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Interaction and medical inducement between pharmaceutical representatives and physicians: a meta-synthesis Salmasi, Shahrzad; Ming, Long C; Khan, Tahir M Nov 17, 2016

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REVIEW Open AccessInteraction and medical inducementbetween pharmaceutical representativesand physicians: a meta-synthesisShahrzad Salmasi1, Long Chiau Ming2 and Tahir Mehmood Khan3,4*AbstractBackground: It has been proven that the interaction between pharmaceutical representatives and physicianscan directly influence the latter’s prescribing behaviour. This meta-synthesis aims to explore the available studiesregarding the nature of the interaction that takes place between pharmaceutical representatives and physicians.It highlights the different aspects of that interaction by investigating the reasons why these meetings happenin the first place, their benefits and drawbacks and their impact on patients’ health and, ultimately, the health ofthe public.Methods: A search for published articles was conducted in April 2015. Three databases (PubMed, Ovid Medline,and ProQuest) were searched for articles published between January 2000 and April 2015. Authors workedautonomously and in pairs to select eligible articles. In this case, the meta-synthesis approach was used to developa fuller understanding and to facilitate new knowledge by bringing together qualitative findings on physician-PRinteraction. ‘Meta-synthesis’ is the process of amalgamation of a group of similar studies with the aim of developingan explanation for their findings (Walsh and Downe, J Advanc Nurs 50: 204–211, 2005). A thematic content analysiswas conducted on the 15 included full text articles (qualitative and quantitative studies) whereby the originalauthors’ understanding of key concepts in each study was identified and listed in a summary form in the dataextraction sheet under “key findings” column. These findings were then juxtaposed to identify homogeneityand dissonance (Walsh and Downe, J Advanc Nurs 50: 204–211, 2005). Homogenous findings were then codedtogether on a different data extraction table to form a theme.Results: A total of 15 articles met the inclusion criteria and were included in this meta-synthesis;six from the UnitedStates, two from Libya, and one each from Turkey, Peru, India, Germany, the United Kingdom, Yemen, and Japan.Six main themes were derived from the included articles: 1-the frequency of pharmaceutical representatives’ visits,2-the perceived ethical acceptability of the interactions between pharmaceutical representatives and physicians,3-the attitudes held by physicians towards visits by pharmaceutical representatives, 4-their perception of the effectof such visits on prescription patterns, 5-reasons to accept or reject pharmaceutical representatives, and lastly,6-guidelines.Conclusions: The physicians referred to pharmaceutical representatives as efficient and convenient informationresources and were willing to meet them and accept their gifts. It was also evident that most physicians believedthat their prescribing would not be influenced by pharmaceutical representatives.Keywords: Inducement, Motivation, Health care quality, Pharmaceutical marketing, Prescription behavior, Marketingethics, Pharmaceutical representatives* Correspondence: tahir.mehmood@monash.edu3School of Pharmacy, Monash University, Sunway City, Selangor, Malaysia4Department of Pharmacy, Abasyn University, Peshawar, PakistanFull list of author information is available at the end of the article© The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.Salmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 DOI 10.1186/s40545-016-0089-zBackgroundThe pharmaceutical industry significantly influences theeconomy and healthcare system of a country. Accordingto The World Health Organization(WHO), by 2017,theglobal pharmaceuticals market will be worth approxi-mately US$400billion with one third of thesales revenueof pharmaceutical companies spent on marketing theirproducts [1]. Physicians are the prime target of pharma-ceutical marketing teams, in which pharmaceuticalrepresentatives (PRs) play a crucial role [1]. The job ofthe PRs is to visit physicians to promote their company’sproducts [2, 3]. In addition, free physician samples, gifts,company supported conferences, workshops and eventsare also brought to the notice of physicians through PRs.Among all the promotional expenses, detailing is the lar-gest category; estimated US$20.4 billion has been usedfor this purpose in United States (US) in 2015 [4, 5].Given the above, PR-physician interactions have thepotential to result in a conflict of interest wherebyphysicians might fail to abide by their moral, legal andprofessional obligations for personal gain [6, 7]. Researchhas shown that the interaction between PRs and thephysicians can directly influence the latter’s prescribingbehaviour; it has been observed that the rate of prescrip-tions increases after physicians see a PR or accept freesamples [8]. This has led to increasing concern over ir-rational and inappropriate prescribing practices [9]which could jeopardize patient care, harm the patients,promote the misuse of drugs, increase costs to thehealthcare system, distort public opinion of the health-care industry and erode the trust of the patients in theintegrity of medical decision making [8, 10].Wazana et al., published a review in 2000 that identi-fied the extent of and attitudes toward the interplay ofrelationship and its impact between physicians towardsthe PR [11]. Wazana’s review received a mixed responsefrom the health care communities because he proposedthat the extent of physician-PR interactions couldpotentially affect prescribing and professional behaviour[12–18]. Ten years later, Spurling et al. who performed asystematic review on 58 articles, reported that exposureto information from pharmaceutical companies was as-sociated with either lower prescribing quality or increasein prescribing frequency or no association was detected.Finally, with