The drug sector represents 1.5% of the gross domestic product in Spain and directly employs approximately 40,000 people.1 Many studies report an increase of drug use and prescription in Spain, even though institutional surveys have shown little variation in use after security/safety alerts.2

Claims about drug use and its impact on the economy are common in the public agendas of developed countries. Populations are aging, and there is a clear increase in drug use in parallel with the age-related burden of disease.3 The medicalization of life is leading to increased spending on drugs and is endangering patients, as the risk-benefit ratio does not always justify the treatment, which is often unwarranted, ineffective and inefficient.4

Drug companies are one of the main sources of information for physicians, and evidence suggests that important bias and problems of veracity, as well as of accuracy, exist in the information they transmit.5,6

Several authors have discussed the influence of promotion on physicians’ prescription practices, referring to doctors’ underestimation of the power of this relationship on their decisions.7,8 Recently, the potential influence of industry activity has come under scrutiny, even reaching decision making institutions such as the World Health Organization whose management of the H1N1 epidemic may have been unduly influenced by the drug industry.9

Several authors have reported physician-industry relationships, such as Campbell et al10 in the USA, Saito et al11 in Japan, and Altisent et al12 in Spain. In addition, some attempts to fight the unlimited growth of drug consumption and expenditure, as well as to avoid “corruption” by pharmaceutical companies have been made.9,13,14 However, quantifying the industry-physician relationship remains important, especially in those health systems predominantly funded by public resources. In Spain, this relationship has only been analyzed in primary care.

This study aims to describe, for the first time, the relationship between the drug industry and physicians and to analyze the characteristics of physicians associated with the probability of receiving benefits from this industry in Aragon, a region of Spain. This report is part of a more general study that analyzed physicians’ opinions and attitudes to industry representatives’ knowledge of their prescribing patterns.15

We performed an observational cross-sectional study in which doctors registered in the Aragon Health System, both in public and private practice, were invited to participate by e-mail or post.16 The study population consisted of 5,038 physicians registered in Aragon, a north-east Spanish region, at the beginning of 2008, and who had publicly accessible contact details. Electronic addresses were found for 3,439 participants while the remaining 1,599 were sent a letter by post. The study's protocol was approved by the Ethics and Clinical Investigation Committee of Aragon.

Physicians who agreed to participate filled in an anonymous, ad-hoc questionnaire available on a web page between June and November 2008. A second e-mail was sent as a reminder 2 months after the first invitation. Questionnaires were considered valid when at least 80% of the items were answered. As an incentive to participate, a prize was drawn for a laptop computer.

To ensure the reliability of the answers, each physician was personally invited to participate and, to avoid more than one questionnaire being completed by the same person, the prize was drawn only for those giving personal data.

Six hundred and fifty nine questionnaires were considered valid for analysis (13.1%), when at least 80% of the questions were answered and less than 1% was discarded. The characteristics of the respondents are shown in Table 1.

Globally, 87% (n=573) reported having received some kind of benefit from industry during the previous year, and 90.1% (n=593) reported having had some meeting with industry representatives monthly. When asked about their opinion of industry representatives having access to personal data on the quantity and kinds of drug prescribed, 58.6% of physicians reported a negative response and 35.6% were indifferent.

Our results indicate that the physician profile which most likely receives industry benefits corresponds to a young man, with a medical specialty, working in a hospital, spending 20-39hours/week on direct provision of care, who reads fewer than 10 articles per month and who has been a resident's tutor in the last 3 years (Table 2).

Table 3 shows the probability of receiving each benefit according to physician characteristics. Overall, hospital medical specialities were more likely to receive benefits from industry. Non-clinical specialists received fewer gifts (OR=0.38; 95%CI: 0.18-0.77), reimbursements (OR=0.14; 95%CI: 0.06-0.35) and payments (OR=0.30; 95%CI: 0.13-0.74) than their clinical colleagues. To eliminate an erroneous interpretation, a secondary analysis was re-run without the non-clinical specialty, and no substantial modifications in the results were observed.

Samples were three times more likely to be given in primary care settings than in the hospital setting (OR=3.67; 95%CI: 1.91-7.06). The probability of receiving gifts was directly associated with the number of meetings between physicians and industry (OR=1.05; 95%CI: 1.03-1.07) and was inversely associated with the number of articles read per month (OR=0.43; 95%CI: 0.25-0.72). Both reimbursements and payments were associated with the number of meetings between physicians and industry (OR=1.05; 95%CI: 1.02-1.07; OR=1.03; 95%CI: 1.02-1.04); and in both, compared with hospitals, primary care settings were less likely to receive these benefits (OR=0.37; 95%CI: 0.15-0.89; OR=0.39; 95%CI: 0.20-0.77).

The mean number of representative visits showed statistically significant differences between physicians who reported receiving samples and those who reported not receiving samples (20.6 vs 10.94; p=0.000), gifts (20.96 vs 9.90; p=0.000), reimbursements (17.43 vs 8.33; p=0.000) and payments (23.25 vs 12.79; p=0.000). Compared with medical hospital specialities, non-clinical specialists met significantly less frequently with industry representatives (Table 4).

This study shows that relationships between industry and physicians do exist and that they are related to specialty and work setting.

