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  Vol. 163 No. 18, October 13, 2003 TABLE OF CONTENTS
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Are Gifts From Pharmaceutical Companies Ethically Problematic?

A Survey of Physicians

Allan S. Brett, MD; Wayne Burr, MD; Jamaluddin Moloo, MD, MPH

Arch Intern Med. 2003;163:2213-2218.

ABSTRACT

Background  Personalized pharmaceutical marketing to physicians, including the provision of gifts and sponsorship of educational and recreational activities, raises ethical issues. We sought to determine the degree to which physicians regarded common pharmaceutical marketing activities as ethically problematic, and to compare the views of experienced physicians and physicians-in-training.

Methods  A questionnaire that included 18 scenarios portraying interactions between physicians and the pharmaceutical industry was distributed to residents and faculty members at a US medical school.

Results  Most marketing activities were not thought to pose major ethical problems. Respondents tended to make distinctions about the ethical appropriateness of gifts on the basis of the monetary value and type of gift. Some respondents' views would be in violation of recent professional guidelines that address interactions between physicians and pharmaceutical companies. However, some respondents were troubled by activities that are permitted by professional guidelines. The responses of residents and faculty physicians were similar.

Conclusions  Despite the recent publicity about ethical problems in relationships between physicians and the pharmaceutical industry, inexperienced and experienced physicians at a single institution continue to have a rather permissive view about a variety of marketing activities.



INTRODUCTION
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 •Introduction
 •Methods
 •Results
 •Comment
 •Conclusions
 •Author information
 •References

THE MARKETING of drugs by the pharmaceutical industry is pervasive and has become a part of everyday life for most physicians. Virtually all medical journals include advertisements for drugs; pharmaceutical companies provide physicians with unsolicited information about new products; and brand-name drugs are marketed directly to consumers. However, many pharmaceutical marketing strategies are far more personal. They include the provision of gifts to physicians, sponsorship of educational and social activities for physicians, and cultivation of relationships between company representatives and physicians. The ethical issues raised by these strategies have been discussed increasingly in the recent medical literature. Many authors have concluded that pharmaceutical marketing activities pose serious problems,1-7 and medical professional organizations have elaborated guidelines on appropriate relationships between the pharmaceutical industry and physicians.8-11 Nevertheless, medical professionals continue to accept gifts and engage in a variety of activities sponsored by drug companies.

This gap between physician behaviors and a literature that generally criticizes these behaviors raises several questions about physicians' perspectives. Do physicians consider personalized pharmaceutical marketing tactics generally to be ethically acceptable despite the critical literature? Do physicians-in-training and experienced physicians have similar perspectives? Do physicians make distinctions between the acceptability of various marketing tactics? To address these questions, we surveyed physicians about whether common scenarios involving pharmaceutical marketing were ethically problematic. Unlike most previous surveys on this topic, we explicitly framed our questions in the language of ethics, and we sought to determine whether physicians make ethical distinctions on the basis of the monetary and educational value of gifts from pharmaceutical companies.


METHODS
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 •Introduction
 •Methods
 •Results
 •Comment
 •Conclusions
 •Author information
 •References

We devised the following 21-item questionnaire on ethical issues in pharmaceutical marketing:

