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Checketts JX, Sims MT, Vassar M. Evaluating Industry Payments Among Dermatology Clinical Practice Guidelines Authors. JAMA Dermatol. 2017;153(12):1229–1235. doi:10.1001/jamadermatol.2017.3109
What is the extent of potential financial conflicts of interest among physicians who author dermatology clinical practice guidelines?
In this cross-sectional, descriptive study of 49 authors of guidelines published between 2013 and 2016, 40 received industry payments. Fifty-one percent received more than $10 000, 37% received more than $50 000, and 24% received more than $100 000. Of the 40 authors receiving payments, 22 (55%) did not accurately disclose industry relationships received between the initial literature search and guideline publication.
These findings raise concern about potential financial conflicts of interest in the dermatology guideline development process.
It is well documented that financial conflicts of interest influence medical research and clinical practice. Prior to the Open Payments provisions of the Affordable Care Act, financial ties became apparent only through self-disclosure. The nature of financial interests has not been studied among physicians who develop dermatology clinical practice guidelines.
To evaluate payments received by physicians who author dermatology clinical practice guidelines, compare disclosure statements for accuracy, determine whether pharmaceutical companies from which the authors received payments manufactured products related to the guidelines, and examine the extent to which the American Academy of Dermatology enforced their Administrative Regulations for guideline development.
Design, Setting, and Participants
Three American Academy of Dermatology guidelines published from 2013 to 2016 were retrieved. Double data extraction was used to record financial payments received by 49 guideline authors using the Open Payments database. Payments received by the authors from the date of the initial literature search to the date of publication were used to evaluate disclosure statement accuracy, detail the companies providing payments, and evaluate Administrative Regulations enforcement. This study is applicable to clinical practice guideline panels drafting recommendations, physicians using clinical practice guidelines to inform patient care, and those establishing policies for guideline development.
Main Outcomes and Measures
Our main outcomes are the monetary values and types of payments received by physicians who author dermatology guidelines and the accuracy of disclosure statements. Data were collected from the Open Payments database and analyzed descriptively.
Of the 49 authors evaluated, 40 received at least 1 reported industry payment, 31 accepted more than $1000, 25 accepted more than $10 000, and 18 accepted more than $50 000. Financial payments amounted to a mean of $157 177 per author. The total reimbursement among the 49 authors from 2013 to 2015 was $7 701 681. Of the 40 authors receiving payments, 22 did not accurately disclose industry relationships. Authors received payments from companies with products directly related to the guideline topic. Violations to the Administrative Regulations were found.
Conclusions and Relevance
Dermatology clinical practice guideline authors received sizable industry payments and did not completely disclose these payments. The American Academy of Dermatology policies may benefit from stricter enforcement or the adoption of new standards.
Physicians and insurance companies use clinical practice guidelines (CPGs) to make decisions about patient care.1 These guidelines include recommendations derived from a systematic review of research evidence and careful consideration of benefits and harms associated with medical interventions. Ideally, guidelines should be free from biased recommendations and should consider patients’ best interests; however, panels often include physicians with financial ties to pharmaceutical or medical device industries.1 Evidence suggests that physicians receiving industry payments are likely to assess clinical trials more favorably.2 Small payments, such as gifts or meals provided by industry, may even increase the likelihood that physicians will prescribe brand-name drugs.3,4 For these reasons, the Institute of Medicine’s Committee on Conflicts of Interest in Medical Research, Education, and Practice states, “conflicts of interest threaten the integrity of scientific investigations, the objectivity of professional education, the quality of patient care, and the public’s trust in medicine.”5
To increase transparency of financial relationships between physicians and industry, the Sunshine provisions of the Affordable Care Act (hereinafter referred to as Open Payments)6,7 make all industry payments more than $10 publically available. In 2014, dermatologists received more than $34 million in industry payments, and the top 1% received at least $93 622.8 The median payment per physician was $298.8 Making Open Payments data publically available allows for more careful monitoring of physicians’ ties to industry, especially among physicians participating in developing CPGs. The purpose of this study is to evaluate the monetary amounts and types of payments received by authors of the American Academy of Dermatology (AAD) CPGs. We also assess the accuracy of authors’ disclosure statements and whether the pharmaceutical companies from which authors received payments manufactured products related to the guideline topics. Finally, we investigate the extent to which the AAD enforced their Administrative Regulations for guideline development.
