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Epidemiology

Interactions with the pharmaceutical industry and the practice, knowledge and beliefs of medical oncologists and clinical haematologists: a systematic review

Abstract

Background

No previous review has assessed the extent and effect of industry interactions on medical oncologists and haematologists specifically.

Methods

A systematic review investigated interactions with the pharmaceutical industry and how these might affect the clinical practice, knowledge and beliefs of cancer physicians. MEDLINE, Embase, PsycINFO and Web of Science Core Collection databases were searched from inception to February 2021.

Results

Twenty-nine cross-sectional and two cohort studies met the inclusion criteria. These were classified into three categories of investigation: (1) extent of exposure to industry for cancer physicians as whole (n = 11); (2) financial ties among influential cancer physicians specifically (n = 11) and (3) associations between industry exposure and prescribing (n = 9). Cancer physicians frequently receive payments from or maintain financial ties with industry, at a prevalence of up to 63% in the United States (US) and 70.6% in Japan. Among influential clinicians, 86% of US and 78% of Japanese oncology guidelines authors receive payments. Payments were associated with either a neutral or negative influence on the quality of prescribing practice. Limited evidence suggests oncologists believe education by industry could lead to unconscious bias.

Conclusions

There is substantial evidence of frequent relationships between cancer physicians and the pharmaceutical industry in a range of high-income countries. More research is needed on clinical implications for patients and better management of these relationships.

Registration

PROSPERO identification number CRD42020143353.

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Data availability

No additional data is available.

References

  1. Waters R and Urquhart L (Eds). World Preview 2019, Outlook to 2024. 12th Ed. London, UK: EvaluatePharma®; 2019.

  2. Wazana A. Physicians and the pharmaceutical industry: is a gift ever just a gift? J Am Med Assoc. 2000;283:373–80.

    Article  CAS  Google Scholar 

  3. Lotfi T, Morsi RZ, Rajabbik MH, Alkhaled L, Kahale L, Nass H, et al. Knowledge, beliefs and attitudes of physicians in low and middle-income countries regarding interacting with pharmaceutical companies: a systematic review. BMC Health Serv Res. 2016;16:57.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Spurling GK, Mansfield PR, Montgomery BD, Lexchin J, Doust J, Othman N, et al. Information from pharmaceutical companies and the quality, quantity, and cost of physicians’ prescribing: a systematic review. PLoS Med. 2010;7:e1000352.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Fickweiler F, Fickweiler W, Urbach E. Interactions between physicians and the pharmaceutical industry generally and sales representatives specifically and their association with physicians’ attitudes and prescribing habits: a systematic review. BMJ Open. 2017;7:e016408.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Brax H, Fadlallah R, Al-Khaled L, Kahale LA, Nas H, El-Jardali F, et al. Association between physicians’ interaction with pharmaceutical companies and their clinical practices: a systematic review and meta-analysis. PLoS ONE. 2017;12:e0175493.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Mitchell AP, Trivedi NU, Gennarelli RL, Chimonas S, Tabatabai SM, Goldberg J, et al. Are financial payments from the pharmaceutical industry associated with physician prescribing?: a systematic review. Ann Intern Med. 2021;174:353–61.

    Article  PubMed  Google Scholar 

  8. Tibau A, Bedard PL, Srikanthan A, Ethier JL, Vera-Badillo FE, Templeton AJ, et al. Author financial conflicts of interest, industry funding, and clinical practice guidelines for anticancer drugs. J Clin Oncol. 2015;33:100–U58.

    Article  PubMed  Google Scholar 

  9. Pokorny A, Bero L, Moynihan R, Fabbri A, Mintzes B. How interactions with the pharmaceutical industry affect the clinical practice, knowledge and beliefs of cancer physicians: a systematic review.: PROSPERO 2020 CRD42020143353; 2020 [cited 2020 October]. Available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42020143353.

  10. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  11. McGowan J, Sampson M, Salzwedel DM, Cogo E, Foerster V, Lefebvre C. PRESS peer review of electronic search strategies: 2015 guideline statement. J Clin Epidemiol. 2016;75:40–6.

    Article  Google Scholar 

  12. Aromataris E, Munn Z, editors. Joanna Briggs Institute Reviewer’s Manual. Adelaide, Australia: The Joanna Briggs Institute; 2017 [cited 2020 June]. Available from: https://reviewersmanual.joannabriggs.org/.