only one exception among the 58 studiesincluded in the review by Spurling et al.; exposure toinformation from PRs was associated with an increase inprescribing costs or no association was detected. Theyreported that interaction of physicians with PRs doesnot negatively affect prescribing [3]. This is the firstmeta-synthesis that fills the literature gap on the inter-action between PRs and physician. The purpose of thismeta-synthesis, therefore, is to explore the availablestudies regarding PR-physician interactions especially tohighlight the detailing aspects of such interactions fromthe physician’s point of view.MethodsA systematic literature search of computerized databaseswas conducted in April 2015 using PubMed, Ovid Med-line and ProQuest. A meta-synthesis approach was usedto integrate results from various studies in order to givea comprehensive overview of the interaction that takesplace between pharmaceutical representatives and phy-sicians [19]. Research papers published between January2000 and April 2015 which presented evidence con-cerning such interactions, were included. The searchstrings used can be found in Supporting InformationAdditional file 1: Table S1.The search strings used were very specific. This is be-cause we were not interested in marketing methodsother than detailing. Our purpose was to focus on theinteraction that takes place between PRs (and not anyother promoter/ representatives from other industrieswho might meet with physicians) and physicians (andnot any other prescriber such as prescribing nurses,dentists, etc.). Hence the search strings were chosencarefully to retrieve the most relevant studies. To ensureall relevant papers were included, we searched the refer-ences of the studies that were included. Furthermore,Monash integrated search panel for Science CitationIndex were also used to screen the relevant citations ofthe included studies.A total of 218 papers were identified using the searchstrings outlined in Additional file 1: Table S1. Duplicatesand articles published before the year 2000 were ex-cluded. The title and abstract of the 72 remaining paperswere assessed for eligibility against the inclusion criteria.This was performed independently by two reviewers,who classified the papers into three groups of “to in-clude”, “to exclude” and “unclear”. Both reviewers (SSand TMK) met to compare their independent reviews. Apaper would be included or excluded once agreed byboth reviewers. In the case of disagreement, or wheneither reviewer was unsure, the opinion of a third person(LCM) was sought.The inclusion criteria were articles focusing on detail-ing and physician interaction with PRs. Studies relatedto marketing methods other than detailing, such asdirect to consumer advertising and ghost writing wereexcluded. Papers written in languages other than Englishwere excluded as we did not have the necessary skills tointerpret them. We also excluded studies focused onprescribers other than physicians, such as prescribingnurses. Opinion papers and interventional studies werealso excluded.The full text of 25 papers was read by the first author.A number of studies were identified at this stage as notSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 2 of 12being written in English (i.e. their title and abstract werewritten in English but the full-text was not) and thesewere therefore excluded, along with a number of othersthat were found to be irrelevant. This left 15 papers.Details about the number of the included and excluded ar-ticles are shown in Fig. 1. The Preferred Reporting Itemsfor Systematic Reviews and Meta-Analyses (PRISMA)checklist is presented in Additional file 2: Table S2.Analysis and theme synthesis‘Qualitative meta-synthesis’ is the process of amalgam-ation of a group of similar qualitative studies with theaim of developing an explanation for their findings [20].In this case, the meta-synthesis approach was used todevelop a fuller understanding and to facilitate newknowledge by bringing together qualitative findings onphysician-PR interaction. The 15 included papers weresubjected to data extraction using a pre-designed data-extraction Excel worksheet on Microsoft Office® 2014. Athematic content analysis was conducted on the15included full text articles whereby the original authors’understanding of key concepts in each study was identi-fied and listed in a summary form in the data extractionsheet under “key findings” column. These findings werethen juxtaposed to identify homogeneity and dissonance[20]. Homogenous findings were then coded together ona different data extraction table to form a theme. Sixbroad themes were formulated for the results section; 1-The frequency of pharmaceutical representatives’ visits, 2-The perceived ethical acceptability of the PR-physicianinteractions, 3-Physicians’ attitudes towards PR visits, 4-Physicians’perceptions of the effect of PR visits onprescription patterns, 5-Reasons to accept/reject PRs and6-Guidelines. Findings were scrutinized under each themeto see if further sub-categories were warranted. The argu-ments for and against PR interaction with physicians werevery rich. We were hence unable to take account of all thearguments, in great detail. Moreover, while all the in-cluded studies presented information about PR-physicianinteractions, they reported different aspects of such inter-actions since they examined the interaction from differentangles, hence a thematic analysis was chosen to classifyand summarize the findings in a systematic, easy to under-stand manner. Through the six themes formulated, wehope to provide an overview of the main aspects of thePR-physician interactions identified.Fig. 1 PRISMA diagram demonstrating the search strategy and its resultsSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 3 of 12ResultsA total of 15 publications were included in the studycovering studies undertaken in a range of countries; sixfrom the US, two from Libya, one each from Turkey,Peru, India, Germany, the United Kingdom (UK), Yemenand Japan. Eight of these articles focused on physicians’attitudes