This cross-sectional study investigated the nature of industry payments made to CPG authors. This study was not subject to institutional review board oversight because it did not meet the regulatory definition of human subject research as defined in 45 CFR 46.102(d) and (f) of the Department of Health and Human Services’ Code of Federal Regulations.9 This cross-sectional study is registered on the University Hospital Medical Information Network Clinical Trial Registry (UMIN-CTR, UMIN000029100). We consulted the study by Mitchell et al2 when developing our methodology.
One of us (J.X.C.) searched for CPGs in December 2016 using the AAD website and the Agency for Healthcare Research and Quality’s National Guideline Clearinghouse.10 To qualify for inclusion, dermatology guidelines had to be published or revised between 2013 and 2016 and contain a listing of authors involved in their development. Only guidelines produced by US citizens were included, because only US-based physicians are subject to the Open Payments Provision. The time frame of 2013 to 2016 was used, since 2013 was the first year that industry payment data were made available publically, with 2015 data being most current. All payment years were included (2013-2015) for each guideline. Rosenfeld and Shiffman11 estimated that guideline development takes approximately 1 year from conception to publication. The AAD and other authoritative bodies, such as the Institute of Medicine, recommend or require authors to avoid receiving industry financial conflicts of interest (FCOIs) in the year following guideline publication.1,12 This timeframe permitted the evaluation of industry relationships prior to guideline development as well as payments received following guideline publication. Guideline authors can receive notoriety from participating in guideline panels. As a result, authors can receive sizable speaking fees, resulting in considerable financial gains.13
The “identifying information” within each guideline was used to locate authors. Physicians’ names were thus extracted and copied into Microsoft Excel by one of us (J.X.C.), who manually entered each author’s last name into the Open Payments search box. In cases of duplicate search results, middle initials were used. Authors were also matched by company and location. If physicians’ names did not return from searches or did not match the information provided by Open Payments, then they were considered to have received $0 in industry payments.
Following data extraction, one of us (M.T.S.) independently reviewed data for accuracy by reentering each physician’s name into Open Payments, selecting the correct physician, and verifying payment data. Any discrepancies were flagged and resolved jointly between the 2 investigators. Open Payment data are classified as follows14:
General payments: These include consulting fees, speaking fees, honoraria, gifts, entertainment, food and beverage, travel and lodging, and education.
Research payments: Payments associated with a research study, including basic and applied research, and product development.
Associated research payments: Funding for a research project or study where the physician is named as a principal investigator.
Ownership: Ownership and investment interest in companies, which describes both the actual dollar amount invested and the value of the ownership or investment interest.
Subcategories of reimbursement were classified by year. Means, medians, and sums were calculated by year and subcategory using Microsoft Excel (J.X.C. performed calculations, and M.T.S. independently verified them).
Next, disclosure information was retrieved from the guidelines to evaluate whether the authors accurately reported the companies making payments found in Open Payments. The guidelines do not list the date of initiation or the authors’ dates of service; however, they do provide the end date of the literature search. We used this as the start date to evaluate discrepancies in disclosures because each author would have submitted a disclosure statement before this date to be considered for appointment. The date of publication was used as the end date. The AAD’s Administrative Regulations state that each author’s disclosure statement is updated throughout guideline development. Because disclosures are continuously updated, the dates used for our search improve accuracy and relevance of potential FCOIs as any discrepant payments would be received during guideline development. Using this time frame (date of final search to publication date as listed in Table 1) is a conservative approach that ensures no authors were inaccurately included as having discrepant disclosures. The authors’ names and the disclosed conflict of interest (COI) information were extracted (by J.X.C.), including the company’s or organization’s name and type of COI. Only payments received after the final date of the literature search and before the publication date were included. Food and beverage payments were not considered discrepancies.