  13. Behdarvand B, Karanges EA, Bero L. Pharmaceutical industry funding of events for healthcare professionals on non-vitamin K oral anticoagulants in Australia: an observational study. BMJ Open. 2019;9:e030253.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Fabbri A, Grundy Q, Mintzes B, Swandari S, Moynihan R, Walkom E, et al. A cross-sectional analysis of pharmaceutical industry-funded events for health professionals in Australia. BMJ Open. 2017;7:e016701.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pokorny AMJ, Bero LA, Moynihan R, Mintzes BJ. Industry payments to Australian medical oncologists and clinical haematologists: a cross-sectional analysis of publicly-available disclosures. Intern Med J. 2020; https://doi.org/10.1111/imj.15005.

  16. Moynihan R, Albarqouni L, Nangla C, Dunn AG, Lexchin J, Bero L. Financial ties between leaders of influential US professional medical associations and industry: cross sectional study. BMJ 2020;369:m1505.

    Article  PubMed  PubMed Central  Google Scholar 

  17. McGuinness LA, Higgins JPT. Risk-of-bias VISualization (robvis): an R package and Shiny web app for visualizing risk-of-bias assessments. Res Syn Meth. 2020;12:55–61.

  18. Decensi A, Numico G, Ballatori E, Artioli F, Clerico M, Fioretto L, et al. Conflict of interest among Italian medical oncologists: a national survey. BMJ Open. 2018;8:e020912.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lee YC, Kroon R, Koczwara B, Haines I, Francis K, Millward M, et al. Survey of practices around pharmaceutical company funding for continuing professional development among medical oncologists and trainees in Australia. Intern Med J. 2017;47:888–93.

    Article  PubMed  Google Scholar 

  20. Ozaki A, Saito H, Onoue Y, Sawano T, Shimada Y, Somekawa Y, et al. Pharmaceutical payments to certified oncology specialists in Japan in 2016: a retrospective observational cross-sectional analysis. BMJ Open. 2019;9:e028805.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Robertson J, Moynihan R, Walkom E, Bero L, Henry D. Mandatory disclosure of pharmaceutical industry-funded events for health professionals. PLoS Med. 2009;6:e1000128.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Marshall DC, Moy B, Jackson ME, Mackey TK, Hattangadi-Gluth JA. Distribution and patterns of industry-related payments to oncologists in 2014. J Natl Cancer Inst. 2016;108:djw163.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Chimonas S, Rozario NM, Rothman DJ. Show us the money: lessons in transparency from state pharmaceutical marketing disclosure laws. Health Serv Res. 2010;45:98–114.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Tao DL, Boothby A, McLouth J, Prasad V. Financial conflicts of interest among hematologist-oncologists on Twitter. JAMA Intern Med. 2017;177:425–7.

    Article  PubMed  Google Scholar 

  25. Inoue K, Blumenthal DM, Elashoff D, Tsugawa Y. Association between physician characteristics and payments from industry in 2015-2017: observational study. BMJ Open. 2019;9:e031010.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Perlis RH, Perlis CS. Physician payments from industry are associated with greater medicare part D prescribing costs. PLoS ONE. 2016;11:e0155474.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bandari J, Turner RM 2nd, Jacobs BL, Canes D, Moinzadeh A, Davies BJ. The relationship of industry payments to prescribing behavior: a study of degarelix and denosumab. Urol Pract. 2017;4:14–20.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Jagsi R, Sheets N, Jankovic A, Motomura AR, Amarnath S, Ubel PA. Frequency, nature, effects, and correlates of conflicts of interest in published clinical cancer research. Cancer. 2009;115:2783–91.

    Article  PubMed  Google Scholar 

  29. Lexchin J. Financial conflicts of interest of clinicians making submissions to the pan-Canadian Oncology Drug Review: a descriptive study. BMJ Open. 2019;9:e030750.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Liu JJ, Bell CM, Matelski JJ, Detsky AS, Cram P. Payments by US pharmaceutical and medical device manufacturers to US medical journal editors: retrospective observational study. BMJ. 2017;359:j4619.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Mitchell AP, Basch EM, Dusetzina SB. Financial relationships with industry among national comprehensive cancer network guideline authors. JAMA Oncol. 2016;2:1628–31.

    Article  PubMed  Google Scholar 

  32. Riechelmann RP, Wang L, O’Carroll A, Krzyzanowska MK. Disclosure of conflicts of interest by authors of clinical trials and editorials in oncology. J Clin Oncol. 2007;25:4642–7.