and views regarding physician-PR interactions[9, 21–27]; four focused on the nature of the interaction[26, 28–30]; two concentrated on the frequency of theseinteractions [31, 32]; and two focused on the reasons be-hind such interactions [33, 34]. The detailed themes andextracted text is presented in Additional file 3. Studyand participants’ characteristics can be found in Table 1.Theme 1.0: The Frequency of PRs visitsThe first step in investigating and understanding theinteraction between the PRs and the prescribers is to de-termine how frequent such interactions are, and if theyare significant enough.Research has shown that frequency of PR visits tophysicians- skilled health-care professionals trained andlicensed to practice medicine- is considered to be a goodindicator of an active relationship between physiciansand the pharmaceutical industry. Lieb et al. reportedthat 77.0% (n = 160) of German respondents met withPRs at least once a week, and 19.0% (n = 39) were visitedby PRs on a daily basis [29]. Other studies also reportedthat PRs visit physicians regularly in order to promotetheir products [9, 21, 22, 26, 29, 32]. De Ferrari et al.studied the relationship between the specialty of the pre-scriber and the frequency of PR visits [9]. Physicians in-volved in teaching and those practicing paediatricmedicine, were reported to receive more frequent visits,while anaesthetists were found to be least frequentlyvisited by PRs [9]. Two studies reported that PRs vis-ited physicians working in a private setting more fre-quently, while physicians working in community anduniversity hospitals experienced less frequent visits[22, 23].Theme 2.0: Perceived ethical acceptability of the PR-physician interactionsThe job of PRs is to introduce and market their com-pany’s products. PRs ensure that physicians are informedof the benefits of the products and are therefore willingto prescribe them to their patients. The interaction be-tween PRs and physicians entails a number of marketingmethods such as gifts, sponsorships, free drug samplesand free lunches. Moreover, in recent years, simplebrand reminders such as stationery with the company’slogo and product name on them have increasingly beenreplaced by gifts of greater value, ranging from jewelleryto iPads [30]. According to policymakers, such gifts havethe potential to act as an ethical inducement andnegatively impact prescribing behaviour and, ultimately,patient health [11, 30]. Brett et al., for example, con-ducted a survey in South Carolina where physicians wereasked to rate 18 scenarios of interactions between physi-cians and PRs from the most ethically appropriate(score = 0) to the least ethically appropriate (score = 5).Results showed that physicians made distinctions aboutthe ethical appropriateness of gifts of different value anddifferent type; recreational gifts were rated to be signifi-cantly less ethically appropriate than educational gifts, aswere the more expensive gifts [23]. According to De Fer-rari et al., activities perceived to be most ethical were theprovision of medical samples (81.8%) and continuingmedical education (68.9%) [9, 25]. Roy et al. furtheradded that, in India, some physicians justify gifts ascompensation for the time spent listening to the PR,time which could have been spent on a patient [30].“PRs never try to bribe to sell their drug. (Gifts)are just a gesture to say thanks for the time thedoctor gives. Let’s say a doctor sees three patientsin 15 minutes, the PR us costing him those threepatients in his 15-minute talk. So the PR tries tocompensate with gifts since obviously he can’tcompensate in cash” [30].In contrast, there were others who felt that air condi-tioners, washing machines, microwaves, cameras, televi-sions and expensive crystals were acceptable gifts [30].Theme 3.0: Physicians’ attitudes towards PR visitsThe physician’s attitude is what determines whether theywould be inclined to believe the information provided bythe PR. Qualitative data demonstrating the attitude ofphysicians are presented in Additional file 4: Table S3.3.1 Perceived legitimacy of the PRLegitimacy refers to the accuracy and accountability ofthe PRs as a source of information. According to Prosseret al., a relationship has been observed between the fre-quency of visits and the perceived legitimacy of the in-formation provided: the more frequently visitedphysicians were more likely to consider the informationprovided to be of “high quality” [33].Physicians have been reported, in a number ofstudies, to consider the information provided by thePRs as “not trustworthy”, “very variable” and “depend-ing on which PR you see”; they also disclosed that thePRs usually choose the promotion of their company’sproduct over the actual benefits for the patient byhardly ever mentioning the drug interactions and theside-effects [9, 21, 29, 30, 33].On the other hand, some physicians from a number ofdifferent studies recognized the professional authority ofSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 4 of 12Table 1 Characteristics of the included studiesStudy Participant’s Specialty (N) Gender M/F Years ofPractice (N)Practice Setting CountryMorgan et al.2006 [25]Gynecologists (397) 125/92 NA Obstetrics-gynaecology partnershipor group (44.2%)Solo practice (27%)Multispecialty group (14.9%)University full-time faculty andpractice (10.7%)Health maintenanceorganisation (3.3%)USAnderson et al.2009 [28]Gynecologists (251) 143/108 Mean (SD):22 (11)Private practice (178)Community hospital (25)University hospital (30)Other (16)USWang et al.2009 [27]Ophthalmology trainees (122):1st year residents (32)2nd year residents (44)3rd year residents (28)Fellows (17)Unknown (1)NA NA NA USMisra et al.2010 [24]Psychiatry trainees (17):Residents (12)Fellow trainee (5)Psychiatry faculty (58):Assistant professor (21)Associate professor (6)Professors (13)NA NA Academic medical centre USFischer et al.2009 [34]Internal medicine (29)Family medicine (17)Pediatric medicine (2)Geriatric medicine (3)23/38 15 Academic affiliation (21)Community-based practice (24)Academic