms and need not be valuable. Gifts can include free product samples, pens, mugs, speaking and consulting opportunities, meals, trips, free CME, publication and authorship opportunities, and research grants. The receipt of a gift or kindness leaves the recipient with a sense of obligation to reciprocate, even if reciprocation involves no more than one’s time and attention to the message being delivered by the initial gift-giver. Because this technique is so commonly used with health care clinicians, it bears further discussion.
Reciprocation and Gifts
To fully appreciate the susceptibility of individuals to the subtle marketing techniques used by the industry requires an understanding of the scientific basis of both influence and reciprocity. Much cognitive activity occurs without conscious awareness, and the most effective marketing and persuasion strategies are designed to engage the subconscious aspects of decision making, making it difficult for an individual to fully “manage” the basis on which they make decisions.4,57,152 Favors (and gifts), independent of any monetary value, represent one mechanism that effectively influences behavior at a subconscious level, by generating positive feelings about the person or entity performing the favor.4
When a health care clinician makes a decision, for example, about which drug to choose for a patient, he or she assumes that this is an entirely conscious and “rational” activity. But much human decision making does not occur using a “rational” assessment of pros and cons.152 The prevailing model of human decision making recognizes 2 distinct brain systems. Decision making appears to rely on dual systems within the brain, a socioemotional system composed largely of limbic and paralimbic structures, and a cognitive control system composed of prefrontal and parietal cortical structures.153–155 The socioemotional system tends to involve rapid, automatic processing that is often reactive, intuitive, unconscious, and sensitive to social norms, motivating behavior change through feelings and autonomic responses. In other words, an action is performed because it feels right. The cognitive control system, on the other hand, tends to be consciously controlled, reasoned, and analytic and requires more time and conscious effort.154,156 Decision making involves some element of both systems but is strongly influenced by the largely unconscious workings of the socioemotional system.157 Effective marketing strategies, including the use of incentives and gifts and the nurturing of relationships, are designed to engage the socioemotional decision-making areas of the brain.104,158–160
Humans also use the cognitive-control system to rationalize behavior that may be morally ambiguous or questionable by creating a story and reasons to justify the path chosen.4,58 Health care clinicians who personally benefit from recommending certain drugs, treatments, or interventions will easily identify reasons to justify how those decisions are in the interest of their patients. Individuals with a vested interest in an outcome are often incapable of unbiased judgment.4,58
The giving of a gift and its effect on behavior is mediated at an unconscious level largely through the socioemotional system. Gift exchange is a means of initiating and sustaining relationships, and acceptance of a gift carries some expectation of reciprocation.49,161 Accepting a gift triggers a feeling of obligation on the part of the receiver—an obligation to accept and continue the relationship, and to reciprocate in some way, even if only with the gift of time and attention.2,49,131,161 Gifts may subtly and subconsciously affect the way the receiver of the gift evaluates the information provided by the gift giver, and these feelings of indebtedness may ultimately lead to changes in prescribing behavior.162
The subconscious nature of this bias makes it particularly effective.58 The receipt of a gift has been correlated with the belief that discussions with pharmaceutical representatives did not affect prescribing behavior.128 Most health care clinicians believe they cannot be bribed and that they would never trade a small gift for changing their prescribing behavior. But this belief misses the point and distracts the health care clinician from the true nature of gift exchanges. The offer of a gift or food is an offer of friendship, an overture to begin or develop a relationship.2,49 The reciprocation sought is, in many cases, simply time and attention. Once the industry representative captures the health care clinician’s time and attention, he or she can deliver the intended message, leveraging some of the other methods of persuasion discussed previously.
The power of reciprocity is well documented,57 and the feeling of reciprocity is not related to the size of the gift.57,163,164 Industry detailers are careful to provide a gift without making the receiver feel as if they are being asked for anything in return, and this is more easily accomplished with gifts that are of minimal value or those that may not initially be perceived as a gift (grants and consultation and speaking opportunities). Although the gift is not attached to an explicit expectation of return, the general sense of reciprocation that accompanies all gifts is sufficient to accomplish a marketing goal.48,49,161 Additionally, a small gift may inoculate the receiver against a larger gift by convincing the potential prescriber that they really can accept a gift without being influenced.48
Examples of gift giving as an effective marketing technique can be found commonly in many nonmedical arenas. Surveys that include a dollar bill or gift card are more likely to be filled out and returned, a store that offers a small gift to customers as they enter the store sees a significant increase in sales,164 a small gift (return address labels) often accompanies requests for donations because they have been shown to increase the number of people who donate, and insurance agents send their clients a birthday card because even that small gift imposes a sense of indebtedness (to stay with the agent). Similarly, an invitation to dinner, even when accompanied by explicit instructions not to bring anything, is generally accompanied by a sense of obligation to bring something for the host (flowers, a bottle of wine, etc). Even gifts of almost no value hold significant power.165
Gifts can take many forms. Research grants, even when not intended to create a conflict of interest, may change dispositions toward the industry sponsor funding the study (and supporting the careers of the investigators). Similarly, free CME opportunities, travel opportunities, and stipends for consulting and speaking, as discussed previously, represent gifts.