Open Payments was used to evaluate the extent to which the AAD enforced their Administrative Regulations for guideline development. The Administrative Regulations consider FCOIs as “any financial or other incentive which can reasonably be perceived by an independent observer as a potential source of bias within the guideline scope.”12 As of April 10, 2017, the AAD Administrative Regulations state the following standards evaluable by our study:
“A Work Group must minimally include 51% of experts without relevant financial conflict of interest.”
“The Chair of the Work Group is prohibited from having any relevant financial conflict of interest, unless the expertise and leadership is deemed necessary by the Clinical Guidelines and Research Committee. In this instance, a co-chair with no relevant financial conflict of interest will be appointed. The chair or co-chair must also remain free of relevant conflict of interest for at least one year after guideline publication.”
“Disclosure updates will be obtained from all Work Group members, medical writer(s) and Academy staff at regular intervals throughout the development process. The guideline text will indicate the full disclosure and recusal history for all listed authors to include the Work Group, Clinical Guidelines and Research Committee Chair or named liaison, and affiliated staff.”
“Work Group members for whom a relevant conflict has been identified will be required to recuse from discussions, drafting, and voting on clinical recommendations or guideline text related to the identified conflict, unless otherwise requested by the Work Group Chair.”
Last, we evaluated whether the companies from which guideline authors received payments manufactured products related to their guideline topics. The methods of inclusion for this aim are identical to aim 1 (2013-2015) and for the same reason. Each author’s name was searched in Open Payments and recorded the companies disbursing payments to CPG authors (by J.X.C.).
Six guidelines produced by the AAD were retrieved, which included 107 authors. Three of the 5 were subguidelines, listing identical authors. These 3 were considered as 1 guideline. Three guidelines, representing 49 CPG authors, comprised our final sample (Table 2).15-17
Of the 49 CPG authors contributing to CPG development, 40 (81.6%) received at least 1 reported industry payment; 31 (63.3%) accepted more than $1000; 25 (51%) accepted more than $10 000; 18 (36.7%) accepted more than $50 000; and 12 (24%) accepted more than $100 000. The authors received a mean (SD) of $157 177 ($332 829) per author. The median total of received industry payments was $33 247. The total payment disbursed to the 49 physicians from 2013 to 2015 was $7 701 681. In the atopic dermatitis guideline published in 2014 (the only guideline for which we could evaluate payments before and after guideline development) there was a 473% increase (from $221 293 to $1 268 462) from 2013 and 2014, and a 97% increase (from $1 268 462 to $2 502 444) from 2014 to 2015 among the authors.
For general payments, CPG authors who accepted payments received a mean (SD) of $83 703 ($167 441), with a median of $10 150 (Figure). Forty CPG authors (81.6%) received general payments totaling $3 348 129. For authors receiving research payments, the mean was $11 250 ($16 055), with a median of $7275. Eleven CPG authors (22%) received research payments amounting to $123 759. Authors receiving associated research payments had a mean of $302 128 ($325 250), and a median of $143 095 per physician. Fourteen CPG authors (29%) received associated research payments totaling $4 229 793. All authors who received research and/or associated research payments also received general payments. There were no CPG authors with reported ownership interests.
For the second aim, the accuracy of disclosures was evaluated. Of the 40 authors who received industry payments, 22 disclosure statements (55%) were discrepant with Open Payments. Of these, 6 (27%) reported no FCOIs yet received significant industry payments. Sixteen (73%) reported some FCOIs; however, these authors received substantial payments from companies not listed in their disclosure statements (Table 1). Undisclosed payments ranged from nearly $1000 to $250 000 and comprised research, travel and lodging, education, consultant fees, and “other” fees.
