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Letters to the Editor   |    
Conflict of Interest, Bias, and Objectivity in Research Articles
Adam J. Starr, MD; Drake S. Borer, MD; Charles M. Reinert; Thomas A. Einhorn, MD
View Disclosures and Other Information
Corresponding author: Adam J. Starr, MD, Department of Orthopaedic Surgery, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-8883 E-mail address: adam.starr@utsouthwestern.edu Deputy Editor for Current Concepts Reviews, The Journal of Bone and Joint Surgery, Needham, Massachusetts

The Journal of Bone & Joint Surgery.  2001; 83:1429-a-1431 
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To The Editor:
We enjoyed the recent Current Concepts Review "The Use of Low-Intensity Ultrasound to Accelerate the Healing of Fractures" (83-A: 259-70, Feb. 2001), by Rubin et al. It sounds like ultrasound is the best thing since sliced bread—and it may be, but we were a little disappointed with the references.
The section entitled "The Ability of Ultrasound to Accelerate Fracture-Healing in the Clinical Setting" cited twelve sources. Two of these were articles published in The Journal of Bone and Joint Surgery. The first, by Heckman, Ryaby, McCabe, Frey, and Kilcoyne1, found that ultrasound made tibial fractures heal faster. The second, by Kristiansen, Ryaby, McCabe, Frey, and Roe2, found that ultrasound made distal radial fractures heal faster.
Since The Journal requires disclosure of potential conflicts of interest, the reader is told that for both papers, "One or more of the authors have received or will receive benefits for personal or professional use from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was Exogen, Incorporated."1,2 The articles also show that Ryaby and McCabe are employees of Exogen and that Frey is an employee of Health Products Development, Inc. The reader is not told what form of support Exogen gave, how much support, or to whom it was given.
A third article, published in Clinical Orthopaedics and Related Research, by Cook, Ryaby, McCabe, Frey, Heckman, and Kristiansen3 and cited in this section, was apparently a second look at the patients from the aforementioned two studies. Cook et al. showed that ultrasound makes fractures in smokers heal better. Since Clinical Orthopaedics and Related Research doesn’t require financial disclosure, the reader cannot find out whether Exogen supported this research as well.
In the Current Concepts Review by Rubin et al., another article cited in the clinical section, by Mayr, Frankel, and Rüter4, apparently analyzed information from Exogen’s database of patients who had received the ultrasound device. This article states that "the device . . . is provided by Exogen." So not only did Exogen provide the devices, they provided the study data as well. No financial disclosure was given, as Archives of Orthopaedic and Trauma Surgery does not require it.
One reference was a case report of one patient5, again with no financial disclosure. Another reference, published in Clinical Orthopaedics and Related Research, by Strauss and Gonya6, reported the successful use of ultrasound in two patients with Charcot arthropathy who underwent revision ankle fusion surgery. Again, no financial disclosure was given.
Other references cited were abstracts presented at an annual meeting of the International Society for Fracture Repair that were later published in the Journal of Orthopaedic Trauma7,8. That journal requires financial disclosure from its authors, but the abstracts contain no such information. Both abstracts showed positive effects of ultrasound. Ryaby was an author of both abstracts.
Two other studies, both by Emami et al., were cited: one was published in the Journal of Orthopaedic Trauma9 and one, in Clinical Orthopaedics and Related Research10. The first states that "Exogen Inc. provided the ultrasound devices used in this study. The authors have received nothing else of value."9 The second article provides no information about financial support of the study. Both studies by Emami et al. were prospective, randomized, blinded, and placebo-controlled. Both showed no difference in healing between the patients who were treated with ultrasound and those who were not.
It may be that ultrasound has an enormous beneficial effect on fracture-healing, and we realize that industry support of research doesn’t necessarily mean that the research is flawed or biased, but the fact that an employee of a company that sells ultrasound devices co-authored the Current Concepts Review raises doubt about the potential for bias. Other investigators have shown that the conclusions of review articles are strongly associated with the affiliations of their authors11. It is also possible that interactions between physicians and industry may affect prescribing and professional behavior12.
Given the shrinking budget for research, it is inevitable that industry will become more important in the funding of clinical studies. It seems likely that the increasing involvement of industry in the design, execution, analysis, and reporting of clinical research will increase the risk that doctors will be fooled occasionally. We need to be vigilant.
Would it have been possible for the Editorial Board of The Journal to find a group of qualified authors who were not financially tied to the device that they were reviewing? One would think that if the thing worked all that well, one would be able to find a reviewer who wasn’t beholden to the company that sells the device.
Readers rely on The Journal of Bone and Joint Surgery to be objective. We’re not certain that this Current Concepts Review passes muster in terms of objectivity.
T.A. Einhorn replies:
Drs. Starr, Borer, and Reinert raise important and timely issues regarding conflict of interest in the medical literature and both the value and the potential failure of disclosure. In this Current Concepts Review, full disclosure by the authors is recognized, but concern is raised regarding inclusion as an author of an individual who is employed by the company (Exogen, Inc.) that provided research funds for some of the studies cited in the review and the use of references taken from sources in which there is no disclosure of conflict of interest.
As many of the so-called cutting-edge technologies in orthopaedic science emanate from pharmaceutical and biotechnology companies, there is concern that the quality and reporting of new data are potentially influenced by corporate agendas. Indeed, some of the most critically reviewed clinical and basic-science journals consistently publish articles written exclusively by authors who are employed by such companies. The Journal of Bone and Joint Surgery is not alone in its ongoing need to address conflict of interest.
Most of the time, when an article reports the results of a clinical or basic-science research study, one can carefully examine the experimental design, the methods used for reducing bias, the statistical methods used for analyzing data, and the conclusions as supported by those data. However, with a review article, the ability to use these criteria is limited. Indeed, many of the references cited in the review by Rubin et al. were from sources in which conflict of interest is not policed. This point, I believe, is particularly important. While I believe it is necessary for editors and readers to rely on disclosure of conflict of interest in published articles, our lack of attention to the use of sources in which conflict of interest is not disclosed requires reexamination, although exploring this would add a layer of complexity to the editorial review process.
One of the suggestions made by Drs. Starr, Borer, and Reinert is that the Editorial Board seek authors who do not have any conflict of interest and therefore could be more objective in writing an article such as the one in question. I disagree with this recommendation. Frequently the so-called thought leaders in our field are called upon to provide critically important information to companies developing our next generation of advanced technologies, and these individuals have every right to be compensated for their time and expertise, as well as to be permitted to pursue their academic goals without a penalty for contributing to a corporate or commercial process. This is where honesty and trust among clinicians and scientists are required.
As new advances in orthopaedic care continue to evolve, the issue of conflict of interest in the reporting of the results of basic-science studies and clinical trials published in The Journal will continue to be reevaluated and redefined. As the Deputy Editor responsible for the editorial preparation of the Current Concepts Review in question, I can assure our readers that exceptional attention was paid to issues of bias in this article. I do not believe that exclusion of an author because he or she is associated with a company is fair or appropriate. On the other hand, I do agree that we and the editors of other journals can and should do a better job of establishing policies on the use of reference materials taken from sources that do not require conflict-of-interest disclosure. On that particular point, I wish to thank Drs. Starr, Borer, and Reinert for their concerns and for making an excellent suggestion for the ongoing reevaluation of the editorial process at The Journal.
Heckman JD, Ryaby JP, McCabe J, Frey JJ,Kilcoyne FR. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J Bone Joint Surg Am,1994;76: 26-34. 7626  1994  [PubMed]
 