  1. A drug company representative gives a practicing physician pens and pads carrying the name of a new drug. Is this scenario ethically problematic?
  2. A drug company representative gives a practicing physician a small medical textbook (eg, Washington Manual of Medical Therapeutics, value about $40). Is this scenario ethically problematic?
  3. A drug company representative gives a practicing physician a box of golf balls (value about $40). Is this scenario ethically problematic?
  4. A drug company representative gives a practicing physician several large medical textbooks (total value, about $500). Is this scenario ethically problematic?
  5. Same basic scenario as scenario 4, but the recipient of the textbooks is a first-year medical resident. Is this scenario ethically problematic?
  6. A drug company sponsors a dinner for practicing physicians at a nice restaurant. Dinner is followed by a speaker on a medical topic. The speaker receives an honorarium from the drug company, and his lecture includes a favorable discussion of a drug made by the company. Is this scenario ethically problematic?
  7. Same basic scenario as scenario 6, but the lecture mentions no products made by the company sponsoring the dinner. Is this scenario ethically problematic?
  8. A drug company pays the honorarium for a speaker at medical Grand Rounds at your institution; this sponsorship is disclosed to the audience. The lecture includes a favorable discussion of a drug made by the company. Is this scenario ethically problematic?
  9. Same basic scenario as scenario 8, but the lecture mentions no products made by the company sponsoring the Grand Rounds. Is this scenario ethically problematic?
  10. A drug company offers a practicing physician an all-expenses-paid weekend trip to a resort hotel (includes airfare, hotel, meals, and entertainment). The physician's only obligation is to spend several hours in seminars focusing on the company's products. Is this scenario ethically problematic?
  11. A drug company representative provides free samples of newly marketed drugs for a physician's office. Is this scenario ethically problematic?
  12. A drug company provides free lunch for a noon conference for residents and medical students; the conference is taught by one of the medical school faculty. At the beginning of the session, the drug company representative gives a 3-minute presentation on his company's newest drug. Is this scenario ethically problematic?
  13. Same basic scenario as scenario 12, but the drug representative does not give a formal presentation; instead, he chats informally with residents and students before and after the session. Is this scenario ethically problematic?
  14. Same basic scenario as scenarios 12 and 13 (the drug company buys the lunch), but no company representative is present at the session. Is this scenario ethically problematic?
  15. A drug company provides an unrestricted monetary gift ($1000) to the department of medicine; it can be used for any educational purpose. Is this scenario ethically problematic?
  16. A medical clinic staffed by residents has a small vacant office in which drug representatives are permitted to sit during clinic hours. Sometimes they bring new drug product information and snacks. During clinic hours, the residents can stop in to chat if they wish. Is this scenario ethically problematic?
  17. A drug company pays for a social event for residents (eg, a "happy hour" at a local bar/restaurant); several drug representatives attend. Is this scenario ethically problematic?
  18. Same basic scenario as scenario 17, but no representatives are present. Is this scenario ethically problematic?
  19. Do drug company representatives provide physicians with reliable information on the indications for, and effectiveness of, newly marketed drugs? (Please respond on a scale of 0-3, where 0 indicates not at all reliable and 3 indicates very reliable.)
  20. Do drug company representatives provide physicians with reliable information comparing the company's newly marketed drugs with similar drugs already on the market? (Please respond on a scale of 0-3, where 0 indicates not at all reliable and 3 indicates very reliable.)
  21. Do you think that the availability of drug samples in a physician's office (provided at no charge by the drug company) influences a physician's choice of drugs? (Please respond on a scale of 0-3, where 0 indicates not at all influential and 3 indicates very influential.)

For each of the 18 items describing scenarios in which physicians received gifts from drug company representatives or attended functions sponsored entirely or partly by drug companies, respondents noted the degree to which the scenario was ethically problematic on a 4-point Likert scale (0 indicates not problematic; 1, mildly problematic; 2, moderately problematic; and 3, very problematic). An introductory paragraph explicitly asked respondents to consider an activity as ethically problematic if it influences physician judgment inappropriately, poses conflicts of interest, or does not serve the best interests of the patients. The final 3 items in the questionnaire addressed the respondents' perceptions of the reliability of information provided by drug company representatives, and the influence of free drug samples on a physician's choice of drugs.

The questionnaire was distributed to all residents and full-time faculty in the Department of Internal Medicine at the University of South Carolina School of Medicine, Columbia. Nonresponders were contacted and asked to complete the survey. All responses remained anonymous.

We compared the responses of residents and faculty members for each scenario on the questionnaire. Because of the relatively small size of our department, we did not analyze subgroups of residents (eg, first- vs second- vs third-year) or faculty (eg, generalist vs specialist). In addition, we prospectively identified 9 pairs of scenarios for statistical comparison. In general, the 2 items within each of these paired scenarios differed in only 1 key respect. For example, in a comparison between scenarios 2 and 3, the value of the gift was held constant ($40), but the purpose of the gift varied (educational vs recreational). In contrast, for the comparison between scenarios 2 and 4, the purpose of the gift was held constant (educational), but the value varied ($40 vs $500).

