Sci Eng Ethics https://doi.org/10.1007/s11948-018-0057-x REVIEW PAPER Integrity in Biomedical Research: A Systematic Review of Studies in China Nannan Yi1   · Benoit Nemery2   · Kris Dierickx1  Received: 27 June 2017 / Accepted: 1 April 2018 © Springer Science+Business Media B.V., part of Springer Nature 2018 Abstract  Recent empirical evidence has demonstrated that research misconduct occurs to a substantial degree in biomedical research. It has been suggested that scientific integrity is also of concern in China, but this seems to be based largely on anecdotal evidence. We, therefore, sought to explore the Chinese situation, by making a systematic review of published empirical studies on biomedical research integrity in China. One of our purposes was also to summarize the existing body of research published in Chinese. We searched the China National Knowledge Infrastructure, Wanfang Data, PubMed and Web of Science for potentially relevant studies, and included studies meeting our inclusion criteria, i.e. mainly those presenting empirically obtained data about the practice of research in China. All the data was extracted and synthesized using an inductive approach. Twenty-one studies were included for review. Two studies used qualitative methods (interviews) and nineteen studies used quantitative methods (questionnaires). Studies involved mainly medical postgraduates and nurses and they investigated awareness, attitudes, perceptions and experiences of research integrity and misconduct. Most of the participants in these 21 studies reported that research integrity is of great importance and that they obey academic norms during their research. Nevertheless, the occurrence of research misbehaviors, such as fabrication, falsification, plagiarism, improper authorship and duplicate submission was also reported. Strengthening research integrity training, Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/ s1194​8-018-0057-x) contains supplementary material, which is available to authorized users. * Kris Dierickx kris.dierickx@kuleuven.be 1 Centre for Biomedical Ethics and Law, Department of Public Health and Primary Care, KU Leuven - University of Leuven, Kapucijnenvoer 35, Blok D, Box 7001, 3000 Leuven, Belgium 2 Centre for Environment and Health, Department of Public Health and Primary Care, KU Leuven - University of Leuven, O&N 1, Herestraat 49, Box 706, 3000 Leuven, Belgium 13 N. Yi et al. developing the governance system and improving the scientific evaluation system were areas of particular attention in several studies. Our review demonstrates that a substantial number of articles have been devoted to research integrity in China, but only a few studies provide empirical evidence. With more safeguard measures of research integrity being taken in China, it would be crucial to conduct more research to explore researchers’ in-depth perceptions and evaluate the changes. Keywords  Research integrity · Research misconduct · Academic integrity · Academic morality · Academic misconduct · Biomedical research · China Introduction Scientific research has been regarded as the scientists’ behavior of pursuing the truth and should be conducted following the principle of integrity (Engel 2015; “Integrity mentors” 2014; Lins and Carvalho 2014). However, according to numerous reports in the past decades, this principle is not always followed, thus possibly hindering scientific progress throughout the world (Gardner et al. 2005; Hawkes 2014; Patnaik 2016; Okonta and Rossouw 2014; Steen 2011). As reported, research misconduct also exists in medical research, which is even more worrying than other areas (Fanelli 2009; Sabir et al. 2015; Steneck 2006). With the rapid economic development in the past decades, China has made considerable efforts in biomedical scientific research (Guo 2010; Xie et al. 2014). With this huge investment, China is expected to produce research achievements of good quality (Grayson 2015; Wang 2015). However, like many other countries, China is also facing the challenge of research misconduct (Jia 2006; Yang 2013). In recent years, a lot of attention from the international scientific community has been paid to the issue of research misconduct in China, which not only curbs Chinese devotion to the world’s scientific development, but also harms the mutual trust and international collaboration with other countries (Baždarić et al. 2012; Tang 2010; Xin 2006). Nonetheless, Chinese biomedical researchers’ perception on this issue remains understudied. It has been claimed that scientific integrity is also of concern in China, and that research misconduct in China has its own reasons and appearance, which differs from those in some other countries (Hu and Wu 2013; Hvistendahl 2013; Li 2013; Tucker et  al. 2011). However, this has not been systematically established. This article presents a systematic review of published empirical studies about research integrity and misconduct in Chinese biomedical research. Through this review, we aim at getting a comprehensive view of existing research that has been conducted in China about the awareness, attitudes, perceptions and experiences of biomedical researchers regarding research integrity and misconduct. 13 Integrity in Biomedical Research: A Systematic Review of Studies… Methods Data Sources A literature search was performed using the following databanks: China National Knowledge Infrastructure (CNKI), Wanfang Data (Wanfang), PubMed and Web of Science (WoS). Key words of disciplines in the biomedical domain were combined with words related to research integrity and misconduct, that are widely used in Chinese or English (Table 1) (Cao 2007; Fang et al. 2014; Yi et al. 2017). The document type was restricted to (journal) articles. The search was conducted in May and June 2016. Inclusion and Exclusion The retrieved articles were first screened on the basis of titles and abstracts. For articles whose titles and abstracts could not provide enough information for inclusion or exclusion, the full texts were read. If it was unclear whether an article met the inclusion criteria, an agreement was reached between Nannan Yi (NY) and Kris Dierickx (KD). Inclusion Criteria Studies included in the review had to meet the following requirements: (1) To explore the perception and experiences of research integrity and misconduct, (2) to be confined to a biomedical area, (3) to be based on empirical research (i.e. with quantitative or qualitative research methods used to collect primary data) and (4) to be peer-reviewed. The term “academic misconduct” has two meanings in China: one meaning concerns misbehavior by students in the classroom, cheating at examinations and so on; the other meaning includes fabrication, falsification, or plagiarism (FFP) and other misbehaviors in scientific research. In general, Chinese scholars agree on the second meaning (Cao 2005; Chen 2011; Liu 2011), but some scholars also use “academic misconduct” to refer to both meanings (Fan et  al. 2013). In this review, we used only the second meaning to include studies. Exclusion Criteria Following articles were excluded: (1) articles outside our research question, (2) articles without primary data (i.e. editorials, opinions, recommendations, etc.). 