Kristiansen TK, Ryaby JP, McCabe J, Frey JJ,Roe LR. Accelerated healing of distal radial fractures with the use of specificlow-intensity ultrasound. A multicenter, prospective, randomized, double-blind, placebo-controlled study. J Bone Joint Surg Am.,1997;79: 961-73. 79961  1997  [PubMed]
 
Cook SD, Ryaby JP, McCabe J, Frey JJ, Heckman JD,Kristiansen TK. Acceleration of tibia and distal radius fracture healing in patients who smoke. Clin Orthop,1997;337: 198-207. 337198  1997  [PubMed][CrossRef]
 
Mayr E, Frankel V,Rüter A. Ultrasound—an alternative healing method for nonunions?. Arch Orthop Trauma Surg, 2000;120: 1-8. 1201  2000  [PubMed]
 
Sato W, Matsushita T,Nakamura K. Acceleration of increase in bone mineral content by low-intensity ultrasound energy in leg lengthening. J Ultrasound Med, 1999;18: 699-702. 18699  1999  [PubMed]
 
Strauss E,Gonya G. Adjunct low intensity ultrasound in Charcot neuroarthropathy. Clin Orthop,1998;349: 132-8. 349132  1998  [PubMed][CrossRef]
 
Lane JM, Peterson M, Ryaby JP,Testa F. Ultrasound treatment in 2126 fractures. In: Proceedings of the Sixth Annual Meeting of the International Society for Fracture RepairStrasbourg. J Orthop Trauma,1999;13: 313.. 13313  1999  [CrossRef]
 