Even drug samples represent a gift to health care clinicians. When used as intended (actually given to patients), they allow access to some products that patients may not otherwise be able to afford. In reality, these samples are no more likely to be distributed to needy individuals than they are to those with insurance coverage.166 In addition, health care clinicians and office staff frequently use drug samples for their personal use.167,168 Drug sample drop offs are also used as a time to talk about other products the company may have, and pharmaceutical representatives consider them to be a valuable and effective marketing tool.50,169 The evidence suggests that the availability of drug samples does change physician prescribing behavior, particularly in the case of long-term drugs, in which the physician is likely to write a prescription for the same drug for which he or she provided samples to the patient.162 Physicians who dispense drug samples appear to write fewer prescriptions for generic medications,138,170 and this practice may lead them to dispense and prescribe drugs that differ from their preferred choice.133 In fact, physicians are more likely to stray from published treatment guidelines when a sample is available for a drug that is not considered first line.133,138
Since 2009, the Pharmaceutical Research and Manufacturers of America issued a revised code significantly restricting the kinds of gifts that pharmaceutical representatives could provide to medical professionals. Those guidelines still allow for “occasional” gifts of educational items as long as they are not valued at more than $100 and have no value to the health care clinician outside the medical environment. Likewise, gifts of food are still allowed as long as they have a connection with informational presentations.171,172 It should be noted that, although these restrictions have eliminated large gifts, they have not eliminated one problem: the ability to leverage the sense of obligation that comes with receipt of any gift or meal, no matter the value.
The Physician Payments Sunshine Act (§6002 of the Patient Protection and Affordable Care Act of 2010 [Pub L No. 111-148]; hereafter referred to as the Sunshine Act) has allowed additional study of the influence of even modest payments to physicians and prescription choices. One recent study of corticotropin prescribing revealed that every $10 000 in payments made to physicians (which includes everything from payments for food and travel to gifts to fees for consulting and speaking) was associated with a 7.9% increase in Medicare spending on prescriptions for corticotropin.173 Similarly, in a situation in which multiple treatment options existed, physicians receiving general payments were more likely to prescribe the product marketed by the company making the payments.174 Other studies have found similar associations between industry payments to physicians and prescribing behavior, even in cases in which physicians received only a single meal.42–47,58,139,160
Possible Solutions and Guidance From Professional Organizations
Given the benefits afforded by physician relationships with the industry, on the one hand, and the potential for industry relationships to persuade, on the other, the goal is to ensure that health care clinicians remain focused on the best interest of the patient while engaging the industry. Not every health care clinician who works with industry, receives honoraria for consulting with the industry or speaking at an industry-sponsored event or accepts a gift from a pharmaceutical representative will have their judgment altered in an adverse way or develop and present biased opinions.175
Nonetheless, the literature on relationships between physicians and the industry is clear on several points. First, physicians do not believe they are influenced by their relationships with the industry (although most of them believe their peers are influenced by these relationships). Second, prescribing behavior of many physicians is likely to be altered by relationships with the industry.42–47,160,176,177 Finally, there is evidence that those who do not acknowledge the influence of small gifts and industry relationships are often influenced by those gifts and relationships.178 Awareness and vigilance are necessary to guard against these subtle and not-so-subtle attempts to alter physician assessments and behaviors.
What assistance exists to address these concerns? At a minimum, all physicians must educate themselves about the subtle influence inherent in any relationship with the medical industry. A recent survey of physicians about their attitudes regarding the Sunshine Act suggested that many, if not most, physicians lack an adequate understanding of conflicts of interest and influence, taking offense at the idea that industry promotion could influence their decision making.125 An important first step is for health care clinicians to recognize that they are vulnerable to the persuasive techniques employed by the industry and to understand and accept that they may be vulnerable to unconscious bias.7 An awareness of methods of influence coupled with a critical and discerning attitude provides a first step in allowing health care clinicians to maintain an exclusive focus on patient welfare when making clinical decisions.