13 N. Yi et al. Table 1  Search strategy applied in China National Knowledge Infrastructure (CNKI) (a), Wanfang Data (Wanfang) (b), PubMed (c) and Web of Science (WoS) (d) (a) Search strategy applied in CNKI 主题: (‘医学’+‘医科’+‘医生’+‘医师’+‘药学’+‘药师’+‘药士’+‘生物医学’+‘中医’+‘中药’+‘中西医’+‘护 理’+‘护士’+‘护师’)*(‘学术道德’+‘科研道德’+‘科学道德’+‘学术规范’+‘科研规范’+‘学术诚信’+‘科研 诚信’+‘科学诚信’+‘学术失范’+‘科研失范’+‘科学失范’+‘学术不端’+‘科研不端’+‘科学不端’+‘学术失 信’+‘科研失信’+‘学术造假’+‘科研造假’+‘科学造假’+‘学术腐败’+‘科研腐败’+‘科学腐败’+‘学术不良 行为’) 跨库选择:期刊、特色期刊、学术辑刊 Translated to English: SUBJECT=(“medicine” OR “medical” OR “physician” OR “pharmac*” OR “pharmacist” OR “biomedic*” OR “Traditional Chinese Medicine” OR “Chinese herbs” OR “Traditional Chinese and Western Medicine” OR “nursing” OR “nurse”) AND (“academic morality” OR “research morality” OR “scientific morality” OR “academic norm(s)” OR ”research norm(s)” OR ”academic integrity” OR “research integrity” OR “scientific integrity” OR “academic anomie” OR “research anomie” OR “scientific anomie” OR “academic misconduct” OR “research misconduct” OR “scientific misconduct” OR “academic dishonesty” OR “research dishonesty” OR “academic fraud” OR “research fraud” OR “scientific fraud” OR “academic corruption” OR “research corruption” OR “scientific corruption” OR “academic misbehavior”) Selection of databases: periodical, characteristic periodical and academic proceeding (b) Search strategy applied in Wanfang 主题: (‘医学’+‘医科’+‘医生’+‘医师’+‘药学’+‘药师’+‘药士’+‘生物医学’+‘中医’+‘中药’+‘中西医’+‘护 理’+‘护士’+‘护师’)*(‘学术道德’+‘科研道德’+‘科学道德’+‘学术规范’+‘科研规范’+‘学术诚信’+‘科研 诚信’+‘科学诚信’+‘学术失范’+‘科研失范’+‘科学失范’+‘学术不端’+‘科研不端’+‘科学不端’+‘学术失 信’+‘科研失信’+‘学术造假’+‘科研造假’+‘科学造假’+‘学术腐败’+‘科研腐败’+‘科学腐败’+‘学术不良 行为’) 文献类型:期刊论文 Translated to English: SUBJECT=(“medicine” OR “medical” OR “physician” OR “pharmac*” OR “pharmacist” OR “biomedic*” OR “Traditional Chinese Medicine” OR “Chinese herbs” OR “traditional chinese and western medicine” OR “nursing” OR “nurse”) AND (“academic morality” OR “research morality” OR “scientific morality” OR “academic norm(s)” OR ”research norm(s)” OR ”academic integrity” OR “research integrity” OR “scientific integrity” OR “academic anomie” OR “research anomie” OR “scientific anomie” OR “academic misconduct” OR “research misconduct” OR “scientific misconduct” OR “academic dishonesty” OR “research dishonesty” OR “academic fraud” OR “research fraud” OR “scientific fraud” OR “academic corruption” OR “research corruption” OR “scientific corruption” OR “academic misbehavior”) Document type: periodical article (c) Search strategy applied in PubMed Title/Abstract=(“research integrity” OR “academic integrity” OR “scientific integrity” OR “research misconduct” OR “academic misconduct” OR “scientific misconduct” OR “academic dishonesty” OR “scientific dishonesty” OR “research fraud” OR “scientific fraud” OR “academic fraud” OR “responsible conduct of research” OR “academic corruption” OR “research dishonesty” OR “research corruption” OR “scientific corruption” OR “questionable research practice” OR “academic misbehavior” OR “research misbehavior” OR “scientific misbehavior” OR “academic morality” OR “research morality” OR “scientific morality” OR “academic disintegrity” OR “ scientific disintegrity”) AND (“China” OR “Chinese”) Filters: Journal Article (d) Search strategy applied in WoS TS=((“medic*” OR “pharmac*” OR “biolog*” OR “clinic*” OR “nurs*” OR “biomedic*” OR “physician” OR “surgeon”) AND (“research integrity” OR “academic integrity” OR “scientific integrity” OR “research misconduct” OR “academic misconduct” OR “scientific misconduct” OR “research dishonesty” OR “academic dishonesty” OR “scientific dishonesty” OR “research fraud” OR “scientific fraud” OR “academic fraud” OR “responsible conduct of research” OR “academic corruption” OR “research corruption” OR “scientific corruption” OR “questionable research practice” OR “academic misbehavior” OR “research misbehavior” OR “scientific misbehavior” OR “academic morality” OR “research morality” OR “scientific morality” OR “research disintegrity” OR “academic disintegrity” OR “ scientific disintegrity”) AND (“China” OR “Chinese”)) Document type: article 13 Integrity in Biomedical Research: A Systematic Review of Studies… Data Extraction and Synthesis For each publication, characteristics including author(s), study design, sampling method and year of publication were extracted. The study results were extracted and classified according to different themes defined using an inductive approach. Figures (e.g. prevalence data) retrieved from quantitative studies were summarized with ranges (minimum value-maximum value). Quotes from the qualitative research were originally in Chinese, and they were translated to English by NY. Critical Appraisal The quality of the included studies was assessed using the criteria developed by Kmet et  al. (2004). These criteria include two separate scoring lists for quantitative studies and qualitative studies, respectively. The score represents the degree to which the specific criteria were met (“yes” = 2, “partial” = 1, “no” = 0). For quantitative or qualitative studies, quality was assessed with the corresponding scoring lists. For studies using mixed research methods, quality was assessed with the two scoring lists separately and then the average score was calculated. Results Study Selection The search in the four databases identified 1578 records, which was reduced to 1311 records after removal of duplicates (Fig. 1). Most of these publications did not fit with Records identified in CNKI, Wanfang, PubMed and WoS: 1578 Records after duplicates removed: 1311 Records excluded on basis of titles and abstracts Outside research question: 524 Non-empirical articles: 729 Records retained: 58 Records excluded on basis of full texts Outside research question: 1 Non-empirical articles: 36 Articles included: 21 Fig. 1  The process of study selection 13 N. Yi et al. our inclusion criteria: 335 were journal notifications of application of anti-plagiarism software, 182 were announcements promoting research integrity or prohibiting research misconduct, including national