affiliation &community-based practice (8)Other (8)USBrett et al.2003 [23]Residents (39)Faculty physicians (37)49/27 NA Medical school USSarikaya et al.2009 [32]Medical students2nd year students (280)3rd year medical students (308)168/140 NA Marmara University School ofMedicine (MUSM)Ege University School ofMedicine (EUSM)TurkeySaito et al.2010 [26]Internal medicine (214)General surgery (181)Orthopedic surgery (177)Pediatrics (221)Obstetrics (210)Psychiatry (197)Ophthalmology (209)1084/326 <10 (339)11–20 (488)21–30 (428)>31 (155)Office (822)Hospital (588)JapanRoy et al. 2003 Senior executives in drug companies (15)PRs (36)Physicians (25)Chemists (25)IndiaAlssageeret al. 2013 [31]General Practitioner (GP) (274)Surgeon (99)Resident MO (41)Anesthesiologist (61)Specialist (91)Others (42)371/237 1-3 (288)4–6 (82)7–9 (45)>10 (193)Public (512)Private (34)Both (62)LibyaAlssageeret al. 2012 [22]GP (274)Surgeon (99)Resident MO (41)Anesthesiologist (61)Specialist (91)Others (42)371/237 1-3 (288)4–6 (82)7–9 (45)>10 (193)Public (512)Private (34)Both (62)LibyaSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 5 of 12PRs as information providers and expressed satisfactionwith the information provided. Just under half of all theparticipants (47.6%) in a study in Peru, for example,stated that the information provided by PRs helps them“learn about new products” and “stay up-to-date”. Simi-larly, Roy et al. reports that physicians were satisfiedwith the information provided despite the fact that side-effects were hardly ever mentioned [30]. De Ferrari et al.also reported that 24% of faculty (n = 10) and 18% ofpsychiatry residents (n = 3) believed that PRs provideuseful and accurate information on new drugs [9].Overall, while opinions on this matter differ amongphysicians, it can be concluded that physicians considerthe information provided by PRs, factual but, to an ex-tent, biased.3.2 Perceived benefits of the interaction with PRsThe perceived benefits of the interaction are the rea-son why physicians continue to see PRs, despiteknowing that the information provided by them may,in some cases, be biased. These perceived benefits areexplained below.3.2.1 Easy access to information Research indicatesthat physicians considered the convenience of acquiringinformation from PRs, regarding both old and newdrugs, to be the main benefit of meeting with them, Thisis true regardless of the country the physicians practicedin [21, 23, 24, 26, 29, 33, 34].Physicians also reported that PRs are useful for obtain-ing research papers and journal off-prints. Physicians’busy schedules leave them no time to look for evidence.Thus, representatives are seen as ‘short-cuts’ and “valu-able sources of information”, simplifying the acquisitionand evaluation of new product information [33].“I’m sure you could manage if you didn’t see anotherdrug rep and I’m sure you could get the information ifyou wanted to, it’s just that it’s not that accessible, andit’s also whether you would have the time to actuallysit and read it” [33].“Although you try and keep up with journals and suchlike that, some things go by, you do miss things. So Ifeel like I’m keeping up to date a little bit. If I didn’tsee reps I feel that I would be slightly disadvantagedin terms of my awareness of medications comingthrough” [33].“[It is positive] that they can inform us about newproducts […] being launched in the market for the firsttime. Secondly, we can [hear about] alternatives fromother companies that have the same effectiveness, lowcost and less side effects” [21].The user-friendly and face-to-face nature of the inter-actions permits physicians to ask questions, and get in-stant answers;“ I think the answer is it’s user friendly, it’s very userfriendly and its easy listening, you know, with yourcoffee listening to what they’ve got to say” [33].Furthermore, according to Prosser et al. [33], severalphysicians have commented that they remember the in-formation better when communicated verbally;“ I can remember the information better after havingtalked to them” [33].“Seeing a representative face to face tends to make amore lasting impression than reading” [33].3.2.2 Free gifts and drug samples The other perceivedbenefit of meeting PRs is the gifts and free samples pro-vided by them. Such gifts can range from materials thatare supposed to directly help the patients (blood sugardiaries, educational materials) to personalized gifts forthe doctor; from cheap stationery to expensive so-calledgifts that act as inducements [21, 34]. According toTable 1 Characteristics of the included studies (Continued)Prosser et al.2003 [33]GP (107) 76/31 <10 (6)11–20 (55)>20 (46)Health authorities in the NorthWest of England (107)UKAl-Areef et al.2013 [21]Physicians (32)(interns, GPs/medical officers, residentsand specialists)4/28 NA NA YemenLieb et al.2010 [29]Neurologists/psychiatrists (83)Primary care physicians (76)cardiologist (49)104/98Unknown gender (6)NA NA GermanyDe Ferrariet al. 2014 [9]Internal medicine (59)General surgery (32)Pediatrics (28)Anesthesiologist (13)Obstetrics (16)96/52 NA Peruvian public general hospital. PeruAbbreviations: GP General Practitioner, NA not applicable/available, UK United Kingdom, US United States of America, MO Medical Officer, SD Standard deviationSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 6 of 12Alssageer et al.(n = 423) 86% of respondents reported tohave received printed material (n = 480; 79%), simplegifts (stationery, n = 442; 73%) or drug samples (n = 418;69%) at least once during the last twelve months [31].“Sometimes we need representatives in providing somemedicines that we need it, some books or bulletin.Really, they help us in getting books, CDs and lecturesfrom abroad that provided by some companies. Theysupport us on this side a lot” [21].Free medication samples are the most frequently ac-cepted gifts in the US and Germany. Physicians considerthese gifts to be the most ethically acceptable and a greatadvantage of meeting with PRs [9, 29, 34].Physicians and PRs justify such gifts on the groundsthat free medications can be used to help patients whoare unable to afford medications due to financialconstraints. Free samples can also be used to determinethe dose and side-effects before the patient has to investin them [34, 36].