With regard to addressing formal relationships with the industry, 2 basic strategies have been suggested179 : a divestment strategy180 and a management strategy.181 Brody argues that a divestment strategy, eliminating any relationship a health care clinician might have with the industry, is the best for minimizing the problem.3 A complete divestment strategy, however, is not feasible in today’s reality of research funding, in which much of the funding for products improving child health is provided by the industry. In addition, pediatric researchers have the expertise needed for the conduct of clinical trials in children, and their involvement in industry-sponsored research is critical to proper study design and the appropriate analysis of and conclusions drawn from the study results. On the other hand, management strategies offer only a partial solution to the problem of industry influence on health care clinicians.3
One frequently proposed management strategy focuses on transparency, arguing that disclosure of industry relationships for those who teach, speak, participate on clinical guidelines committees, conduct research, and write should be required. This strategy has been implemented by most medical journals, guidelines committees, and more recently through the Sunshine Act, which requires commercial health entities to report to the Centers for Medicare and Medicaid Services any payments over $10 made to physicians and teaching hospitals.182 These data are made publicly available on a searchable Open Payments Web site. However, disclosure does not appear to eliminate bias or conflict of interest and may lead consultants or speakers to increase their bias (perhaps because they feel the disclosure has addressed the issue) and readers or listeners to underestimate the potential for bias in an article or presentation.183–189 This suggests that it is incumbent on health care clinicians to consider disclosures as they read the medical literature and attend conferences, considering how those disclosed conflicts might affect the presentation of the material and require a more critical analysis.190
Transparency is also limited by inadequate disclosures.191 A 2018 study using the Open Payments database found that, among articles published by the 100 physicians receiving the highest payments from 10 device manufacturers, only 37.3% included all relevant conflicts of interest in the disclosure accompanying the article, suggesting that current journal disclosure practices are inconsistent and inadequate.192 Conflict of interest disclosures would be more effective if they included precise descriptions of the industry relationship along with the amount paid and included all payments from industry sponsors, not simply those deemed relevant by the author.193 In scientific publication, the inclusion of information about who funded a study, who planned and designed the study, who controls the data, who wrote the first draft, and whether final approval was required from an industry sponsor would enhance the transparency of disclosure practices. Transparency of potential conflicts of interest should extend to situations beyond the disclosures required for publication and speaking engagements. Medical schools should consider disclosure policies that require faculty who lecture or teach students, even preclinical students, to disclose ties to the industry that are relevant to the subject being discussed.194
In the end, there may not be a level of contact with the industry that is free from concerns regarding conflicts of interest.195,196 One recent suggestion flows from the recognition that eliminating conflicts of interest is neither possible nor always desirable and that the focus should be on managing the risks that arise.197 Hurst has suggested a strategy that combines disclosure of conflicts of interest with a 2-part test. First, when partnering with the industry, health care clinicians should only accept relationships in which the industry partner shares at least 1 of 2 primary goals with the professional: the provision of high-quality clinical care to existing patients or advancing the clinical care of future patients through the conduct of scientifically and ethically sound research. Second, explicitly identifying where the industry partner’s interests may not be entirely aligned with the health care clinician’s primary interests and proactively creating personal rules that will protect those primary interests when there is a conflict or misalignment.197
With regard to the receipt of gifts from the industry, the American Academy of Pediatrics (AAP) has endorsed the AMA guidelines, which do not prohibit gifts outright but offer the following basic principles for managing them:198
Physicians should decline cash gifts in any amount from an entity that has a direct interest in physicians’ treatment recommendations.
Physicians should decline any gifts for which reciprocity is expected or implied.
Physicians should accept an in-kind gift for the physician’s practice only when the gift is of minimal value and will directly benefit patients, including patient education.
Academic institutions and residency and fellowship programs may accept special funding on behalf of trainees to support their participation in professional meetings, including educational meetings, provided the program identifies recipients based on independent institutional criteria and funds are distributed to recipients without specific attribution to sponsors.