guidelines and journal statements, etc. Many publications were not based on empirical data, but on theoretical considerations. In the end, based on our inclusion and exclusion criteria, we identified 21 studies containing empirical data, all written in Chinese. Most of these studies (18) used quantitative research methods (surveys), two studies were based on qualitative research, and one “mixed method” studied used both approaches. Study Characteristics The characteristics including author(s), study design, sampling method and year of publication are shown in Table 2. The included studies contained a broad variety of participants (Table 2): the authors of one medical journal, postgraduates (majoring in western medicine, traditional Chinese medicine, pharmacy, nursing and others), clinical nurses and supervisors of medical postgraduates. These participants had been recruited from universities, hospitals and other institutions in more than 10 cities throughout China. (Some studies did not specify the institution of the participants or they just listed a few geographical locations.) Quality Assessment Results of the quality assessment are shown in Tables 3 and 4. The scores [according to Kmet et al. (2004)] of the quantitative studies ranged between 0.64 and 0.93, with a mean of 0.87. The scores of the two qualitative studies were both 0.70. The score of the study with mixed methods was 0.44 (average of 0.58 and 0.30). We defined four main themes: (1) the perception of academic norms and research misconduct, (2) perceived prevalence of research misconduct, (3) attitudes towards research misconduct, and (4) suggestions to promote research integrity. In these studies, different keywords were used. For instance,“学术诚信 (academic integrity)” and “学术道德 (academic morality)” were used to refer to issues related to research integrity, while “学术不端 (academic misconduct)”, “科研中的失信行为 (dishonest behavior(s) in research)”, “学术失范 (academic anomie)” and “违反学术 规范 (violations of academic norms)” were used to refer to issues related to research misconduct. Considering the different concepts and terms used in Chinese and English and to be consistent in the words (Yi et  al. 2017), we used “research integrity” and “research misconduct” to replace relevant phrases in included studies, respectively. Academic Norms and Research Misconduct Awareness of Academic Norms In general, according to four studies, a majority of the respondents (63–99.5%) indicated awareness of the academic norms (Fan and Yi 2015; Guo et  al. 2015; 13 Wu, X, et al. Xu, Z, et al. Song, D, et al. Nursing Postgraduate Students’ Recognition and Attitude Toward Research Integrity 护理学专业研究生 Survey of Status 学术失范现状调查 Quo of Academic Misconduct of Graduates in Nursing Profession 七年制本硕医学生 Survey and Analysis 学术诚信状况调查 of the state quos of 与分析 academic integrity among medical students of seven-year program* 护理硕士研究生对 科研诚信的认识 与态度 Sampling method Logitudinal study of medical students (seven-year program) in Guangxi Medical University Logitudinal survey and in-depth interview of nursing postgraduates in a university Descriptive survey: effective response rate 71.8% (467/650) Unstated Unstated Descriptive survey: survey(effective response rate 96% (96/100)) + indepth interview with 12 participants Interview study: face- Purposive sampling to-face non-structured interviews with 10 participants Study design Logitudinal study of Interview study: face- Purposive sampling to-face in-depth Master’s Students interviews with 12 in Nuring (those participants who have taken courses related to nursing research) in School of Nursing in a university Qualitative Research Zheng, Z, et al. Logitudinal study of nurses (clinical on the Writer’s Cogworking stanition and Behavior tus + with at least of Academic Mis2 publications) in conduct a grade A tertiary hospital Setting 作者学术不端认知 和行为情况的质 性研究 Authors Title (English) Table 2  Characteristics of included studies Title Unclear Unstated – – Survey administration method 2015 2013 2014 2014 Year of publication Integrity in Biomedical Research: A Systematic Review of Studies… 13 13 Title (English) Authors 医学研究生学术不 Survey Analysis and Wusiman, A 端行为的调查分析 Countermeasure 及对策研究—以新 Research on Aca疆医科大学为例 demic Misconducts of Medical Graduates-Taking Xinjiang Medical University as a Example 高等中医院校研究 Fan, X, et al. Study of Academic 生学术廉洁文化 Integrity Culture 调查与建设路径 Survey and Con探究—以福建中医 struction Path of 药大学为例 Graduate of TCM— Based on the Survey of Fujian University of Traditional Chinese Medicine 导师视角下的研究 Guo, L, et al. An Investigation of 生学术道德规范教 Post Graduates’ 育现况调查 Ethics Education From the Perspective of a Thesis Advisor Title Table 2  (continued) Unstated Unstated Random sampling Unstated Logitudinal study of Descriptive survey: effective response medical postgradurate 93.0% ates in Fujiang (465/500) University of Traditional Chinese Medicine Logitudinal survey of Descriptive survey: effective response medical promoters rate 84.7% in Peking Univer(375/443) sity Health Science Center Survey administration method Unstated Sampling method Random sampling Study design Descriptive survey: Logitudinal study effective response of second-year rate 93.3% Master’s Students (280/300) in Xinjiang Medical University Setting 2015 2015 2015 Year of publication N. Yi et al. Table 2  (continued) Title (English) Authors Zhao, S, et al. 药学研究生学术道 德培养与保障体 系研究 Academic moral training system research and security research of pharmacognosy Long, L, et al. 医学研究生学术不 Survey and analysis 端行为的调查分析 of academic misconduct among medical postgraduate 研究生学术规范认 Chen, H, et al. Investigating and 知及学术失范行为 analyzing the cogni的调查分析 tive of academic criterion and the behavior of academic anomie in graduate students 综合性大学医学研 Lin, Q, et al. Investigation and 究生学术道德现状 analysis of medical 调查与分析 postgraduates’ academic moral status quo Title Logitudinal study of medical postgraduates in Shenyang Pharmaceutical University Descriptive survey: effective response rate 92.4% (462/500) Logitudinal survey of Descriptive survey: effecmedical posttive response rate graduates trained 90.9%(120/132) in Xinjiang Uiger Municipal People’s Hospital Unstated Unstated Handed out + online Unstated Unstated Unstated Descriptive survey: effective response rate 96.9% (483/500) Logitudinal study of medical postgraduates in First School of Clinical Medicine, Wuhan University Survey administration method Unstated Sampling method Unstated Descriptive survey: response rate 92.3% (277/300) Study design Logitudinal study of Master’s Students in the First Affiliated Hospital of Wenzhou Medical University Setting 2014 2014 2014 2014 Year of publication Integrity in