We compared the responses of residents and attending physicians using the unpaired t and {chi}2 tests. We compared the responses to pairs of questions using the paired t and McNemar tests. Because of the large number of comparisons, we set statistical significance at P<.01.


RESULTS
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 •Methods
 •Results
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 •Conclusions
 •Author information
 •References

The questionnaire was circulated to 42 residents (representing all 3 years of training) and 51 faculty physicians. Thirty-nine residents (93%) and 37 faculty physicians (73%) completed the questionnaire. There were 18 women (46%) among resident respondents and 9 (24%) among faculty respondents.

The mean responses for each scenario are noted in Table 1. For most of the scenarios, mean responses were less than 1.0, indicating the range of not problematic to mildly problematic. For example, for 14 of the 18 scenarios, residents' mean responses were less than 1.0. For 10 of the 18 scenarios, faculty physicians' mean responses were less than 1.0. Residents and faculty physicians generated a mean response exceeding 1.0 for only the following 4 scenarios: the gift of golf balls, the dinner/lecture with a potentially biased speaker, the Grand Rounds with a potentially biased speaker, and the trip to a resort. At the prespecified level of P<.01, there was a significant difference between responses of residents and faculty for only the following 2 scenarios: the gift of a $500 textbook to a practicing physician and the presence of drug company representatives at a resident clinic. In both cases, faculty found these scenarios more ethically problematic than residents did.


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Table 1. Mean Responses*


The proportions of respondents indicating that a scenario was moderately or very problematic (ie, responses of 2 or 3 on the Likert scale) are given in Table 2. The general pattern of these results is similar to that of Table 1. Only 1 scenario (the trip to the resort) was deemed moderately to very problematic by a majority of both resident and faculty respondents. Resident and faculty responses differed significantly only for the scenario of drug company representatives at a resident clinic, which was considered more problematic by faculty than by residents.


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Table 2. Proportions Responding in Moderately or Very Problematic Range


Even for the items deemed most ethically acceptable (ie, those with low mean scores in Table 1), some physicians provided responses other than 0 (not problematic), suggesting at least some concern about ethical appropriateness. For example, 11 residents (28%) and 16 faculty (43%) provided responses other than 0 for gifts of pencils and pads. For the inexpensive textbook gift, 16 residents (41%) and 18 faculty (49%) provided responses other than 0.

To examine the ethical distinctions made by respondents, we compared the responses to 9 pairs of scenarios. A difference between responses to 2 scenarios is described as significant when a comparison of the mean scores from Table 1 or the proportions from Table 2 yielded P<.01.

Scenarios 2 and 3 compare an educational gift (textbook) and a recreational gift (golf balls), both valued at $40. Residents and faculty physicians found the recreational gift to be significantly more problematic than the educational gift.

Scenarios 2 and 4 compare 2 gifts of educational textbooks, one valued at $40 and the other at $500. Residents and faculty physicians found the more expensive gift to be more ethically problematic.

Scenarios 4 and 5 involve $500 worth of textbooks given to a first-year resident in one case and to a practicing physician in the other. Neither group of respondents noted a significant ethical difference between the 2 scenarios.

Scenarios 6 and 7 involve a free dinner followed by a speaker sponsored by a pharmaceutical company; however, the speaker discusses one of the company's drugs favorably only in the first scenario. Residents and faculty found the first scenario to be more problematic than the second.

Scenarios 8 and 9 involve medical Grand Rounds with a drug company–sponsored speaker; however, the speaker discusses one of the company's drugs favorably only in the first scenario. Residents and faculty found the first scenario to be more problematic than the second.

Scenarios 3 and 10 compare a relatively inexpensive recreational gift (golf balls) and an expensive recreational gift (trip to a resort). The faculty found them equally problematic, whereas the residents found the inexpensive gift less problematic than the expensive one.