“We want to make people happy and you make peoplehappy often when you give them a sample” [34].Morgan et al. reported that the main reason for whichthe free drug samples are distributed is patients’ financialneeds, followed by patients’ convenience and to builda good relationship with the patient, but less thantwo-thirds of physicians distributed free samples witha good basis of knowledge as to the efficacy of thesample product [25].3.2.3 Social aspects of the interaction Some physiciansliked the casual, friendly aspect of the interaction andthought of the representatives as more of their friendthan a promoter;“Going out to dinner as a group….That’s why we do it,more of a social setting outside of the wards” [34].3.3 Perceived drawbacks of the interaction with PRsDespite the above-mentioned positive attitudes towardsPRs, the prescribers do admit that there are certaindrawbacks to seeing PRs. These drawbacks, in theiropinion, are:3.3.1 Negative impact on the patient Some physiciansbelieve that PRs take up a proportion of the doctor’s time,which could have been spent attending to patients [29, 30].“Doctors always perceive MRs’ visits as an intrusion.Every minute taken up by the MR is time which couldhave been spent seeing patients and making money inthe clinic. Often, MRs queue up early in the morningfor doctors who allow only the first three MRs to seethem” [30].Al-Areefi et al. reported that some physicians hate thefact that PRs interrupt their patient care process, espe-cially those working in the emergency departments witha high workload and a large number of patients to at-tend to. These physicians have absolutely no time to lis-ten to PRs and even refer to them as “time wasters” [21].Some other physicians reported discomfort with or dis-like of the interactions, and this appeared to be rooted intheir perception that PRs harm the ethical reputation ofthe profession and adversely affect patients [21, 34].“My rule is I [listen but] don’t believe anything they’resaying” [34].3.3.2 Pressure from PRs Studies suggest that drugsoften complain about the “pushy” behaviour of PRs thatputs them under pressure to prescribe a certain productfrom a certain company. They have been reported tohave experienced aggressive sale techniques, which theydefined as: asking physicians to justify their current pre-scribing and even direct requests using emotional ap-peals to the physicians to prescribe a certain medicine asa favour to the PR. Such aggressive marketing methodsare criticized by physicians [29, 30, 33].“Such approaches could discourage prescribing arepresentative’s product or seeing a particularrepresentative again. What we don’t like is a drug repcoming in and questioning us, because I don’t thinkthat’s their role or asking us what we do prescribe, andthen why. We don’t like that. Some of them can bequite pushy” [33].“In some cases, the representative imposes on thephysician to prescribe a certain product. We canprescribe it in rare cases for some diseases. Somerepresentatives say: I have certain amount of medicinein your pharmacy and it's not dispensing, prescribe,just one or two’. This forced us to refuse to meet himagain, because he imposes [on] me to prescribe hisproduct for any patient without any reason” [21].Studies also indicate that physicians feel obliged to thePR because of previous service they may have provided.Although this is not a direct pressure from the PR, itcan still pressure the prescribers indirectly and affecttheir prescription patterns, which they dislike [21].Both direct and indirect pressure from PRs are dislikedby physicians and can result in the physician deciding tostop seeing that particular PR [29, 30, 33].Salmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 7 of 12Theme 4.0: Physicians’ perceptions of the effect of PRvisits on prescription patternsPhysicians’ perception as to whether or not their pre-scribing is influenced by PRs is very important since itcan determine their attitudes towards PRs [37].Wang et al. reported that 36% (n = 32) of ophthal-mology trainees reported having changed prescribingbehaviour based on the information provided by aPRs, 77% (n = 94) stated that they changed prescribingbehaviour based on the availability of medicine sam-ples [27].Research shows, however, that the majority of physi-cians are convinced that PR visits do not influence theirprescribing behaviour [24, 26, 27, 29, 31, 32, 34, 36]. DeFerrari et al. reported that about 88% of study respon-dents disclosed that they believe receiving gifts or goingfor company sponsored lunches does not affect theirprescribing [9]. All 15 included studies illustrated onecommon point: that physicians almost always believethat such interactions can influence their colleagues’prescription patterns but not theirs; Roy et al. has forexample, revealed that most physicians usually do notadmit having accepted gifts from PRs and even if theydo, they usually believe it does not affect their prescrib-ing. Almost all of them, however, claim to know col-leagues who accept gifts and whose prescribingbehaviour is influenced by this [30, 38].“I think drug reps are a good thing…Just because Ihave a pen with the name of a drug on it, doesn’tmean I’m going to prescribe it” [33].The other reason stated by the physicians for theirperceived immunity against biased information is thefriendship between them and the PR over the years:“I think if you see a rep who you know well … it’s thesame rep who you’ve seen for several years, they don’ttry and pull the wool over your eyes. They know that ifthey tell you lies you’ll be seeing them again in sixmonths and you’ll find them out” [33].On the contrary, some other physicians found thisvery same social bond to be the main reason their pre-scribing behaviour being affected; they felt they weresometimes influenced to prescribe a particular medicinedue to their long term and continuous relationship withthe representative [33].Theme 5.0: Reasons to accept/reject PRsUnderstanding the reasons behind physicians accept-ing PRs would be a breakthrough in understandingthe overall nature of the interaction between PRs andprescribers [35].5.1 Reasons for accepting PRs5.1.1 Sponsorship, gifts One incentive behind meet-ing PRs is the sponsorship, gifts and products pro-vided by them.