Several inconsistencies were found in the extent to which the AAD enforced its Administrative Regulations for guideline development. Specifically, more than 70% of authors received payments in all CPGs, which is much higher than the allowable 51% stated in the Regulations. Fifty-one percent of authors received at least $10 000. Two guidelines had 2 co-chairs; 1 guideline had a single chair. The single chair accurately reported no FCOIs. In the guidelines with co-chairs, notable discrepancies were found. Both chairs of the atopic dermatitis guideline had discrepancies between their disclosure statement and Open Payments data. One chair reported some FCOIs; however, they also received nearly $50 000 in payments from companies not listed in the disclosure statement; the second chair reported no FCOIs yet received more than $3000 in industry payments prior to guideline publication. One chair received more than $100 000 in the year following guideline development, and the other received more than $50 000 in that year. Both chairs received payments more than $50 000 from Anacor (which states that its flagship product is a solution for treating atopic dermatitis)18 following guideline publication. For the acne guideline, 1 co-chair accurately reported no FCOIs; however, the other received payments from companies not accounted for in the disclosure statement. This co-chair also received almost $100 000 in research and other payments from a company in which the disclosure statement listed only that the co-chair “serves on the advisory board.” Two authors of the office-based surgery CPG did not have a published disclosure statement. One received nearly $20 000 during guideline development and $125 000 in industry payments leading up to guideline development.
There was a small number of companies making payments to a large proportion of authors. Of 40 authors receiving payments, 22 (55%) received payments from Anacor and Galderma, 16 (40%) from Valeant, and 13 (33%) from Celgene, GlaxoSmithKline, and Allergan (Table 3). Anacor’s leading product in development is a treatment for atopic dermatitis.18 Galderma considers treatments for atopic dermatitis and acne among its major brands.19 Valeant’s “key products” include treatments for atopic dermatitis and acne.20 Allergan is conducting a phase 3 trial for a potential acne medication, and this trial was in progress during development of the acne guideline.21,22 This company also produces a botulinum toxin drug, a focus area of the office-based surgery guideline. GlaxoSmithKline’s company, Stiefel, has product lines for acne and atopic dermatitis.23 The top companies that made payments to the office-based surgery guideline authors sell products relevant to treatments or conditions treated by the procedures discussed in the guideline24-26 (eg, Mohs surgery, laser treatments, topical and/or local anesthetics, photodynamic therapy, and botulinum toxin injections).
Our study suggests that (1) dermatology CPG authors received sizable industry payments from companies relevant to the guideline topics, (2) disclosure forms were discrepant when compared with Open Payments data, and (3) the AAD Administrative Regulations were not strictly enforced.
In 2016, Feng et al8(p1312) reported that 73% of all dermatologists accepted industry payments, with 63% receiving less than $500, concluding that industry relationships are “varied, complex, and robust.” We found that 82% of dermatology CPG authors received industry payments, most often by companies that manufacture products relevant to the guidelines. The average payment received by each CPG author was $157 177 over the 3-year span and totaled $7 701 681 across the 49 authors. Associated research payments were the largest source. Because most research funding comes from industry, many clinicians who perform clinical trials receive payments to support the work of the clinical trial.2 Academic medical centers with physicians performing clinical research supported by industry and universities have safeguards to protect against bias in research. General payments, which do not support clinical research vetted by the university, were most frequently received by these CPG authors, which raises concern about CPG development because evidence suggests that small gifts, meals, or items can affect prescribing practices.3
The AAD reports that all guidelines adhere to its Administrative Regulations stemming from the Council of Medical Specialty Societies recommendations.12 However, there seems to be lack of enforcement of these standards. More than 51% of authors received industry payments, a large portion of the authors received payments from companies relevant to guideline topics, and most disclosure statements were discrepant when compared with Open Payments. In 2017, Andreatos et al27 evaluated 223 CPGs, which included 1329 authors with Open Payments data. Of these, 523 (39%) received more than $5000 in industry payments, and only 56 (11%) accurately disclosed FCOIs. In comparison with Andreatos et al,27 we found that 27 authors (55%) received more than $5000 in industry payments, and of the 40 authors receiving industry payments, only 18 (45%) accurately disclosed them. Two authors did not have disclosure statements, raising questions about whether such statements are actually reviewed on multiple occasions per AAD Administrative Regulations. Our findings, in combination with those of Andreatos et al,27 suggest the need for more careful monitoring of disclosures.