Biomedical Research: A Systematic Review of Studies… 13 13 Survey of Academic Literacy and Academic Standardization Among Medical Postgraduates* 医学研究生学术素 养及学术规范情 况调查 Li, L, et al. Authors 《武警医学》作者 Li, X, et al. Survey on Cogni学术不端认知与行 tion and Behavior 为调查分析 About Academic Misconduct Among Authors of Medical Journal of the Chinese People’s Armed Police Forces 临床护士对科研诚 Liu, M, et al. Investigation of 信认识及科研规 the cognition of 范了解度的调查 scientific research 分析 integrity and know status of scientific research standard among clinical nurses 医科研究生学术道 Lu, J, et al. Surveying Medical 德失范行为的调查 Graduate Students’ Behaviors Against Academic Morals Title (English) Title Table 2  (continued) Study design Descriptive survey: effective response rate 87.0% (296/340) Convenience sampling Unstated Descriptive survey: response rate 71.5% (261/365) Cluster sampling Sampling method Cluster sampling Logitudinal survey of Descriptive survey: response rate 98.9% medical postgradu(1173/1186) ates in a military medical university Logitudinal survey of clinical nurses (working experience ≥ 5y + with publication) in 13 grade A tertiary hospitals of 7 cities Logitudinal survey of authors of the Medical Journal of the Chinese People’s Armed Police Forces (publishing in the last 2 years) Logitudinal survey of Descriptive survey: effective response medical postgradurate 95.2% ates in a medical (762/800) university Setting 2013 2013 Year of publication Unstated 2012 Handed out by the 2013 nursing department Email Handed out Survey administration method N. Yi et al. Liu, M, et al. Li, Y, et al. Nursing Research 13所三级甲等医院 Integrity Among 308名临床护士护 308 Clinical Nurses 理科研诚信状况调 查分析 医学院校研究生科 Reasons and Solu研诚信缺失的原因 tions of Dishonesty 与对策研究 in Research Among Postgraduates in Medical Colleges and Universities* Lu, J, et al. Liu, M, et al. A Survey on Medical Graduate Students’ Attitudes Toward Academic Ethical Misconducts 医科研究生对学术 道德失范的态度 调查 Authors 临床护士科研诚信 Investigation on 意识调查及影响因 Research Integrity 素分析 Awareness Among Clinical Nurses and Influencing Factors Title (English) Table 2  (continued) Title Study design Unstated Handed out by the counselors 2012 2012 Handed out by the nursing administrative department Convenience sampling Descriptive survey: effective response rate 90.6% (308/340) 2012 Year of publication 2012 Handed out by the nursing administrative department Unstated Survey administration method Convenience sampling Cluster sampling Sampling method Descriptive survey: effective response rate 89.1% (286/321) Logitudinal survey of Descriptive survey: effective response medical postgradurate 96.6% ates in Shanghai (338/350) University of Traditional Chinese Medicine Logitudinal survey of clinical nurses (working experience ≥ 5y + with publication) in 13 grade A tertiary hospitals of 7 cities Logitudinal survey of clinical nurses (working experience ≥ 5y + with publication) in 13 grade A tertiary hospitals of 7 cities Logitudinal survey of Descriptive survey: effective response medical postgradurate 98.9% ates in a medical (1173/1186) university Setting Integrity in Biomedical Research: A Systematic Review of Studies… 13 13 Title (English) Study design Sampling method Random sampling Logitudinal survey of Descriptive survey: effective response medical postrate 98.0% (98/100) graduates in Third Military Medical University Setting Cluster sampling Wang, Q, et al. Logitudinal survey of Descriptive survey: response rate 92.4% final-year medical (424/459) postgraduates in Peking University Health Science Center Peng, Z, et al. Authors *There is no English translation in the original article. The English title was translated by NY 浅谈医学研究生科 Analysis of the 研诚信存在的问题 Academic Honesty 及对策 Among the Medical Postgraduate Students and Its Strategies 北京大学医学部研 Academia criterion 究生学术规范教育 education of gradu的调查分析 ated students in Pekjng University Health Science Center Title Table 2  (continued) Unstated Handed out Survey administration method 2007 2010 Year of publication N. Yi et al. 1 2 Method of 1 subject/ comparison group selection or source of information/input variables described and appropriate? Subject (and 0 comparison group, if applicable) characteristics sufficiently described? 3 4 2 Study design N/A evident and appropriate? 2 2 1 Question/ objective sufficiently described? 2 2 2 2 2 2 2 2 2 1 2 2 2 1 2 2 2 1 2 2 2 1 2 2 0 1 2 1 2 2 2 2 2 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Guo Chen Lin Long Zhao Li Li Liu Lu Lu Liu Liu Xu Song Wusi- Fan (2015) (2015) (2014a) (2014) (2014) (2014) (2013a) (2013b) (2013) (2012a) (2012b) (2012a) (2012b) (2013) (2015) man (2015) Scores 1 Criteria Table 3  Quality of quantitative studies and mixed-methods studies 2 1 2 2 2 2 2 1 Li Peng (2012) (2010) 2 2 2 2 Wang (2007) Integrity in Biomedical Research: A Systematic Review of Studies… 13 13 N/A N/A If interventional and blinding of investigators was possible, was it reported? If intervenN/A tional and blinding of subjects was possible, was it reported? 6 7 N/A N/A If intervenN/A tional and random allocation was possible, was it described? N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A Guo Chen Lin Long Zhao Li Li Liu Lu Lu Liu Liu Xu Song Wusi- Fan (2015) (2015) (2014a) (2014) (2014) (2014) (2013a) (2013b) (2013) (2012a) (2012b) (2012a) (2012b) (2013) (2015) man (2015) Scores 5 Criteria Table 3  (continued) N/A N/A N/A N/A N/A N/A Li Peng (2012) (2010) N/A N/A N/A Wang (2007) N. Yi et al. N/A N/A N/A Analytic methods described/ justified and appropriate? N/A Some estimate of variance is reported for the main results? 11 N/A 10 N/A Sample size appropriate? 9 2 Outcome 2 and (if applicable) exposure measure(s) well defined and robust to measurement/misclassification bias? means of assessment reported? N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 2 N/A N/A N/A 1 N/A N/A N/A 2 Guo Chen Lin Long Zhao Li Li Liu Lu Lu Liu Liu Xu Song Wusi- Fan (2015) (2015) (2014a) (2014) (2014) (2014) (2013a) (2013b) (2013) (2012a) (2012b) (2012a) (2012b) (2013) (2015) man (2015) Scores 8 Criteria Table 3  (continued) N/A N/A N/A 2 N/A N/A N/A 1 Li Peng (2012) (2010) N/A N/A N/A 2 Wang (2007) Integrity in Biomedical Research: A Systematic Review of Studies… 13 13 Results reported in sufficient detail? Conclusions supported by the results? 13 14 Summary score Controlled for confounding? 