The Inclusion of Nurses in Pharmaceutical

Letters

disease has remained relatively stable from 2009 through 2014, ease and wheat allergy. Instead, researchers and clinicians can although the prevalence of individuals reporting adherence to use this as an opportunity to understand how factors associated a gluten-free diet has more than tripled (0.52% in 2009-2010 with this diet affect a variety of symptoms, including gastroin- to 1.69% in 2013-2014). testinal function, cognition, and overall well-being. Part of what may be driving this gluten-free diet trend is simply a belief, fueled by marketing and media, that these foods are Daphne Miller, MD healthier. However, surveys suggest that many individuals who adhere to a gluten-free diet believe that the exclusion of gluten Author Affiliation: Department of Family and Community Medicine, University of California, San Francisco. has resulted in subjective health benefits from weight loss to re- Corresponding Author: Daphne Miller, MD, Department of Family and duced symptoms of inflammation and gastrointestinal Community Medicine, University of California, San Francisco, 1157 Cragmont 3,4 distress. Because a gluten-free diet may have negative social, Ave, Berkeley, CA 94708 ([email protected]). financial, and health repercussions, it is important for clinicians Published Online: September 6, 2016. doi:10.1001/jamainternmed.2016.5271 to understand whether, in most cases, it is the elimination of the Conflict of Interest Disclosures: None reported. protein gluten that is responsible for symptom improvement or 1. Riffkin R. One in five Americans include gluten-free foods in diet. Gallup Inc. whether following a gluten-free diet is simply a marker of other http://www.gallup.com/poll/184307/one-five-americans-include-gluten-free- dietary choices that are creating positive effects.5 foods-diet.aspx. Published July 23, 2015. Accessed June 12, 2016. Not all research has found that individuals who adhered 2. Kim H-s, Patel KG, Orosz E, et al. Time trends in the prevalence of celiac disease and gluten-free diet in the US population: results from the National to a gluten-free diet resulted in subjective health benefits. A Health and Nutrition Examination Surveys 2009-2014 [published online recent 2-year prospective study6 from Italy suggests that some- September 6, 2016]. JAMA Intern Med. doi:10.1001/jamainternmed.2016.5254. thing other than gluten itself is resulting in self-reported health 3. Nielsen Co. We are what we eat: healthy eating trends around the world. benefits. Researchers enrolled all consecutive patients with glu- http://www.nielsen.com/us/en/insights/reports/2015/we-are-what-we-eat .html. Published January 20, 2015. Accessed June 12, 2016. ten-related symptoms, and after those with celiac disease or 4. Hartman Group. Gluten free trends. http://www.hartman-group.com wheat allergy were eliminated, only 7.5% experienced any /hartbeat-acumen/120/gluten-free-trend. Accessed June 12, 2016. change of symptoms with a gluten-free diet. Studies such as 5. Reilly NR. The gluten-free diet: recognizing fact, fiction, and fad [published this raise the question of what other than gluten might ex- online May 10, 2016]. J Pediatr. doi:10.1016/j.jpeds.2016.04.014. plain the symptomatic improvement experienced among those 6. Capannolo A, Viscido A, Barkad MA, et al. Non-celiac gluten sensitivity among following a gluten-free diet. patients perceiving gluten-related symptoms. Digestion. 2015;92(1):8-13. One explanation is that it is not the gluten but the grain 7. Halmos EP, Power VA, Shepherd SJ, Gibson PR, Muir JG. A diet low in itself. Researchers in Australia found that that the ferment- FODMAPs reduces symptoms of irritable bowel syndrome. Gastroenterology. 2014;146(1):67-75.e5. able oligosaccharides, disaccharides, monosaccharides, and 8. Biesiekierski JR, Peters SL, Newnham ED, Rosella O, Muir JG, Gibson PR. No polyols (FODMAPs) and insoluble fiber that are found in gluten- effects of gluten in patients with self-reported non-celiac gluten sensitivity after containing foods may be responsible. FODMAPS and in- dietary reduction of fermentable, poorly absorbed, short-chain carbohydrates. soluble fiber increase the osmotic pressure in the large intes- Gastroenterology. 