“We were building a new surgery and, you know, weneeded some sponsorship” [33].“I don’t mind a nice hotel for a weekend. You don’t getmany perks unfortunately as a GP, and I don’t see aproblem in that” [33].“I work in non-profit…you know [reps] do provideme with pens…[and] somehow my administratordoesn’t want to spend too much money on officesupplies” [34].5.1.2 Social aspect of the interaction Friendship andthe social bonds made between physicians and PRs overthe years has been proven to have a direct effect on thephysicians’ decisions on whether or not to accept a PR.Some physicians considered these meetings as a chancefor social interaction and as a break from their busywork routine [21, 33].The social aspect of the interaction is even strongenough that the physicians who have stopped seeingPRs still make exceptions for the ones who are theirfriends:“Some reps I’ve known for donkey’s years and theyknow all about my life and I know all about their lifeand you have a chat about things which are totallyunrelated to why they came, but it does make lifemore interesting and you’re probably more likely toactually retain what they came in to tell you if you’vehad a pleasant time talking to them about your kidsor something” [33].Participants reported that they sometimes acceptedthe PRs not because they want to hear about new drugsbut just to enjoy the social aspect of the visits.“Sometimes we don’t even talk about drugs, we justchat about the kids and it’s good to have a relaxedand friendly lunch” [34].5.1.3 Courtesy and tradition Another reason for phy-sicians to agree to meet PRs is the matter of cour-tesy, where physicians accept to meet a PR just sothat they are not rude; some of the sample com-ments are as follows:“I think they have a very difficult job. There will bean element of empathy for somebody who comes andsays can I talk to you about something. Out ofpoliteness, really” [33].Salmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 8 of 12“I know it’s just the guy’s job, and if I don’t talk to himthen he may lose it, so I talk to him” [33].“The other side is to facilitate services forcolleagues as they do this task [to support] theirfamilies. This refers to a social and economicsituation for colleagues because he gets a payoffto spend on his family” [21].Some physicians accepted representatives simply be-cause it was tradition or, in other words, part of the jobof a physician. Some reported ‘inheriting’ such visitsfrom their previous colleagues, the practice then becom-ing part of their routine [23].5.2 Reasons for avoiding/rejecting PRsNot all physicians readily accept PRs, there are a fewphysicians who either have a certain criteria for choosingPRs or choose to avoid them completely [23]. The cri-teria used by some physicians are: personal style, com-pany and the kind of drugs PRs offer.“I have specific criteria for selection. I mean,whether I like this representative or not, whether Iam comfortable with him or not and whether hisstyle is true or not true. Is he logical or not logical?There are companies that [I] do not care aboutthem. For example, a new company whose productsare widely available such as popular products. Ioften do not meet them because they do not giveus new ideas” [21].One of the physicians who avoids PRs’ comments:“Really, from the time that I came here to work, I[have tried] to avoid meeting them because my use islimited, but I have to meet my colleagues. I try toavoid the interview because I know that I will notprescribe his product. I am a surgeon and my use islimited. Just I have painkiller. There is no otherchoice” [21].Physicians cited many reasons for refusing to meetPRs, such as bad experience with PRs and commercialcontext (e.g., disagreements about some commercialdeal), obligations to other companies, lack of convictionabout the product, lack of credibility of PRs and work-load or inappropriate timing of visits [21, 33].“The other thing, I may refuse to meet [a]representative if the owner of the company behaveswith our colleagues [in an] inhuman or dishonorable[way], so this forces us to stop prescribing its productand prescribe a similar alternative that exists in themarket” [21].Reasons for avoiding PRs, other than the ones men-tioned above, were: commercially-biased information,pushy and argumentative approach, and a lack of accur-acy in the information provided, and, finally, the PR’s in-fluence on prescribing behaviour.“I have been very influenced in the past by myprescribing so I don’t see them anymore now. I wasgetting no advantage from it at all, it was skewing myprescribing and I was losing a lot of time, so I stoppedseeing them” [33].Theme 6.0: Guidelines6.1 Guidelines and their impactOver the years, there have been a number of guidelinesdeveloped by different healthcare societies regarding theinteraction between physicians and PRs such as; theAmerican College of Obstetricians and Gynecologists(ACOG), the American Medical Association (AMA) andthe Association of American Medical Colleges, CanadianMedical Association (CMA). Morgan et al. [25] andAnderson et al. [28] have each investigated the use andeffect of guidelines in the US. Anderson et al. reportsthat 154 (62%) of participants in the US were familiarwith guidelines on interacting with the pharmaceuticalindustry, of whom 81 (33%) had read guidelines devel-oped by ACOG, 86 (35%) had read AMA guidelines, and49 (21%) had read guidelines from other sources such ashospital guidelines, journal articles, and continuing med-ical education programmes [28].Studies show that those who had read the guidelineswould actually provide fewer free samples to patients orhave less frequent