12 Criteria 2 2 0.86 1 1 0.58 N/A N/A 0.93 2 1 N/A 0.93 2 1 N/A 0.86 2 1 N/A 0.86 2 1 N/A 0.86 2 1 N/A 0.86 2 1 N/A 0.64 2 1 N/A 0.93 2 1 N/A 0.86 2 1 N/A 0.93 2 1 N/A 0.93 2 1 N/A 0.93 2 1 N/A 0.86 2 1 N/A 0.93 2 1 N/A Guo Chen Lin Long Zhao Li Li Liu Lu Lu Liu Liu Xu Song Wusi- Fan (2015) (2015) (2014a) (2014) (2014) (2014) (2013a) (2013b) (2013) (2012a) (2012b) (2012a) (2012b) (2013) (2015) man (2015) Scores Table 3  (continued) 0.86 2 1 N/A 0.78 2 1 N/A Li Peng (2012) (2010) 0.93 2 1 N/A Wang (2007) N. Yi et al. Integrity in Biomedical Research: A Systematic Review of Studies… Table 4  Quality of qualitative studies and mixed-methods studies Criteria Scores Zheng (2014) Wu (2014) Xu (2013) 1. Question/objective sufficiently described? 2 2 1 2. Study design evident and appropriate? 2 2 1 3. Context for the study clear? 2 2 1 4. Connection to a theoretical framework/wider body of knowledge? 1 1 1 5. Sampling strategy described, relevant and justified? 2 2 0 6. Data collection methods clearly described and systematic? 1 1 0 7. Data analysis clearly described and systematic? 2 2 0 8. Use of verification procedure(s) to establish credibility? 0 0 0 9. Conclusions supported by the results? 2 2 2 10. Reflexivity of the account? 0 0 0 Summary score 0.70 0.70 0.30 Li et al. 2013a; Wusiman 2015). However, when asked about the national or university guidelines, most of those surveyed stated that they were unaware of these guidelines. In one survey of 280 medical postgraduates, the majority of participants (98%) reported to be unaware of “Opinions on Strengthening Academic Morality (关于加强学术道德建设的若干意见)” published by the Ministry of Education (Wusiman 2015). Many postgraduates (61%) indicated to know that the university had relevant guidelines but they had no idea of their content (Song et al. 2015). About one-third of the supervisors reported to be unaware of how the university dealt with research misconduct (Guo et al. 2015). Perception of Research Misconduct Based on a study of 120 postgraduates, Long et al. found that most postgraduates (69%) reported to be aware or relatively aware of the definition of research misconduct. The higher the number of years into training, the higher the awareness was (Long and Yang 2014). Specifically, the awareness varied for different forms of research misconduct. In a survey of authors of scientific articles, fabrication, falsification and plagiarism (FFP) were identified as research misconduct by the majority (88%) of the scientific authors, whilst improper authorship (62%), duplicate submission (56%), salami publication (56%), improper citation (30%) were considered to be research misconduct by fewer scientific authors (Li et al. 2013b). In another study, fewer medical students considered using others’ results without citation (17%), coauthorship without contribution (9%), duplicate submission (20%) as forms of research misconduct (Song et al. 2015). 13 N. Yi et al. Perception of Factors Responsible for Research Misconduct Several studies (Chen et  al. 2014a; Li et  al. 2012; Lin et  al. 2014; Liu and Zhou 2012a; Long and Yang 2014; Wusiman 2015; Xu et al. 2013) have attempted to find out how research misconduct may occur, at least as perceived by various categories of researchers. In summary, the main factors that were perceived responsible for research misconduct included the unhealthy atmosphere of the society/institution (22–38%), insufficient research ability (7–26%), insufficient knowledge of academic norms (14–19%), limitations of the education/evaluation system (12–87%), lack of heteronomy/supervision (10–67%), lack of guidance/training (in both research skills and research integrity) (8–37%), lack of self-discipline (12–18%), too much pressure to publish (23–24%) and others. Awareness of Measures Safeguarding Research Integrity Four studies (Long and Yang 2014; Song et al. 2015; Wang et al. 2007; Wusiman 2015) dealt with the main approaches to safeguard research integrity. Thus medical postgraduates reported to have learnt about the knowledge of academic norms and research misconduct through courses, lectures or campus dissemination of the university (16–37%), guidelines of the university (14–29%), online study (16–42%), supervisor’s or senior postgraduates’ emphasis (12–36%), the (good) examples nearby (6%) and other means. Perceived Prevalence of Research Misconduct Self‑evaluation and Perception of the General Research Practices With regard to general research practices, two aspects, including the awareness of academic norms and practices of research misconduct, were investigated by asking participants about their own behaviors and their perception of the general research environment. On one hand, in terms of self-report, more than half of the medical postgraduates indicated that they had the academic norms in mind during their research and the writing process of their thesis (Li et  al. 2013a; Xu et  al. 2013). A small portion (18%) of the 338 postgraduates in one study reported that their awareness of research integrity was weak (Li et  al. 2012). According to three studies, 10–32% of postgraduates admitted that they had committed research misconduct (Li et  al. 2013a; Lin et al. 2014; Lu and Zhou 2012). On the other hand, the perception of the general research environment was explored among nurses, postgraduates and supervisors. Generally, based on four studies, the majority of the respondents were satisfied with the general environment (Guo et al. 2015; Li et al. 2013a; Liu and Zhou 2012a; Wang et al. 2007). Nevertheless, when asked about the perception of research misconduct, paradoxically, a number of supervisors from the same study indicated that research misconduct was serious among postgraduates (48%) and teachers (35%) (teachers here included those 13 Integrity in Biomedical Research: A Systematic Review of Studies… professors, associate professors, lecturers and teaching assistants in universities who were also involved in scientific research) (Guo et al. 2015). In addition, according to six other studies, a considerable proportion of the respondents (30–60%) stated to be aware of the existence of research misconduct among their peers (Chen et al. 2014a; Li et al. 2013b; Liu and Zhou 2012a; Long and Yang 2014; Wang et al. 2007; Wusiman 2015). Perceived Prevalence of Specific Forms of Research Misbehavior Eight studies gave examples of research misconduct and reported their prevalence. The most mentioned forms of research misconduct in these reviewed studies include fabrication and falsification of data (self-report prevalence 2–19%, observed prevalence among others 15%), plagiarism (self-report prevalence 2–11%, observed prevalence 10%), improper authorship (observed prevalence 11%), duplicate submission (self-report prevalence 16%, observed prevalence 7%), duplicate publication (observed prevalence 4%) and improper citation (18%) (Chen et al. 2014a; Li et al. 2013b; Lin et al. 2014; Lu and Zhou 2012; Peng