Scenarios 12 through 14 involve a free lunch at a noon conference for residents, with progressively less visibility of the pharmaceutical representative. Residents perceived no ethical distinctions between the 3 scenarios. In contrast, the faculty found the scenario with the formal presentation by the representative to be significantly more problematic than the other 2 scenarios.

Scenarios 17 and 18 involve a social event (a happy hour at a local bar) sponsored by a drug company; however, company representatives are present only in the first scenario. The faculty, but not the residents, found the event to be more ethically problematic when the representative was present.

Questions 19 and 20 examined the perceived reliability of information provided by pharmaceutical representatives (Table 3). None of the differences between residents and faculty were statistically significant. However, resident and faculty respondents considered information regarding comparisons between new and old drugs to be significantly less reliable than information regarding drug indications and effectiveness.


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Table 3. Responses to Questions About Reliability of Information and Influence of Drug Samples*


Question 21 examined the perceived influence of drug samples on a physician's choice of drugs for patients. Although residents appeared more likely than faculty to view drug samples as very influential, the differences between faculty and residents were of borderline significance (P = .01 for comparison of means, and P = .02 for comparison of proportions).


COMMENT
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 •Introduction
 •Methods
 •Results
 •Comment
 •Conclusions
 •Author information
 •References

We presented a series of scenarios to examine physicians' beliefs regarding ethical issues associated with various pharmaceutical marketing activities. Our findings suggest 3 general conclusions.

First, physicians appeared to believe that most of these activities do not pose major ethical problems. On average, physicians rated most of the scenarios, which covered a wide spectrum of gifts and interactions with pharmaceutical representatives, as not ethically problematic or as mildly ethically problematic. Only about half of respondents found noneducational gifts from pharmaceutical representatives and social events to be moderately to very ethically problematic. Less than half of respondents found drug company–sponsored lectures with potentially biased speakers to be moderately to very problematic, even when a free restaurant meal preceded the lecture.

Second, physicians-in-training and experienced physicians had similar perspectives; differences between their responses were statistically significant for only 2 scenarios. Nevertheless, faculty scores were higher than resident scores for most items, suggesting that faculty may be somewhat more concerned about these ethical issues than residents are. In particular, for the 3 scenarios involving direct contact between residents and pharmaceutical representatives (scenarios 12, 16, and 17), there were significant differences or nonsignificant trends in which faculty expressed more concern than residents did. Medical educators should be aware of these findings, which suggest that physicians become comfortable with the culture of personalized pharmaceutical marketing at a very early stage of their careers.

Third, many physicians made distinctions about ethical appropriateness that reflected the value of a gift, the type of gift, and the extent to which an activity conveys potentially biased information. For example, residents and faculty believed that a recreational gift was more problematic than an educational gift of equal monetary value; a $500 educational gift was more problematic than a $40 educational gift; and drug company–sponsored lectures with favorable discussions of the company's products were considered more ethically problematic than lectures without such discussions. Although these distinctions may seem sensible at first glance, they are not shared by some critics who believe that all gifts from the pharmaceutical industry, regardless of monetary value or alleged purpose, are highly problematic.3-6

In recent years, published surveys have examined the attitudes of physicians regarding gifts from the pharmaceutical industry and encounters with pharmaceutical representatives.12-18 In general, surveyed physicians have been asked whether these activities are appropriate, and whether they compromise clinical judgment. A recent comprehensive review of this literature concluded that most physicians deny that gifts could influence their behavior, and that most physicians are equivocal about the appropriateness of gifts from pharmaceutical representatives.7 Only 1 previous survey, to our knowledge, explicitly asked physicians whether various marketing practices are ethical, but this survey was directed exclusively toward physicians who were chairpersons of hospital pharmacy and therapeutics committees.17 A recent study presented scenarios and reached conclusions that were similar to ours18; however, that survey included only residents and inquired about the appropriateness of promotional items. We used the language "Is this scenario ethically problematic?" because we wanted to learn how respondents view these activities from the perspective of personal or professional morality. In contrast, a question such as "Is this scenario appropriate?" could be construed from various perspectives (eg, law, etiquette, economics, and institutional policy) that might not always coincide with the perspective of ethics.