meals with the PRs. They were alsoless likely to receive first hand news on medical productsfrom PRs or include PRs in the decision as to whetherto prescribe a new drug, compared to those who had notread the guidelines [25, 28].According to Anderson et al., there was no significantdifference between those who reported reading ethicalguidelines and those who did not do so pertaining tousing PRs for obtaining drug information [28]. It is pos-tulated that having read guidelines did not affect the per-ceived value of PRs [28].6.2 Physician’s opinion on guidelines that restrict physician-PR interactionsThe opinion of physicians on the policies that limit orprohibit the physician-PR interaction varied significantly.Some participants believed such restrictions to be unfairto prescribers and patients; some welcomed them withopen arms. While others reported having doubts aboutpolicies, particularly those related to prohibition of freedrug samples. These physicians however, disclosed that,over time they realized that their prescribing behaviourSalmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 9 of 12had actually been affected by the visits of PRs and avail-ability of free drug samples, and they eventually startedsupporting policies that prohibit/restrict PR visits. In astudy done in the US in 2003, 39.9% of participantsstated that they disagreed with placing limitations on theinteraction between physicians and PRs, while roughlythe same percentage (33.3%) agreed with the policy. InGermany the data is slightly different, over half of theGerman physicians (n = 108; 52%) indicated that theywould regret the cessation of the visits while theremaining 45% (n = 94) supported it [29, 34].“I was really hesitant about getting rid of the samplecloset years ago, but now I think it was really,definitely the right thing because I would reach for thebest non-steroidal that was in there and at that pointit was [brand name]. So I give a patient [brand name]thinking I did a good thing because he told me hedidn’t have any money, but often they would comeback wanting [brand name] where I just could havegiven him Ibuprofen. …Once we didn’t have it any-more, I realized that…” [34].DiscussionAs part of the health care system, pharmaceutical manu-facturers have benefited countless people through theirinvestment in research and product development. Theirultimate responsibility, however, is to their shareholders,who expect a reasonable profit from their investments[6]. The pharmaceutical industry, therefore, cannot beentirely blamed for trying to increase returns, withinlegal boundaries. Inappropriate marketing practices thatmay arise from this profit-led competition have beenproven, however, to have the potential to influence phys-ician prescribing.Policymakers have therefore tried to restrict the inter-action between physicians and PRs, which is where mostof the marketing occurs, by developing guidelines andmaking relevant policies. The World Health Assembly,in an attempt to tackle the issue, adopted the WHO Eth-ical Criteria for Medicinal Drug Promotion in 1988,which requires PRs to have an appropriate educationalbackground and be adequately trained with sufficientmedical and technical knowledge and integrity to presentinformation on products in an accurate, unbiased, and re-sponsible manner. WHO also holds employers respon-sible, for not only the basic and continuing training oftheir representatives, but also for their statements and ac-tivities [39]. Many critics, however, have complained thatthese guidelines have been largely disregarded, includingthe voluntary Code of Pharmaceutical Practices developedby the industry’s own International Federation of Pharma-ceutical Manufacturers’ Associations (IFPMA) [1]. Whilethe development of guidelines and policies has provenhelpful, therefore, it certainly is not enough..As demonstrated by this meta-synthesis, the attitudeof physicians towards PRs is a very crucial determinantof the potential of PRs to indirectly influence the healthof patients in a positive or negative way. The studies in-cluded in this meta-synthesis were undertaken in ninedifferent countries with significantly different economies,cultures, education/healthcare systems, and health pol-icies, yet the positive attitude of physicians towards PRswas evident in all of them.As stated earlier, there are a number of reasons behindthis positive attitude with the one-to-one medium ofinteraction being one of them; the results of the researchconducted by McGettigan et al. showed that the infor-mation sources most frequently rated important by phy-sicians were not those most used in practice. Thesources of practical importance were those involving thetransfer of information through personal face-to-facecontact, indicating the importance of the mediumthrough which information is conveyed [40] which posesan advantage for direct pharmaceutical detailing.Lack of time to read and keep abreast of the myriad ofnew medical information is another important facilitatorfor physicians to meet PRs. PRs are seen as convenientand timely sources of medicine related information. Phy-sicians perceive the information provided by PRs as fac-tual but in some cases biased. Our findings are in linewith that of the systematic review conducted by Wazanaet al. [11];physicians believe that they are immune fromany potential marketing influence. This is mainly be-cause most of physicians believe that they have therequired expertise and knowledge to assess the pre-sented information and distinguish the valid informa-tion from the exaggerated, biased information [21, 22,24–27, 29, 32–34]. This is despite the clear evidencein the literature regarding the effect of PRs on pre-scribing behaviour [32].Undeniably, detailing poses as a convenient face-to-face educational meeting [21, 23, 24, 26, 29, 33, 34],espe-cially for newly launched medicines [33, 35]. Instead ofseeking to ban these interactions, therefore, medicalregulatory bodies could implement proactive measuresto educate medical students about potential medical in-ducements [10]. Vinson