et al. 2010; Wang et al. 2007). In addition, some other behaviors were also reported, such as providing or using false certificate(s) (2%), ghost writer/transaction of academic products (7–8%), making a new article based on the pieces of others’ publications (2–20%), writing papers for others or having others write for one’s self (6%), interfering with the editor during submission (2%), imitating supervisors’ signature (in application for scholarships, funds and so on) (Guo et al. 2015; Lin et al. 2014; Lu and Zhou 2012; Wang et al. 2007; Xu et al. 2013). Attitudes Towards Research Misconduct Respondents’ opinions of research misconduct were mixed. Opinions included objection (“feeling ashamed for those who misbehaved”, “cannot tolerate research misconduct”, “object to research misconduct firmly” or “sticking to academic norms is extremely important and compulsory”) (39–79%), acceptance (“can accept/understand/forgive research misconduct” or “sticking to academic norms is relatively important but sometimes flexible”) (7–43%) and indifference (“It doesn’t matter” or “It is not so important”.) (1–22%) (Chen et al. 2014a; Li et al. 2013a, b; Lin et al. 2014; Long and Yang 2014; Lu et al. 2012; Wusiman 2015). Regarding the opinions on research misconduct, a challenging paradox was observed. On the one hand, at the principle level, nursing postgraduates generally opposed research misconduct. As some students stated, “Plagiarism is a reflection of irresponsibility towards yourself and others” (Wu et al. 2014). Also, in one quantitative study, 79% of the medical postgraduates indicated “obeying academic norms is very important and compulsory” (Li et al. 2013a). Nevertheless, on the other hand, at the practical level, some of them showed understanding attitudes. Thus, some nursing postgraduates held these views: “For the first time to hear (research misconduct), I found it was unbelievable, and then I found everyone did that, so it’s OK, it’s somewhat understandable” (Wu et al. 2014). Moreover, when asked about specific 13 N. Yi et al. forms of research misconduct- (plagiarism and data fabrication), in comparison to the attitudes towards general research misconduct reported above, only 51% of the medical postgraduates indicated “cannot tolerate” (Li et  al. 2013a). This paradox illustrates how attitudes may differ between principles and practice. Some studies went beyond just asking about opinions, they also enquired about responses to research misconduct. A small group of postgraduates (11–27%) reported that they would take measures against research misconduct or report it, while a majority of postgraduates indicated indulgence: they would not report or they held an indifferent attitude (Chen et al. 2014a; Lin et al. 2014). Nevertheless, concerning their own research, most of the respondents (82–92%) indicated that they would take measures to protect their own publications or research results against plagiarism or other misbehaviors (Chen et al. 2014a; Liu and Zhou 2012a), which might be a sign of higher concerns of their own rights. Suggestions to Improve Research Integrity In addition to the perception and attitude toward research integrity and misconduct, some suggestions to promote research integrity were also sought in these studies, from both the study participants and investigators. Efforts were expected to improve the governance system, the evaluation system and training. Suggestions by the Participants Improvement of four aspects were suggested by the participants. Firstly, to develop the governance system, some specific measures were suggested: developing the guidelines and policies, application of the academic misconduct detection system(s), building up a management department of research integrity (70%), signing a research integrity pledge (75%), strengthening supervisors’ supervision (11%), creating a bank of authors who misbehaved, absolute blind peer review, audit after publication, request for necessary original data, punishing serious misconduct, etc. (Chen et al. 2014a; Guo et al. 2015; Li et al. 2013b; Li et al. 2012; Wusiman 2015). Secondly, in order to improve the scientific evaluation system, the emphasis on the number of publications and the excessive publication pressure shoud be reduced (Chen et al. 2014a; Guo et al. 2015; Li et al. 2013b; Wusiman 2015). In addition, hospitals should not require members of their staff to publish scientific papers for evaluation and promotion (Li et al. 2013b). Thirdly, the respondents also suggested to enhance the training of researchers (Chen et  al. 2014a; Guo et  al. 2015). They stated that research integrity training could be added to the curriculum of postgraduates (43–76%) and the pre-enrollment training (81%), and that focused activities of research integrity training (81%) could also be organized (Guo et al. 2015; Li et al. 2012; Wusiman 2015). In addition, the training of supervisors should be enhanced as well (13%) (Guo et al. 2015). In more detail, research integrity training should include relevant laws/guidelines (74%), case analysis (55%) (especially mentioned by young supervisors), punishment of 13 Integrity in Biomedical Research: A Systematic Review of Studies… research misconduct (54%), detailed guidance on article writing (46%) (Guo et al. 2015). Moreover, specific sections on research integity in scientific journals could improve the awareness and knowledge of research integrity (Li et al. 2013b). Furthermore, a well respected academic atmosphere was believed to be one important factor for ensuring research integrity (Chen et al. 2014a; Guo et al. 2015; Li et al. 2013b). Suggestions by the Investigators Based on the empirical data, the authors of these 21 studies also proposed suggestions to promote research integrity. Firstly, as suggested by 20 out of the 21 included studies, training should be organized on: (1) the research ability (Fan and Yi 2015; Liu and Zhou 2012a, b), (2) the scientific spirit (Fan and Yi 2015; Li et al. 2013a; Liu and Zhou 2012b, 2013) and (3) research integrity (Chen et al. 2014a; Fan and Yi 2015; Guo et al. 2015; Li et al. 2013a; Li et al. 2012; Lin et al. 2014; Liu and Zhou 2012a, b, 2013; Long and Yang 2014; Lu et al. 2012; Lu and Zhou 2012; Peng et al. 2010; Song et al. 2015; Wang et al. 2007; Wu et al. 2014; Wusiman 2015; Xu et al. 2013; Zhao and Jia 2014; Zheng et  al. 2014). The definitions and examples of good research practices, the good practices of some prestigious senior researchers, the laws related to research practices, as well as the definitions of research misconduct, procedures for handling research misconduct and punishment for