In 1991, the Council on Ethical and Judicial Affairs of the American Medical Association (AMA) published a statement entitled "Gifts to Physicians From Industry."8 This statement includes guidelines permitting gifts that are not "of substantial value," as long as the gifts "entail a benefit to patients" or are "related to the physician's work." More recently, recognizing that much gift giving from the pharmaceutical industry is not in compliance with these recommendations, the AMA issued more elaborate commentary on these guidelines and initiated a national educational effort to encourage closer adherence to the guidelines.9 The American College of Physicians (ACP) published a similar position paper in 1990,10 and updated it in 2002.11 The ACP, like the AMA, finds inexpensive gifts for office use, patient care, and education to be "generally acceptable."

Overall, the responses to our survey reflect the graded distinctions endorsed by the AMA and ACP, in which the type and monetary value of gifts are thought to determine their ethical propriety. However, we found some exceptions to this generalization. For example, nearly half of respondents rated purely recreational gifts to be not problematic or to be only mildly so. Physicians who accept these gifts would presumably be in violation of the AMA or ACP guidelines.

In our view, the AMA guidelines focus inordinately on fine distinctions regarding the value or type of gifts, and are not sufficiently concerned with the ultimate rationale for industry-sponsored gifts and activities, ie, to establish relationships with physicians that yield increased sales of a company's products. Several authors have written about the subliminal expectation for reciprocity that accompanies gift giving1-2,11; moreover, the subliminal effects of marketing and advertising are well known to business and industry. For example, pads and pens are of trivial value and can be construed as related to the physician's work. However, the guidelines fail to emphasize that distribution of these items, which are conspicuously labeled with the names of new drugs, is essentially a form of inexpensive advertising. When these items saturate the workplace, they increase product recognition and likely increase the probability that physicians will prescribe the advertised drug.

Our survey provides a hint that some physicians recognize this potential influence on behavior and may in fact be troubled by activities that the AMA and ACP find acceptable. For example, the guidelines permit gifts of pens and pads, low-cost textbooks, and inexpensive meals; yet nearly half of respondents gave these items a score other than 0, and thus found them to be at least mildly problematic. Thus, some physicians appear to believe that even inexpensive or educational gifts may influence clinical judgment or pose conflicts of interest.

The first and most important limitation of this study is that it was conducted only among internists in a single academic institution. Until these questions are examined in other practice settings and among physicians from other specialties, readers should be cautious about generalizing our results. However, because our response rate was high, the findings should be reasonably representative within our institution.

Second, we do not know the degree to which individual responses reflected the physicians' real-life experiences with these scenarios. We suspect that most of our respondents have had at least some experience with these activities as direct participants or through knowledge that they occur commonly. For example, internal medicine lunch conferences are sponsored by pharmaceutical companies at a secondary teaching hospital but not at our main teaching hospital; drug companies donate modestly priced textbooks for residents, but the books are usually distributed by our administrative staff; free drug samples are available in a faculty outpatient practice but not in the residents' continuity clinic; and drug companies bring outside speakers to our community fairly regularly for evening lectures with dinner. We have no reason to believe that the prevalence of interactions between physicians and pharmaceutical representatives in our community is dramatically different from the prevalence in other communities of similar size.

Third, we used a 4-point scale anchored with the terms not, mildly, moderately, and very ethically problematic. Although we believe that these categories capture an intuitively sensible gradient of ethical distinctions, the connotation of any single category might differ somewhat from person to person.


CONCLUSIONS
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 •Introduction
 •Methods
 •Results
 •Comment
 •Conclusions
 •Author information
 •References

We found that physicians at a single institution tended to hold fairly lenient views on the ethical propriety of a wide range of gifts and activities sponsored by the pharmaceutical industry. The views of physicians-in-training and experienced physicians were similar. Many physicians did not seem troubled by gifts and activities that are considered problematic by professional organizations such as the AMA and ACP. Nevertheless, some physicians appeared to believe that even gifts of minimal monetary value might pose ethical problems. In our view, the medical profession should focus more attention on the underlying rationale for personalized marketing to physicians by the pharmaceutical industry and less attention on fine distinctions among the specific gifts and activities themselves.