The AMA guidelines, although necessary, may not offer sufficient guidance to physicians or protection against the subtle persuasive influence of industry relationships. It is fairly clear that any gift, even de minimus noncash gifts, whether related to work and regardless of whether they benefit patients, do in fact come with “strings attached.” AAP guidance to health care clinicians would be to avoid any gift provided by an industry sponsor who sells a product that falls within the prescribing realm of the health care clinician.
In 2012, the ACOG also addressed the topic of physician relationships with the industry, stating: “Physicians have an obligation to seek the most accurate, up-to-date, evidence-based, and balanced sources of information about new products that they contemplate using.” The ACOG further stated that physicians should seek to minimize true and perceived conflicts of interest and understand that gifts, including CME credits, food, symposia, consulting arrangements, and social events, are intended to influence their decision making and behavior. Payments to defray costs to attend CME events should not be accepted directly from the company. The ACOG also strongly discourages participation in speakers’ bureaus and explicitly condemns ghostwriting as unacceptable.35
Similarly, in 2009, the IOM called for a ban on physician participation in industry-associated speakers’ bureaus and any other activity in which physicians are asked to present or promote content that is directly controlled by the industry. The IOM also recommended bans on gifts in any amount from the medical industry and advocated for the prohibition of direct industry funding of clinical practice guideline development and limits on the participation of those with conflicts of interest.90
Finally, in late 2020, the Department of Health and Human Services Office of the Inspector General issued a special fraud alert highlighting concerns about “companies offering or paying remuneration (and HCPs [health care professionals] soliciting or receiving remuneration) in connection with speaker programs.” The Office of the Inspector General warned both companies and health care professionals that such arrangements may, under certain circumstances, violate antikickback statutes. Cases in which health care professionals receive “generous compensation to speak at programs offered under circumstances that are not conducive to learning or speak to audience members who have no legitimate reason to attend” suggest that “one purpose of the remuneration to the health care professional speaker and attendees is to induce or reward referrals.”199 Physicians who currently participate in such programs or who are considering doing so should include the potential legal risk in addition to the other issues discussed in this report.
Health care clinicians must conduct their professional duties in a way that allows patients and the public to trust their actions and judgments. Health care clinicians must recognize that the interests of the industry and the duties of the health care clinician may, at times, significantly diverge and that relationships with the industry, even seemingly minor ones, have the potential to shape the decisions health care clinicians make on behalf of patients. Health care clinicians have an ethical duty to recognize the situations and marketing strategies that are designed to influence their selection of therapeutic options for their patients. At a minimum, health care clinicians should be cognizant of the techniques used to attempt to alter their behavior and guard against them.
Douglas S. Diekema, MD, MPH, FAAP
Committee on Bioethics, 2018–2019
Robert Macauley, MD, FAAP, Chairperson
Ratna Basak, MD, FAAP
Gina Marie Geis, MD, FAAP
Naomi Tricot Laventhal, MD, FAAP
Douglas J. Opel, MD, MPH, FAAP
Mindy B. Statter, MD, FAAP
Mary Lynn Dell, MD, DMin, American Academy of Child and Adolescent Psychiatry
Douglas S. Diekema, MD, MPH, FAAP, American Board of Pediatrics
David Shalowitz, MD, American College of Obstetricians and Gynecologists
Nanette Elster, JD, MPH, Legal Consultant
Past Committee Members
William R. Sexson, MD, MAB, FAAP (2017)
Ginny Ryan, MD, American College of Obstetricians and Gynecologists (2017)
Alison Baker, MS Florence Rivera, MPH
Dr Diekema reviewed the literature, drafted the initial manuscript, reviewed and revised the manuscript, approved the final manuscript as submitted, and agrees to be accountable for all aspects of the work.
This document is copyrighted and is the property of the American Academy of Pediatrics and its board of directors. All authors have filed conflict of interest statements with the American Academy of Pediatrics. Any conflicts have been resolved through a process approved by the board of directors. The American Academy of Pediatrics has neither solicited nor accepted any commercial involvement in the development of the content of this publication.
Technical reports from the American Academy of Pediatrics benefit from the expertise and resources of liaisons and internal (AAP) and external reviewers. However, technical reports from the American Academy of Pediatrics may not reflect the views of the liaisons or the organizations or government agencies that they represent.
The guidance in this report does not indicate an exclusive course of treatment or serve as a standard of medical care. Variations, taking into account individual circumstances, may be appropriate.
All technical reports from the American Academy of Pediatrics automatically expire 5 years after publication unless reaffirmed, revised, or retired at or before that time.