misconduct should be presented during the training (Long and Yang 2014; Song et al. 2015). And 12 studies proposed various forms of research integrity training (e.g. courses and lectures), tailored to different target groups, tied to the specific profession and daily research practices (Guo et al. 2015; Li et al. 2013a; Li et al. 2012; Liu and Zhou 2012a, b; Long and Yang 2014; Lu et al. 2012; Peng et al. 2010; Song et al. 2015; Wang et al. 2007; Xu et al. 2013; Zheng et al. 2014). Secondly, the current academic evaluation system needs to be reformed. The evaluation should give more emphasis to the research process rather than on the number of publications. In other words, the pressure to publish should be reduced. A multiple-indexed evaluation system should be developed (Fan and Yi 2015; Guo et al. 2015; Long and Yang 2014; Peng et al. 2010; Wang et al. 2007; Xu et al. 2013). Thirdly, some solutions were proposed to improve governance: guidelines and policies must be developed to oversee and tackle research misconduct (mentioned by 8 out of 21 studies) (Fan and Yi 2015; Li et al. 2012; Liu and Zhou 2013; Long and Yang 2014; Lu and Zhou 2012; Wang et al. 2007; Wu et al. 2014; Xu et al. 2013), specialized departments should be established to promote research integrity and deal with research misconduct (Fan and Yi 2015; Wang et al. 2007; Xu et al. 2013), an (academic) credit system could be set up (Fan and Yi 2015; Song et al. 2015), and laws on research integrity are needed (Long and Yang 2014; Peng et al. 2010; Zhao and Jia 2014). To monitor research misconduct, detection technology could be applied (Li et al. 2013b; Zhao and Jia 2014). Once research misconduct has been identified, there should be punishments proportional to the magnitude of misconduct (Li et al. 2012; Liu and Zhou 2012a; Lu and Zhou 2012; Wang et al. 2007; Xu et al. 13 N. Yi et al. 2013). In addition, an appropriate model of research integrity could help to lead to acceptable research practices (Fan and Yi 2015). Further suggestions were raised for two main populations in these studies (medical postgraduates and nurses). For postgraduates, suggestions concerning supervisors’ mentoring were made. The following reasons emphasized the role of supervisors: Firstly, supervisors, being senior researchers, are expected to influence postgraduates positively by words and deeds (Guo et  al. 2015; Long and Yang 2014; Song et  al. 2015; Wu et  al. 2014; Zhao and Jia 2014). Secondly, in addition to being role models, supervisors should train and supervise postgraduates in research integrity (Guo et al. 2015; Long and Yang 2014; Peng et al. 2010; Wusiman 2015; Xu et al. 2013; Zhao and Jia 2014), research skills (Peng et  al. 2010; Xu et  al. 2013) and scientific spirit (Long and Yang 2014; Peng et al. 2010). As a consequence, in addition to improve the aspects above, the selection, appraisal and training (on research skills and research integrity) of supervisors should be enhanced (Chen et al. 2014a; Guo et al. 2015; Long and Yang 2014; Wusiman 2015; Zhao and Jia 2014). Moreover, supervisors should bear the joint liability when research misconduct by their postgraduates is identified (Guo et al. 2015; Zhao and Jia 2014). For nurses, efforts are expected to: (1) boost the investment in nursing research and (2) improve the governance of nursing research (Liu and Zhou 2012a, b, 2013). Additional data are given in Online Resource 1. Discussion The goal of our systematic review was to uncover what has been studied in China about biomedical researchers’ awareness, perceptions, attitudes and experiences of research integrity and misconduct. After systematic search and screening, we identified 21 studies that collected information from various populations using quantitative and qualitative methods. Interestingly, our review indicates that research integrity among nurses has been studied more in China than elsewhere. The reasons for this are not clear; this could be due to the specific requirement of having to publish article(s) to qualify for promotion, the higher salary and allowances of nurses in China, whereas this is not so frequent in other countries (Fanelli 2009; Okonta and Rossouw 2014; Sabir et al. 2015). In general, most of these studies share a common interest in (1) the perceived importance and compliance of academic norms, (2) the perceived definition and attitudes of research misconduct, (3) the forms, prevalence and responsible factors of research misconduct, as well as (4) solutions to promote research integrity. Forms and Prevalence of Biomedical Research Misconduct in China We conducted this systematic review as a first endeavor to establish whether biomedical research integrity in China is really of more concern than elsewhere (“China’s medical research integrity questioned” 2015). Our review does not give a formal 13 Integrity in Biomedical Research: A Systematic Review of Studies… answer to this question (this would require a comparative analysis), but it does provide an idea of the state of empirical research about scientific integrity in China. The available evidence suggests that Chinese researchers involved in these studies generally have a valid appreciation of academic norms (Fan and Yi 2015; Guo et al. 2015; Li et  al. 2013a; Wusiman 2015; Xu et  al. 2013). Nevertheless, this review also documents that research misbehaviors, such as fabrication and falsification of data, plagiarism, inappropriate authorship, duplicate submission, improper citation and using false certificate(s), transaction of academic products, exist in China (Chen et al. 2014a; Fan and Yi 2015; Guo et al. 2015; Li et al. 2013b; Lin et al. 2014; Lu and Zhou 2012; Peng et al. 2010; Wang et al. 2007; Xu et al. 2013). Some of these forms of misconduct have been reported before (Hu and Wu 2013; Xinhua News Agency 2009), but some features might differ from other regions, especially transaction of academic products is less reported in other countries (Hvistendahl 2013; Lins and Carvalho 2014; Okonta and Rossouw 2014). Regarding the prevalence of misbehaviors, the prevalence range proved to be wide, which might be related to the broad variation in participants and institutions included in the studies. The self-reported prevalence of fabrication and falsification of data (2–19%) and plagiarism (2–11%) in the Chinese studies appears to be higher than the average prevalence reported by Fanelli, who concluded mainly on the basis of studies in the US and the UK (Fanelli 2009), that “A pooled weighted estimate of 1.97% of scientists admitted to have fabricated, falsified or modified data or results”. However, the prevalence