AUTHOR INFORMATION
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Corresponding author: Allan S. Brett, MD, Department of Medicine, University of South Carolina School of Medicine, 2 Medical Park, Suite 502, Columbia, SC 29203.

Accepted for publication December 6, 2002.

From the Department of Medicine, University of South Carolina School of Medicine, Columbia. The authors have no relevant financial interest in this article.


REFERENCES
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 •References

1. Chren MM, Landefeld CS, Murray TH. Doctors, drug companies, and gifts. JAMA. 1989;262:3448-3451. ABSTRACT
2. Shaughnessy AF, Slawson DC, Bennett JH. Separating the wheat from the chaff: identifying fallacies in pharmaceutical promotion. J Gen Intern Med. 1994;9:563-568. ISI | PUBMED
3. Waud DR. Pharmaceutical promotions: a free lunch? N Engl J Med. 1992;327:351-353. ISI | PUBMED
4. Margolis LH. The ethics of accepting gifts from pharmaceutical companies. Pediatrics. 1991;88:1233-1237. FREE FULL TEXT
5. Goodman B. It's time to just say no to drug reps. Soc Gen Intern Med Forum. 1999;22(7):10, 18.
6. Panush RS. Not for sale, not even for rent: just say no: thoughts about the American College of Rheumatology adopting a code of ethics. J Rheumatol. 2002;29:1049-1057. ISI | PUBMED
7. Wazana A. Physicians and the pharmaceutical industry: is a gift ever just a gift? JAMA. 2000;283:373-338. FREE FULL TEXT
8. Council on Ethical and Judicial Affairs of the American Medical Association. Gifts to physicians from industry [editorial]. JAMA. 1991;265:501. FULL TEXT | ISI | PUBMED
9. E-Addendum II: Council on Ethical and Judicial Affairs of the American Medical Association. Clarification on gifts to physicians from industry (E-8.061). Available at: http://www.ama-assn.org/ama/pub/category/4263.html. Accessed June 23, 2003.
10. American College of Physicians. Physicians and the pharmaceutical industry. Ann Intern Med. 1990;112:624-626.
11. Coyle SL. Physician-industry relations, I: individual physicians. Ann Intern Med. 2002;136:396-402. FREE FULL TEXT
12. Gibbons RV, Landry FJ, Blouch DL, et al. A comparison of physicians' and patients' attitudes toward pharmaceutical industry gifts. J Gen Intern Med. 1998;13:151-154. FULL TEXT | ISI | PUBMED
13. Banks JW, Mainous AG. Attitudes of medical school faculty toward gifts from the pharmaceutical industry. Acad Med. 1992;67:610-612. ISI | PUBMED
14. McKinney WP, Schiedermayer DL, Lurie N, Simpson DE, Goodman JL, Rich EC. Attitudes of internal medicine faculty and residents toward professional interaction with pharmaceutical sales representatives. JAMA. 1990;264:1693-1697. ABSTRACT
15. Lichstein PR, Turner RC, O'Brien K. Impact of pharmaceutical company representatives on internal medicine residency programs: a survey of residency program directors. Arch Intern Med. 1992;152:1009-1013. ABSTRACT
16. Brotzman GL, Mark DH. The effect on resident attitudes of regulatory policies regarding pharmaceutical representative activities. J Gen Intern Med. 1993;8:130-134. ISI | PUBMED
17. Poirier TI, Giannetti V, Guidici RA. Pharmacists' and physicians' attitudes toward pharmaceutical marketing practices. Am J Hosp Pharm. 1994;51:378-381. PUBMED
18. Steinman MA, Shlipak MG, McPhee SJ. Of principles and pens: attitudes and practices of medicine housestaff toward pharmaceutical industry promotions. Am J Med. 2001;110:551-557. FULL TEXT | ISI | PUBMED


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