2013;145(2):320-328.e1, 3. tine and promote bacterial fermentation, which results in gas 9. Genoni A, Lyons-Wall P, Lo J, Devine A. Cardiovascular, metabolic effects and dietary composition of ad-libitum Paleolithic vs. Australian guide to healthy production and abdominal bloat. In a controlled, crossover eating diets: a 4-week randomised trial. Nutrients. 2016;8(5):314. study7 of patients with irritable bowel syndrome, a diet low in FODMAPs effectively reduced these symptoms; in a related study,8 patients who improved while following a low- The Inclusion of Nurses FODMAP diet experienced no exacerbation of symptoms when in Pharmaceutical Industry–Sponsored Events: gluten was introduced. Guess Who Is Also Coming to Dinner? Another explanation is that gluten elimination may ac- The release of the Open Payments data in the United States, company other dietary trends that are associated with im- which detail payments from pharmaceutical and medical de- proved symptoms. For example, adherents to the popular Pa- vice companies to physicians, enables analysis of the finan- leolithic and autoimmune protocol diets might also report being cial relationships between physicians and industry.1 How- on a gluten-free diet.9 There is a debate about whether these ever, the Physician Payments

diets, which promote eating unprocessed foods that were avail- Invited Commentary Sunshine Act, which man- able in preagricultural times while avoiding grains, oils, and page 1720 dates these disclosures, omits legumes, offer any health advantage over other whole food registered nurses. A recent diets (such as the Mediterranean diet). Nonetheless, some have qualitative study suggests nurse-industry interactions in US argued that simply eliminating highly processed foods (in- hospitals may be common and influential.2 The limited preva- cluding highly processed gluten-containing foods) might re- lence data available, based on self-report, suggests that 51% sult in an improved sense of well-being. to 96% of nurses have contact with industry representatives.3 Following a gluten-free diet likely means different things to Australia is one of the few jurisdictions to report pay- different people, and a heterogeneous group of individuals are ments to all registered health professionals. Since 2007, mem- adhering to this dietary trend. Although the choice to be gluten ber companies of the industry trade association, Medicines free may be driven in part by marketing and a misperception that Australia, have voluntarily reported sponsorship of functions gluten free is healthier, it is important that this choice not be dis- for health professionals.4 This report describes the extent of missed as an unfounded trend except for those with celiac dis- inclusion of nurses in pharmaceutical company-sponsored

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Table. Characteristics of 81 946 Eventsa

No. (%) With Nurses and Other Characteristic With Only Nurses Professionalsb With Only Physicians Events, Total No. (Total = 81 946) 5645 (7) 40 569 (50) 35 732 (44) Attendees, No. Total No. (Total = 2 495 400) 147 311 (6) 1 196 745 (48) 1 151 344 (46) Abbreviation: IQR, interquartile Median No. (IQR) 11 (6-23) 20 (14-27) 16 (10-25) range. Location and formatc a P< .001 for all comparisons. Overseas location 141 (2) 188 (0.5) 1654 (5) b Events where at least 1 nurse was in Clinical setting 3182 (56) 28 268 (70) 17 497 (49) attendance in addition to In-service format 1087 (19) 1039 (3) 158 (0.4) physicians, pharmacists, Scientific meeting 492 (9) 1124 (3) 2202 (6) physiotherapists, psychologists, and/or trainees. Dinner served 598 (11) 6161 (15) 8691 (24) c Reported percentages for location Expenses, $d and format are column percentages. Total cost of function, 12 563 204 (5) 79 783 601 (35) 138 830 547 (60) d Total = $231 177 352e Cost variables are reported in Australian dollars. Median total cost per event (IQR) 176 (44-932) 250 (163-694) 482 (167-2330) e Total cost of function includes food Median total cost per person (IQR) 12 (5-51) 13 (10-30) 31 (12-114) and beverages and/or venue and Total cost of food and beverages, 2 938 344 (4) 26 480 923 (40) 37 064 775 (56) audiovisual hire, speaker honoraria, Total = $66 484 042 speaker and attendee airfare and Median total cost of food and 63 (16-254) 211 (136-373) 207 (77-943) accommodation, parking, and beverages per event (IQR) meeting sponsorship