Our findings have implications on CPG development and FCOI disclosure policies. Although the AAD has policies in place to minimize bias owing to FCOIs, our findings raise questions regarding the enforcement of these policies. It is recommended that the AAD take action to increase compliance with its Administrative Regulations and consider new policies to reduce the risk of bias during CPG development.
Disclosure statements should include detailed, publicly available disclosures, including the amounts received prior to, during, and 2 years following CPG development. If the AAD wants to improve transparency, then 5 years of disclosures from authors prior to guideline development are recommended, which is the policy of the American Pain Society.28 In addition, the accuracy of disclosure statements needs to be verified using Open Payments. The Administrative Regulations requires recusal of members with relevant FCOIs and states that recusals will be listed in the guideline; however, our study located only 8 instances of recusal despite the large amount of relevant FCOIs among authors. An additional recommendation is limiting authors with FCOIs to one-third rather than one-half of the guideline committee. This may reduce the risk of bias, streamline guideline development, and still allow experts in the field to contribute to guideline development. The Infectious Diseases Society’s antitrust settlement concerning the development of Lyme disease guideline required open and transparent practices during the guideline review, including open selection of the chair and panel members, independent review of FCOIs by a medical ethicist, a public call for submission of evidence, and a public evidence hearing.29 Consideration of these practices may aid future CPG development by the AAD and may bring CPGs closer to the transparency and trustworthiness that patients expect and deserve.30
Our study’s limitations include possible inaccuracies of Open Payments data as well as the possibility of human data interpretation error. Multiple physicians within the Open Payments database had the same name, which could lead to potential data extraction inaccuracies. In some cases, physicians were not retrievable during the searches. This could mean the physician had not received financial compensation, or alternatively, that parties responsible for reporting these payments failed to report them.31 If the latter, data will be misleading since there is no public record regarding the amount that physicians actually received. In addition, Open Payments allots physicians a 45-day period to dispute any payments sent to Open Payments in their name. However, only 4.8% of physicians successfully reviewed their data in the program’s first year,32,33 meaning it is unlikely that potential inaccuracies were amended. Because Open Payments only reports data from US-based physicians, our results are not generalizable outside of the United States. Finally, there is no way to determine the extent to which each FCOI affected the physician’s decision-making or if the physicians’ FCOIs influenced the CPGs they developed.
Dermatology CPG authors received sizable industry payments. There were inaccuracies in disclosure forms when compared with Open Payments data and a lack of enforcement of AAD guideline Administrative Regulations. Changes are recommended for panel composition, disclosure policies, and development practices to promote transparency and minimize bias resulting from industry FCOIs.
Corresponding Author: Jake X. Checketts, BS, Oklahoma State University, Center for Health Sciences, 1111 W 17th St, Tulsa, OK 74107 (email@example.com).
Accepted for Publication: June 18, 2017.
Published Online: October 18, 2017. doi:10.1001/jamadermatol.2017.3109
Author Contributions: Mr Checketts and Mr Sims had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: All authors.
Acquisition, analysis, or interpretation of data: Checketts, Sims.
Drafting of the manuscript: All authors.
Critical revision of the manuscript for important intellectual content: All authors.
Statistical analysis: All authors.
Obtained funding: Checketts.
Administrative, technical, or material support: Checketts.
Study supervision: Checketts, Vassar.
Conflict of Interest Disclosures: None reported.