Strauss E, Ryaby JP,McCabe J. Treatment of Jones’ fractures of the foot with adjunctive use of low-pulsed ultrasound stimulation. In: Proceedings of the Sixth Annual Meeting of the International Society for Fracture RepairStrasbourg. J Orthop Trauma,1999;13: 310.. 13310  1999  [CrossRef]
 
Emami A, Petren-Mallmin M,Larsson S. No effect of low-intensity ultrasound on healing time of intramedullary fixed tibial fractures. J Orthop Trauma,1999;13: 252-7. 13252  1999  [PubMed][CrossRef]
 
Emami A, Larsson A, Petren-Mallmin M,Larsson S. Serum bone markers after intramedullary fixed tibial fractures. Clin Orthop,1999;368: 220-9. 368220  1999  [PubMed]
 
Barnes DE,Bero LA. Why review articles on the health effects of passive smoking reach different conclusions. JAMA, 1998;279: 1566-70. 2791566  1998  [PubMed][CrossRef]
 
Wazana A. Physicians and the pharmaceutical industry: is a gift ever just a gift?. JAMA,2000;283: 373-80. 283373  2000  [PubMed][CrossRef]
 

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Heckman JD, Ryaby JP, McCabe J, Frey JJ,Kilcoyne FR. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J Bone Joint Surg Am,1994;76: 26-34. 7626  1994  [PubMed]
 
Kristiansen TK, Ryaby JP, McCabe J, Frey JJ,Roe LR. Accelerated healing of distal radial fractures with the use of specificlow-intensity ultrasound. A multicenter, prospective, randomized, double-blind, placebo-controlled study. J Bone Joint Surg Am.,1997;79: 961-73. 79961  1997  [PubMed]
 
Cook SD, Ryaby JP, McCabe J, Frey JJ, Heckman JD,Kristiansen TK. Acceleration of tibia and distal radius fracture healing in patients who smoke. Clin Orthop,1997;337: 198-207. 337198  1997  [PubMed][CrossRef]
 
Mayr E, Frankel V,Rüter A. Ultrasound—an alternative healing method for nonunions?. Arch Orthop Trauma Surg, 2000;120: 1-8. 1201  2000  [PubMed]
 
Sato W, Matsushita T,Nakamura K. Acceleration of increase in bone mineral content by low-intensity ultrasound energy in leg lengthening. J Ultrasound Med, 1999;18: 699-702. 18699  1999  [PubMed]
 
Strauss E,Gonya G. Adjunct low intensity ultrasound in Charcot neuroarthropathy. Clin Orthop,1998;349: 132-8. 349132  1998  [PubMed][CrossRef]
 
Lane JM, Peterson M, Ryaby JP,Testa F. Ultrasound treatment in 2126 fractures. In: Proceedings of the Sixth Annual Meeting of the International Society for Fracture RepairStrasbourg. J Orthop Trauma,1999;13: 313.. 13313  1999  [CrossRef]
 
Strauss E, Ryaby JP,McCabe J. Treatment of Jones’ fractures of the foot with adjunctive use of low-pulsed ultrasound stimulation. In: Proceedings of the Sixth Annual Meeting of the International Society for Fracture RepairStrasbourg. J Orthop Trauma,1999;13: 310.. 13310  1999  [CrossRef]
 
Emami A, Petren-Mallmin M,Larsson S. No effect of low-intensity ultrasound on healing time of intramedullary fixed tibial fractures. J Orthop Trauma,1999;13: 252-7. 13252  1999  [PubMed][CrossRef]
 
Emami A, Larsson A, Petren-Mallmin M,Larsson S. Serum bone markers after intramedullary fixed tibial fractures. Clin Orthop,1999;368: 220-9. 368220  1999  [PubMed]
 
Barnes DE,Bero LA. Why review articles on the health effects of passive smoking reach different conclusions. JAMA, 1998;279: 1566-70. 2791566  1998  [PubMed][CrossRef]
 
Wazana A. Physicians and the pharmaceutical industry: is a gift ever just a gift?. JAMA,2000;283: 373-80. 283373  2000  [PubMed][CrossRef]
 
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These activities have been planned and implemented in accordance with the Essential Areas and policies of the Accreditation Council for Continuing Medical Education (ACCME) through the joint sponsorship of the American Academy of Orthopaedic Surgeons and The Journal of Bone and Joint Surgery, Inc. The American Academy of Orthopaedic Surgeons is accredited by the ACCME to provide continuing medical education for physicians.
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