events in Australia. In 2016, there were 271 423 practicing reg- nificantly less than multidisciplinary events with at least 1 nurse istered nurses in Australia. Of these, 1380 (0.005%) were nurse present ($250; IQR, $163-$694) (P < .001). The median cost per practitioners, which is the category of registered nurse per- event was significantly greater for events with physicians-only mitted to prescribe medicines.5 ($482; IQR, $167-$2330) compared with multidisciplinary events (P < .001). Events with nurses only were significantly more likely Methods | We downloaded all available reports of sponsored to be scientific meetings or in-services than multidisciplinary events for health professionals from the Medicines Australia or physician-only events (P < .001). Events held overseas or website. The reports covered 6-month intervals from October where dinner was served were significantly more likely to be 2011 to September 2015 (n = 301 reports) and detailed 116 845 physician-only than multidisciplinary or nurse-only (P < .001). events. We converted the PDF reports to Excel format and coded the unstructured data using iteratively generated keywords and Discussion | Whereas most transparency regulation focuses on Excel’s filter function. We focused analysis on a subset of events physicians, the pharmaceutical industry targets a broader range (71% [81 946]) to compare events with nurses in attendance and of health professions in sponsored events. Thirty-five per- physician-only events. We excluded events without nurses or cent of all events included nurses in addition to colleagues from physicians, physician-only events with trainees, and those miss- a range of disciplines, suggesting that this type of marketing ing data on professional status of attendees. We used SPSS sta- targets health care teams. However, nurses were also specifi- tistical software (version 22) to conduct descriptive analyses, cally targeted, and a small proportion of events included nurses Kruskal-Wallis tests for the differences among medians and χ2 only. Although a small proportion of nurse attendees had pre- tests for differences among proportions. Significance of post hoc scribing authority, nonprescribing nurses may have been rou- comparisons was evaluated using a Bonferroni correction. tinely included in pharmaceutical industry-sponsored events, which perhaps reflects their role in medication compliance, the Results | Nurses were present at 39.6% of all events (46 214 of management of chronic disease, and hospital purchasing.6 Al- 116 845 events), nearly twice as often as primary care physi- though we could not verify the accuracy of the reports and our cians (21.1% [24 662 of 116 845). Physician specialists were pres- analysis was limited by the available data, to our knowledge, ent at most events (68.5% [80 060 of 116 845]). Over 40% of this is the first measure of prevalence of nurses’ attendance events (47 084 of 116 845) included attendees from multiple at pharmaceutical industry-sponsored events. The high preva- professions, whereas 4.8% (5645 of 116 845) included only lence of nurses’ attendance suggests that transparency regu- nurses, 9.1% (10 647 of 116 845) only primary care physicians, lation and conflict of interest management should routinely and 17.7% (20 692 of 116 845) only specialists. Nurse practi- include nurses and other health professionals. tioners in Australia have prescribing authority: they were present at less than 1% of events (1013 of 116 845). Quinn Grundy, PhD, RN The Table details characteristics of nurse-attended events Alice Fabbri, MD compared with physician-only events (with costs given in Aus- Barbara Mintzes, PhD tralian dollars) (71% [81 946]). The median cost per event with Swestika Swandari, BSc(Pharm) nurses-only ($176; interquartile range [IQR], $44-$932) was sig- Lisa Bero, PhD

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Author Affiliations: Faculty of Pharmacy and Charles Perkins Centre, The physician clinicians who have the statutory authority to University of Sydney, Sydney, Australia (Grundy, Fabbri, Mintzes, Swandari, prescribe, for example, NPs and physician assistants (PAs). Bero); Centre of Research in Medical Pharmacology, University of Insubria, Varese, Italy (Fabbri). However, there still remains a relative paucity of evidence on Corresponding Author: Quinn Grundy, PhD, RN, Faculty of Pharmacy and the effect that these promotional activities have on this alter- Charles Perkins Centre, The University of Sydney, D17, Sixth Floor, The