et al. measured the effect of aone-hour lecture and discussion about the appropriate-ness of pharmaceutical gifts among second-year medicalstudents. Findings from the survey have showed thatthese students had become statistically significantlymore resistant to the gifts compared to the first-year stu-dents who served as a control group and had not experi-enced the lecture. This study strongly suggested thatchanges in students’ attitudes towards marketingmethods used by PRs may be fostered [41]. Similarly,Salmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 10 of 12positive long term effects were observed from educatingtrainees and physicians about understanding and respond-ing to pharmaceutical promotion [42–44].We believe that this meta-synthesis has given new in-sights into the PR-physician interaction. The findings of thismeta-synthesis have implications for policy makers and ed-ucators. Future research should focus on practical educa-tion and policy interventions to better limit any potentialconflict of interest that may arise from such interactionsthrough education and informed policy development.LimitationsThis meta-synthesis focused on the recent literature andexcluded studies published before 2000. This means thatsome relevant, important points might have been missedif they were published before 2000. Meanwhile, thethemes were generated in such a way as to offer, in theauthors’ opinion, a useful insight into the different as-pects of the PR-physician interaction. Drawing togetherdata from multiple countries has some value, certainly.However, looked at from the opposite point of view, it isnot entirely clear that the cultures of pharmaceuticalcompanies and of physicians, and the regulatory/health-care systems in countries as diverse as Peru, India, theYemen, the UK and the US can be easily comparable.Direct to consumer advertising is, for example allowedin US but banned in other countries. Thus, there is aneed for some further country specific studies.ConclusionsThe purpose of this meta-synthesis, was to highlight the de-tailing aspects of PR-physician interactions from the physi-cian’s point of view. This meta-synthesis shows thatphysicians generally see meetings with PRs as advantageousto everyone: the patients, because they receive free drugsamples, the hospital/clinic, because they would receivestationery, books, and, most importantly, themselves, asthese meetings help them to stay up-to-date and aware ofnewly launched medications. Future research should focuson educating medical students to correct their perceptionof immunity against marketing which may hold them backfrom critically appraising the information provided by PRs.This will ensure that patients do not bear the cost of com-petition between pharmaceutical companies.Additional filesAdditional file 1: Table S1. Description of the search strings used andthe results obtained. (DOCX 13 kb)Additional file 2: Table S2. PRISMA 2009 Checklist. (DOC 209 kb)Additional file 3: Data extraction from the studies included in thereview. (DOCX 130 kb)Additional file 4: Table S3. Qualitative data demonstrating thephysician’s attitude. (DOCX 34 kb)AbbreviationsACOG: American College of Obstetricians and Gynecologists; AMA: AmericanMedical Association; CMA: Association of American Medical Colleges,Canadian Medical Association; GP: General Practitioner; IFPMA: InternationalFederation of Pharmaceutical Manufacturers’ Associations; MO: Medicalofficer; NA: Not applicable/available; PR: Pharmaceutical representative;SD: Standard deviation; UK: United Kingdom; US: United States; WHO: WorldHealth OrganizationAcknowledgementsWe would like to acknowledge Johnathan from academic English editors forhis services to check the language appropriateness of the paper.FundingNone.Availability of data and materialsData sharing not applicable to this article as no datasets were generated oranalyzed during the current study.Authors’ contributionsConceived and designed the experiments: TMK and SS. Analyzed the data:SS, TMK and LCM. Wrote the paper: SS, TMK and LCM. Designed searchstrategies: TMK and SS. Critically reviewed the manuscript for importantintellectual content: TMK and LCM. Read and approved the final version: SS,TMK and LCM. All authors read and approved the final manuscript.Competing interestsThe authors declare that they have no competing interests.Consent for publicationNot applicable.Ethics approval and consent to participateNot applicable.Author details1Collaboration for Outcomes Research and Evaluation (CORE), Faculty ofPharmaceutical Sciences, The University of British Columbia, Vancouver,British Columbia, Canada. 2Unit for Medication Outcomes Research andEducation (UMORE), Pharmacy, School of Medicine, University of Tasmania,Hobart, Tasmania, Australia. 3School of Pharmacy, Monash University, Sunway City,Selangor, Malaysia. 4Department of Pharmacy, Abasyn University, Peshawar,Pakistan.Received: 21 July 2016 Accepted: 5 November 2016References1. WHO. Trade, foreign policy, diplomacy and health. 2014. Available online:http://www.who.int/trade/glossary/story073/en/. 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Does exposure toconflict of interest policies in psychiatry residency affect antidepressantprescribing? Med Care. 2013;51:199–203.44. McCormick BB, Tomlinson G, Brill-Edwards P, Detsky AS. Effect of restrictingcontact between pharmaceutical company representatives and internalmedicine residents on posttraining attitudes and behavior. JAMA. 2001;286:1994–9.•  We accept pre-submission inquiries •  Our selector tool helps you to find the most relevant journal•  We provide round the clock customer support •  Convenient online submission•  Thorough peer review•  Inclusion in PubMed and all major indexing services •  Maximum visibility for your researchSubmit your manuscript atwww.biomedcentral.com/submitSubmit your next manuscript to BioMed Central and we will help you at every step:Salmasi et al. Journal of Pharmaceutical Policy and Practice  (2016) 9:37 Page 12 of 12


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