    Article  PubMed  Google Scholar 

  33. Saito H, Ozaki A, Sawano T, Shimada Y, Tanimoto T. Evaluation of pharmaceutical company payments and conflict of interest disclosures among oncology clinical practice guideline authors in Japan. JAMA Netw Open. 2019;2:e192834.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Wayant C, Turner E, Meyer C, Sinnett P, Vassar M. Financial conflicts of interest among oncologist authors of reports of clinical drug trials. JAMA Oncol. 2018;4:1426–8.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Haque W, Alvarenga M, Hsiehchen D. Nonresearch pharmaceutical industry payments to oncology physician editors. Oncologist. 2020;25:e986–e9.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Cherla DV, Olavarria OA, Holihan JL, Viso CP, Hannon C, Kao LS, et al. Discordance of conflict of interest self-disclosure and the centers of medicare and medicaid services. J Surg Res. 2017;218:18–22.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Harada K, Ozaki A, Saito H, Sawano T, Yamamoto K, Murayama A, et al. Financial payments made by pharmaceutical companies to the authors of Japanese hematology clinical practice guidelines between 2016 and 2017. Health Policy. 2021;125:320–6.

    Article  PubMed  Google Scholar 

  38. Bandari J, Ayyash OM, Turner RM 2nd, Jacobs BL, Davies BJ. The lack of a relationship between physician payments from drug manufacturers and Medicare claims for abiraterone and enzalutamide. Cancer. 2017;123:4356–62.

    Article  PubMed  Google Scholar 

  39. Zezza MA, Bachhuber MA. Payments from drug companies to physicians are associated with higher volume and more expensive opioid analgesic prescribing. PLoS ONE. 2018;13:e0209383.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Eisenberg MD, Stone EM, Pittell H, McGinty EE. The impact of academic medical center policies restricting direct-to-physician marketing on opioid prescribing. Health Aff. 2020;39:1002–10.

    Article  Google Scholar 

  41. Mitchell AP, Winn AN, Lund JL, Dusetzina SB. Evaluating the strength of the association between industry payments and prescribing practices in oncology. Oncologist. 2019;24:632–9.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hadland SE, Cerda M, Li Y, Krieger MS, Marshall BDL. Association of pharmaceutical industry marketing of opioid products to physicians with subsequent opioid prescribing. JAMA Intern Med. 2018;178:861–3.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Mitchell AP, Winn AN, Dusetzina SB. Pharmaceutical industry payments and oncologists’ selection of targeted cancer therapies in medicare beneficiaries. JAMA Intern Med. 2018;178:854–6.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hollander MAG, Donohue JM, Stein BD, Krans EE, Jarlenski MP. Association between opioid prescribing in medicare and pharmaceutical company gifts by physician specialty. J Gen Intern Med. 2020;35:2451–8.

    Article  PubMed  Google Scholar 

  45. Sah S, Loewenstein G. Nothing to declare: mandatory and voluntary disclosure leads advisors to avoid conflicts of interest. Psychol Sci. 2014;25:575–84.

    Article  PubMed  Google Scholar 

  46. Tibau A, Ocana A, Anguera G, Seruga B, Templeton AJ, Barnadas A, et al. Oncologic drugs advisory committee recommendations and approval of cancer drugs by the US Food and Drug Administration. JAMA Oncol. 2016;2:744–50.

    Article  PubMed  Google Scholar 

  47. Ahearne M, Gruen TW, Jarvis CB. If looks could sell: Moderation and mediation of the attractiveness effect on salesperson performance. Int J Res. Mark. 1999;16:269–84.

    Article  Google Scholar 

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Acknowledgements

The authors thank Dr. Patrick Donald, medical oncologist, Darwin, Australia, for his assistance in assessing the quality appraisal of three included studies.

Funding

AP was supported by a University of Sydney Postgraduate Award.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the protocol development, selection of studies, interpretation of data and final manuscript. AP undertook the literature searches and extracted data. BM confirmed the extracted data. AP, BM and AF performed the quality appraisals.

Corresponding author

Correspondence to Adrian M. J. Pokorny.

Ethics declarations

Competing interests

In 2020, Barbara Mintzes acted as an expert witness for Health Canada in a legal case related to the marketing of an unregistered product in Canada. There are no other conflicts to declare.

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No ethics approval was necessary as all data analysed exist in the public domain.

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Not applicable.

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Pokorny, A.M.J., Fabbri, A., Bero, L.A. et al. Interactions with the pharmaceutical industry and the practice, knowledge and beliefs of medical oncologists and clinical haematologists: a systematic review. Br J Cancer 126, 144–161 (2022). https://doi.org/10.1038/s41416-021-01552-1

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