Hub, native group of prescribers. Available studies have revealed that NSW, 2006, Australia ([email protected]). NPs interact frequently with industry,2 feel that these inter- Published Online: September 12, 2016. doi:10.1001/jamainternmed.2016.5276. actions are ethically acceptable,2,3 and are deemed to affect Author Contributions: Dr Grundy had full access to all of the data in the study patient care in a generally positive way.2-5 To our knowledge, and takes responsibility for the integrity of the data and the accuracy of the data there have been no studies to date that describe the effect that analysis. Study concept and design: Grundy, Mintzes, Bero. industry interactions with nurse practitioners have on pre- Acquisition, analysis, or interpretation of data: Grundy, Fabbri, Mintzes, scribing outcomes. Swandari. The frequent presence of nurses at pharmaceutical com- Drafting of the manuscript: Grundy. pany–sponsored educational events indicates that they are val- Critical revision of the manuscript for important intellectual content: All authors. Statistical analysis: Grundy, Swandari. ued by industry in a way that has heretofore gone unnoticed. Obtained funding: Mintzes. This lack of consideration is the consequence of the assump- Administrative, technical, or material support: Mintzes, Swandari. tion that physicians alone influence pharmaceutical deci- Study supervision: Grundy, Mintzes, Bero. No additional contributions: Fabbri. sions. Financial allocation for promotion to nurses most cer- Conflict of Interest Disclosures: None reported. tainly provides a very positive return on investment for the Funding/Support: The work was partially funded via a University of Sydney pharmaceutical industry; they would not continue to invest Faculty of Pharmacy summer scholarship. in these activities unless they resulted in favorable financial Role of the Funder/Sponsor: The funding source had no role in the design and outcomes. As the authors1 note, industry may deem nurses to conduct of the study; collection, management, analysis, and interpretation of be very influential in purchasing decisions in hospitals by sit- the data; preparation, review, or approval of the manuscript; and decision to ting on pharmacy and therapeutics committees or by provid- submit the manuscript for publication. ing informal guidance to consumers around the pharmaceuti- Additional Contributions: We thank Ray Moynihan, PhD (Bond University), for access to the data and project guidance and Joanne Gale, PhD (University of cal treatment of chronic disease. In addition, nurses without Sydney), for guidance on statistical methods. Neither Dr Moynihan nor Dr Gale prescribing authority may influence prescribing patterns by were compensated for this support. steering prescriptions toward the brand-name drug brought by 1. Marshall DC, Jackson ME, Hattangadi-Gluth JA. Disclosure of industry pharmaceutical representatives or suggesting that patients start payments to physicians: an epidemiologic analysis of early data from the open payments program. Mayo Clin Proc. 2016;91(1):84-96. with samples. Perhaps, industry is capitalizing on the find- 2. Grundy Q, Bero LA, Malone RE. Marketing and the most trusted profession: ings of the Gallup poll for 14 years and counting that nursing is 6 the invisible interactions between registered nurses and industry. Ann Intern Med. the most “trusted profession.” Indeed, nurses have garnered 2016;164(11):733-739. a cultural authority that may translate into a de facto role as 3. Grundy Q, Bero L, Malone R. Interactions between non-physician clinicians arbiters of influence that may be very productive for industry. and industry: a systematic review. PLoS Med. 2013;10(11):e1001561. Although data are limited, nurses seem to attend a signifi- 4. Robertson J, Moynihan R, Walkom E, Bero L, Henry D. Mandatory disclosure cant number of pharmaceutical company–sponsored educa- of pharmaceutical industry-funded events for health professionals. PLoS Med. 2009;6(11):e1000128. tional events in the United States as well. Massachusetts, as 5. Nursing and Midwifery Board of Australia. Registrant Data. Canberra, Australia: part of the Pharmaceutical Code of Conduct law that was passed Nursing and Midwifery Board of Australia; 2016. in 2008,7 maintains a robust database of payments that are 6. Institute of Medicine. The Future of Nursing: Leading Change, Advancing