Discussion

We assessed the experiences of research activities, awareness of research integrity and factors associated with potentially inappropriate research behaviours by conducting a nationwide survey of physicians in Japan. Half of the physicians had been first authors in a published paper over the past 5 years, and most physicians had experience learning about research integrity, but the reasons for learning were passive, and the recall rate was not high enough. Two-thirds of the physicians had been involved in clinical research at hospitals rather than universities, but their experiences of learning research integrity were lower than those from university hospitals. Appropriate authorship or transparency of organisational relationships were less likely to be recognised than other aspects such as autonomy and safety of subjects or appropriate data management among physicians. One in nine physicians had indulged in copying and pasting or gifted authorship, and passive reasons for learning research integrity were significantly associated with such behaviours.

Most participants in this study had experienced learning about research integrity. The Ministry of Education, Culture, Sports, Science and Technology in Japan revised the guidelines for dealing with fraudulent activities in research in 2014.21 According to these guidelines, universities and institutes, including university hospitals, were responsible for improving and managing the environment for conducting research integrity education, and funding agencies requested all funded researchers to be educated on research integrity. As a result, 87% of research institutes had an educational system for research integrity in place by 2015,14 and our data showed that 99% of participants affiliated with university hospitals had this experience. These data indicate that educational opportunities for research integrity are present in university hospitals. However, two-thirds of physicians who conducted clinical research were affiliated with hospitals other than universities, and they were less likely to receive this education compared with physicians at university hospitals. In addition, less than half of the physicians paid attention to the Ethical Guidelines, Clinical Trials Act or other policies.

We hypothesised that the relatively lower penetration rate of education among hospitals other than universities or lower awareness of the guidelines was because current methods of learning research integrity were passive or forced. A majority of participants reported that they had learnt research integrity because it was a requirement of the institution or necessary to obtain approval from the IRB, and those who reported proactive reasons such as necessity or interest were a minority. Participants with experience of the first author tended to have passive reasons for learning, but they recalled the information and were more aware of research integrity policies than those without this experience. In this context, national initiatives on research integrity were satisfactory in Japan, although there are still areas that require reform.

We found that the transparency of organisational relationships was the least known aspect of research integrity. Although only 16% of physicians who conducted clinical research were aware of it, those who recalled learning content well after learning research integrity or had knowledge of public policies were twice as likely to be aware of it than those who did not. Interpersonal relationships in environments where scientists conduct their work are a factor associated with research misconduct.22 Physicians belonging to an organisation may think that the transparency of relationships is not an individual issue. Along with individuals, organisations must also contribute to improving the research environment.23 Therefore, learning programmes for research integrity should target the research team as well as individual investigators.

We investigated the factors associated with copying and pasting, gifted authorship and conducting clinical research without IRB approval. These behaviours are discussed at the Collaborative Institutional Training Initiative in the USA so that they can be avoided in research activities,24 although they might still be poorly recognised as unethical behaviour. We recognised that researchers outside English-speaking countries sometimes referred to descriptions from articles written in English to write their manuscripts in English.25 26 As the inappropriate behaviour of copying and pasting was also reported in areas where English was the first language, the difficulty of writing in another language was not the sole reason for this behaviour, which implies that this behaviour might be extended to plagiarism.27 We demonstrated that younger investigators, those with affiliations other than university hospitals, first presenters at scientific meetings, and those with passive reasons for learning about research integrity, were associated with this type of behaviour. We assumed that younger investigators or those with affiliations other than university hospitals tended to copy and paste because of the lack of experience or opportunities in scientific and academic writing. They may also lack other skills required to conduct quality research, including methodology. These groups should be the key targets when implementing a new strategy for research integrity education in conjunction with research methodology.

The ultimate result of copying and pasting is plagiarism. Because plagiarism check programmes are now widely used by institutions or journals, the incidence of plagiarism or copying and pasting might not be problematic in the future. However, such programmes might mask the actual behaviour of copying and pasting if many researchers routinely use them. We should thus stress the importance of proactive education of researchers to be aware of research integrity in the era of constantly advancing technology.

The International Committee of Medical Journal Editors has published authorship criteria in medical journals.28 However, clinical research often involves multiple physicians with several roles. Therefore, it may be difficult for each of them to fulfil the authorship criteria.29 In addition, institutional hierarchy has resulted in passive but forced gifted authorship in the past. With such long-standing customs, as well as poor education in authorship, physicians tend to be gifted co-author status. For this study, we asked only if the participant had received gifted authorship and did not ask whether they had gifted authorship to anyone. This was done to avoid the double count of gifted authorship.

Some researchers might not have known that retrospective studies reviewing medical records do not require IRB approval. Similarly, scientific meetings or conferences also do not require IRB approval for submission or presentation. These situations might result in the continued omission of IRB approval for clinical research. In the multivariable models used in this study, recalling learning content was not significantly associated with any of these potentially inappropriate research behaviours. Therefore, additional proactive education should be considered to change behaviours among physicians who conduct clinical research.

Consistent with previous reports investigating the age distribution of research activities among researchers in all scientific fields,30–32 our study found that physicians aged 50 years or older tended to become co-author only. They were more aware of the many aspects of research integrity than the other age groups. Co-authors were likely to be senior authors who acted as mentors for the research group, thus making them responsible for research quality.32 Mentoring has been reported to play an important role in preventing research misconduct.33–35 The relatively higher awareness of research integrity among senior physicians might be due to having more research experience and perhaps becoming motivated to improve research integrity as a result.

Our findings were supported by a previous report, which suggested that training to reduce research misconduct should be conducted in a laboratory rather than in the classroom.36 Professional decision-making in research was reported to be an important element of research integrity that is based on experience.37 38 Moreover, simple accumulation of research experience risks encouraging individuals to follow their own judgement of research integrity or past customs. Therefore, proactive learning of research integrity is desirable when conducting actual clinical research. There were several programmes to train practising physicians about clinical research skills, where the experiences of learners became the primary resource of teaching.39 40 This style of education should be employed to teach physicians about research integrity in the context of clinical research. Although this study sampled physicians conducting research, the importance of research integrity and its education should be universal for other healthcare professionals as well as scientists. The findings of this study should be shared with other scientific fields.

This study had several limitations that are inherent to the study design. Most importantly, the physicians in this cross-sectional study were sampled from internet panels. Although we conducted stratified sampling through geographic and subspecialty distributions, the registered physicians could still have been different from general physicians. However, 35% of physicians belonged to university hospitals or institutes in this study, and this figure was consistent with 27% from the physicians’ census.41 The age distribution was similar to that of the same census.41 Therefore, our samples should be considered reflective of the actual situation in Japan. Second, we presented many questionnaire items and compared them between the characteristic variables. Although the accompanying p values represented the degree of reliability of associations, they should be interpreted cautiously and considered exploratory. Finally, the results of the cross-sectional study did not always reflect actual behaviours. Reporting biases might exist because we asked about delicate experiences related to potentially inappropriate research behaviours. However, other methods, such as direct observations, were flawed by the Hawthorne effect. Therefore, we anonymously conducted this study so that the participants could report their actual behaviours without the risk of blame, although recall bias was unavoidable.