Our findings agree with those of previous studies.8,10,11,17 We replicate the findings of a previous study reporting that payments for services were more frequent for men than for women and explain this in terms of the possible effects of physician gender on medical practice.18 Our data also support the idea that the more years of practice, the fewer gifts the physician receives, previously documented in the American and Japanese studies.10,11

The influence of specialty has previously been reported by Campbell et al.10 We observed a tendency of surgical and medical hospital specialities to have more representative visits and to more frequently receive benefits from industry than primary care and non-clinical. The comparison might be limited because the sample analyzed in the present study included non-clinical specialists; however, the secondary analyses without that category contradicts this argument. Therefore, we may conclude that medical specialty is an indicator of the relationship and we provide suggestions for probable context differences among countries.

As found by previous studies,10,17 we found differences between hospital and primary care but the implications differ since Spanish medical care is mainly public and few physicians develop their practice exclusively in private services, as might be the case in the USA. In Spain, primary care physicians were more likely to receive samples but were less likely to be given reimbursements and payments than professionals in hospitals. This finding might be due to the specific Spanish context. Physicians working in hospitals probably attract industry more, as private medical settings often have hospital medical or surgical specialists who work partly in the public sector but very rarely professionals working in public primary care. The peculiarities of the Japanese health system hamper the comparison as primary care does not exist in that country. Saito et al11 used the workplace variable, hospital versus office, and found no significant associations.

The assumption that the more a physician prescribes, the greater the probability of a relationship with the pharmaceutical industry may help to explain why, in our data, non-clinical specialists were less likely to receive gifts, payments or expenses from industry.19 In this sense, “big ticket” prescribers are probably more likely to benefit from industry perks and, therefore, present clear conflicts of interest.20

The variable of time spent on direct care determined only the probability of receiving samples while no statistically significant differences were found in relation to other kinds of benefit. In addition, primary care physicians in Spain do not spend less time on direct care and/or prescribe less than medical hospital specialists. Time spent on direct care, as well as other explanations found in the literature such as the patients’ age, would fail to explain our finding that medical hospital specialists received more benefits.21 A better explanation could be that hospital medical-surgical specialists in Spain frequently work in both the public and private settings.

The inclusion of all kinds of specialists and all kinds of work settings is original and adds strength to our findings, since it allows us to observe that the influence of industry is not limited to prescribers. We found that at least 5.7% of the physicians developed some activity not directly related to the provision of care; 87% of the sample reported having received some benefit from industry in the last year and 90.1% reported having met with representatives various times monthly. The implications of this finding should be highlighted since, reinforcing previous results,19,22,23 education, management, decision making and research might be influenced by the pharmaceutical industry.

The number of articles read per month could be an important indicator of physicians’ attitude and professionalism. The inverse association with the probability of receiving gifts observed in the present study might correspond to a more evidence-based clinical practice.

The present study has some limitations. The literature suggests the effects of “social desirability” in surveys such as ours. However, this study consisted of an anonymous questionnaire and we believe this bias was minimized when questions were asked on practice behavior and opinions. Although the response rate of less than 60% limits the study's validity, low response rates were also obtained in other studies in the literature on the same subject.11 The low response rate and participants’ anonymity hampers generalization of the results.

An important consideration relates to the fourth category of benefits. Although benefits can determine drug prescription, payments might be assumed to be a different relationship between physicians with industry and to have a closer connection with scientific considerations. Future research might include benefits as a specific outcome variable.

Importantly, although physicians answered questions related not only to drug companies but also to other medically related companies, we have presumed that relationships with industry were mostly focused on drugs and thus our interpretations of results refer to pharmaceutical corporations.

More detailed information on working hours, patient characteristics, prescribing behavior and volume should be included in future research, and the policies of hospitals and clinics on physician-industry relationships should be analyzed in our setting, as has been studied elsewhere.24,25

The data presented herein are innovative and useful for decision making in our region and, perhaps, in other regions and countries with similar health systems. Our results are coherent with previous findings; the role of industry and the response of the medical profession seem to be similar in our region and in the USA. However, the implications differ, given the specific characteristics of the two health systems. In Spain, drug costs are shouldered mostly by the public healthcare system, which means that government authorities should make greater efforts to control drug expenditure through medical education or management policies. Recent health reforms in Spain have focused on drugs and new activities such as providing physicians with advice on the rational use of drugs and studying prescription habits, which may pose organizational challenges.26 The data presented herein support the idea of including the study of drug-industry relationships. The different intensity found in physician-industry relationships depending on the physician's specialty and work setting provides important information for future research on the appropriateness and efficiency of prescription and for improving the transparency of the physician-industry relationship, especially in public healthcare systems.27,28

E. Lobo participated in the analysis and interpretation of the data and was involved in the drafting of the manuscript and its final approval. M.J. Rabanaque contributed to the conception and design of the study, helped to review the manuscript and approved the final version to be published. P. Carrera participated in data acquisition and analysis, helped to draft the manuscript and approved the final version. J.M. Abad participated in data interpretation, in critically revising the manuscript and approved the final version. J. Moliner made substantial contributions to the conception and design of the study, data acquisition and the interpretation of the results, helped to revise the manuscript and approved the final version for publication.

This study received grant support from the Instituto Aragonés de Ciencias de la Salud of Zaragoza (Spain), Reference Number “PIURM07/13”.

None.