Health. made by industry to all “health care practitioners.” In addi- Washington, DC: Institute of Medicine; 2011. tion to hospitals and physicians, covered recipients include nonprescribing nurses, pharmacists, respiratory therapists, op- Invited Commentary tometrists, occupational therapists, dental hygienists, and even Pharmaceutical Industry Interactions massage therapists. Nonprescribing nurses (registered nurses) With Nonprescribing Clinicians: in the 2013 data (the last year of available data) represented A Complex Web of Influence 16% of all covered recipients in Massachusetts, who received Grundy and colleagues1 have elegantly quantified a practice a total of $1 112 666 in payments by the pharmaceutical and that has garnered scant attention in the literature; that is, that medical device industries. Most of these payments (74%) were pharmaceutical promotions reach well beyond the bounds of for food; the average payment in this category was $119. How- physicians and even other au- ever, more than $707 000 represented “compensation for bona thorized prescribers, such as Related article page 1718 fide services,” which includes consulting, speakers fees, and nurse practitioners (NPs). The services provided as “key opinion leaders.”8 findings that nonprescribing nurses were present at nearly 40% The Massachusetts data serve as a small window, illustrat- of pharmaceutical company–sponsored educational events in ing how industry directs marketing to nonphysicians in the Australia between 2011 and 2015 were noteworthy, yet not at United States. However, there is no reason to think it would dif- all surprising. fer in any other US state. Also, the data clearly point to the need These findings from Australia carry important global les- for greater transparency into industry payments made to a sons, including for the United States. In the United States, in- wider cadre of health care professionals, particularly nurses. dustry has long targeted their marketing dollars toward non- The Sunshine provisions of the Patient Protection and Afford-

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able Care Act were crafted to shed light on physician and hos- LESS IS MORE pital interactions with industry. However, a critical gap is that Eliminating Routine Glucometer Readings it does not capture payments made to other health care pro- in the Office Setting: Correcting a Foolish fessionals that may also influence, both directly or indirectly, Consistency purchasing decisions that are made for pharmaceuticals or Although new, expensive diagnostic tests are attractive tar- medical devices. Senators Chuck Grassley (R-Iowa) and Richard gets for critics of runaway health care costs, overall health care Blumenthal (D-Connecticut) have recently introduced the Pro- costs may be driven more by a high volume of more routine, vider Payment Sunshine Act (S. 2153) that would partially ex- less costly tests.1 Estimating pand the Sunshine provisions to include other prescribing pro- blood glucose with a glucom- 9 Editor's Note page 1722 fessionals, eg, nurse practitioners and physician assistants. eter in patients with diabetes Based on Grundy’s study, and what is revealed by the Mas- is a standard procedure in most primary care clinical settings.2 sachusetts data, it is clear that even the Provider Payment Sun- Routinely providing the busy clinician with a glucometer read- shine Act does not go far enough. All nurses, in addition to the ing seems an efficient way of preparing for informed clinical myriad of professionals that are included in the Massachu- decision making about diabetic management in the ambula- setts reporting regulations, should be covered under the Pro- tory setting. However, the routine tasks that are components vider Payment Sunshine Act or related legislation. In the United of rooming the clinic patient are increasing in number.3 In the States, the pharmaceutical and medical device industries have process of exploring how to make the rooming process more fashioned a remarkable web of influence with strands that cap- efficient, we examined the value of the glucometer test as a ture more than just the obvious players—that is, physicians. routine maneuver in the clinic. This web reaches a wide cadre of health care professions and risks accumulating conflicts of interest into every corner of our Methods | Setting and Population. The Downtown Health Plaza health care system. However, without inclusion in transpar- Adult Medicine Clinic of Wake Forest Baptist Health typi- ency policies and reporting mechanisms, it is difficult if not cally logs more than 60 000 primary care clinic visits each impossible to say what influence industry has on nurses and year. Approximately one-third of clinic patients have diabe- other health care professionals. One can assume it is at least tes, and the average glycated hemoglobin (hemoglobin A1C) worth the cost of a dinner. level has long been approximately 9.1% (reference range, 4.5%-6.4%). Elissa Ladd, PhD, FNP-BC Increasing delays from accumulating tasks assigned to the Alex Hoyt, PhD, FNP nurse and/or assistant rooming the patient (vital signs mea- Author Affiliations: MGH Institute of Health Professions, Boston, surement, screening for clinical conditions; alcohol abuse, de- Massachusetts. pression, falls; medication reconciliation, and health mainte- Corresponding Author: Elissa Ladd, PhD, FNP-BC, MGH Institute of Health nance update) led us to scrutinize the value of a routine Professions, 36 First Ave, Boston, MA 02129 ([email protected]). glucometer reading on every patient with diabetes. After a Published Online: September 12, 2016. doi:10.1001/jamainternmed.2016.5284 1-week trial without routine clinic glucometry, we subse- Conflict of Interest Disclosures: None reported. quently made glucometer readings optional with the under- 1. Grundy Q, Fabbri A, Mintzes B, Swandari S, Bero L. The inclusion of nurses in standing that the nurse or patient could request a glucometer pharmaceutical industry–sponsored events: guess who is also coming to dinner? [published online September 12, 2016]. JAMA Intern Med. doi:10.1001 reading at any time. /jamainternmed.2016.5276. 2. Ladd EC, Mahoney DF, Emani S. “Under the radar”: nurse practitioner Study Design. The 3-month period before the policy change prescribers and pharmaceutical industry promotions. Am J Manag Care. 2010; (January 1, 2015, to March 15, 2015) was compared with the 16(12):e358-e362. 3-month period after the change date (March 16, 2015, to 3. Crigger N, Barnes K, Junko A, Rahal S, Sheek C. Nurse practitioners’ June 30, 2015). For each month, a random sample of 10 perceptions and participation in pharmaceutical marketing. J Adv Nurs. 2009; 65(3):525-533. doi:10.1111/j.1365-2648.2008.04911.x. patients with both an established diagnosis of diabetes and a 4. Mahoney DF, Ladd E. More than a prescriber: gerontological nurse documented continuity clinic visit were chosen for medical practitioners’ perspectives on prescribing and pharmaceutical marketing. chart review. In addition to the random sample of patients Geriatr Nurs. 2010;31(1):17-27. doi:10.1016/j.gerinurse.2009.09.003. with diabetes, a download of all glucometer readings con- 5. Fischer MA, Keough ME, Baril JL, et al. Prescribers and pharmaceutical ducted in the clinic was available. The cost of a glucometer representatives: why are we still meeting? J Gen Intern Med. 2009;24(7):795-801. reading was estimated to be approximately $7 for glucometer doi:10.1007/s11606-009-0989-6. supplies and 5 minutes of nursing time.4 An institutional 6. Gallup, 2015. Honesty/ethics in professions. Available at: http://www.gallup .com/poll/1654/honesty-ethics-professions.aspx. Accessed June 28, 2016. review board waiver was obtained from the Wake Forest Uni- 7. Commonwealth of Massachusetts. Pharmaceutical and Medical, Device versity School of Medicine. Manufacturer Code of Conduct. 2008). https://malegislature.gov/Laws /GeneralLaws/PartI/TitleXVI/Chapter111N. Accessed June 27, 2016. Results | The Figure shows a marked decrease in number of 8. Massachusetts Health and Human Services. Massachusetts Pharmaceutical glucometer readings that coincides with the change in clinic Code of Conduct Data Download. http://www.mass.gov/eohhs/gov policy. A conservative estimate of the decrease from an aver- /departments/dph/programs/hcq/healthcare-quality/pharm-code-of-conduct /data/data-download.html. Updated April 22, 2015. Accessed June 26, 2016. age of 400 to 100 glucometer readings per month resulted in 9. S. 2153: Provider Payment Sunshine Act. Govtrac.us. https://www.govtrack an estimated cost savings over $2000 per month and 25 .us/congress/bills/114/s2153. Accessed June 26, 2016. hours of nursing time.

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