in China was lower than in one study in Nigeria, where 42.2% researchers admitted to have committed “falsification of data, falsification of biosketch, resume and plagiarism” (Okonta and Rossouw 2013). Nevertheless, owing to the differences in the methodological approaches and the sample sizes, we cannot draw firm conclusions. Moreover, it has been demonstrated that research misconduct in medicine is more prelvalent than in other domains (Fanelli 2009). Consequently, we need more evidence to situate the state of the integrity of Chinese biomedical research internationally. In general, the more serious the misconduct is, the lower its prevalence, which is consistent with the results of other studies (Ana et al. 2013; Fanelli 2009). However, the difference between the self-reported prevalence and the observed prevalence is not as marked as the difference observed by Fanelli (1.97% self-report prevalence of data or result fabrication, falsification or modification vs. 14.12% observed prevalence of falsification) (Fanelli 2009). This could be attributed to the factor that the background of the respondents in these studies is diverse and that they come from different universities, hospitals and other institutions, which may influence their perception of research integrity and their research practices. Again, it might be inappropriate to simply compare the percentages among these studies. As mentioned by Fanelli, reports on research misconduct might be biased by the way in which surveys are conducted, the influence of social expectations and the explicit use of the terms “fabrication”, “falsification” (Fanelli 2009). Hence, the reported prevalence in our study might also be a conservative estimate. The attitudes towards research misconduct are mixed. Most participants in these 21 studies found research misconduct objectionable, while others held an understanding or indifferent attitude. Regarding attitudes towards specific misbehaviors, 13 N. Yi et al. the existence of making a new article based on the pieces of others’ publications (Chen et  al. 2014a; Lin et  al. 2014; Peng et  al. 2010; Wang et  al. 2007) might be an indicator of higher tolerance of plagiarism, although these studies did not document obvious differences on the attitudes towards plagiarism and data fabrication or falsification. Concerning the current academic environment in China, quite a number of those surveyed did not have a positive evaluation (Li et al. 2013a; Liu and Zhou 2012a), which is in accordance with the CAST report (Xinhua News Agency 2009). The current social and research atmosphere, where a substantial number of researchers held an indifferent or even indulging attitude towards research misconduct (Chen et  al. 2014a; Lin et  al. 2014), is regarded as the breeding ground for misconduct. One included study revealed that senior postgraduates had higher tolerance for research misconduct than junior researchers (Lu et  al. 2012), which is consistent with the study referred to by Cyranoski where the students’ tolerance of misconduct increased with the time they stayed in the education system (Cyranoski 2012). With such an environment they study and work in, it is difficult to build honest culture in research (Binder et al. 2015; Grinnell 2014). The Scientific Evaluation System The pressure to publish is usually believed to be one of the main factors responsible for research misconduct (Luther 2010; Steneck 2002). Quantitative metrics of publication have been applied for graduation, promotion, fund allocation and salaries in many Chinese biomedical institutions (“China’s medical research integrity questioned” 2015; Peng et al. 2010). As Suo stated, “The current assessment system is not perfect but appropriate in China”. In Suo’s opinion, the current assessment of researchers’ academic performance in China is based on their publications, but both the quantity and quality are considered (Suo 2016). Although the quality of accepted papers is not completely controlled by the impact factor of the journal, compared to other indexes, SCI (Science Citation Index) papers and journal’s impact factor are more objective and fair (Suo 2016). Nevertheless, the current evaluation system remains of doubtful value and multiple criteria are expected to work (Chen et  al. 2014b; Hvistendahl 2013; Xu et  al. 2013). Currently, a reform is taking place at the Chinese Academy of Sciences (CAS), where the process of scientific research is given more attention (Huang 2015). Another dilemma is that some Chinese researchers, such as nurses, experience the pressure to publish, although they have hardly received systematic training on research methods and skills. This gap may contribute to certain misbehaviors. Unfortunately, this problem also exists in some other countries and regions (Ryan et al. 2012). Research Integrity Training This review has shown that most participants in the included studies have only a vague impression of the definition of research integrity and misconduct. Most 13 Integrity in Biomedical Research: A Systematic Review of Studies… participants in these studies stated to be aware of academic norms or the university guidelines, but not in detail (Li et al. 2013a; Song et al. 2015). The knowledge of research misconduct was mainly limited to fabrication, falsification, or plagiarism (FFP), while some other practices, such as improper authorship and duplicate submission were not always recognized as research misconduct (Guo et  al. 2015; Li et al. 2013b). Therefore, systematic training in research integrity may be needed to fill gaps in knowledge and awareness. Though the effectiveness of training in achieving changes of attitudes and practices needs further research (Schmaling and Blume 2009), it has proved to increase at least the knowledge of research integrity and misconduct (Anderson 2007; Fanelli et al. 2015; Jordan and Gray 2013; Li et al. 2012; Liu and Zhou 2012b). Besides, guideline and policy documents at both national and institutional levels cannot play the expected role because of inadequate publicity and training. In the last decades, the Chinese government and research institutions have published a series of policies and documents of research integrity, ranging from several-page guidelines to hundred-page manuals (Fudan University 2014; National Health and Family Planning Commission of the People’s Republic of China 2014; Ren 2012; Zeng and Resnik 2010). However, emphasis on the dissemination of these guidelines is still lacking (Cyranoski 2012; Michel 2010). In addition, junior researchers have poor knowledge of research integrity and misconduct (Li et al. 2013a), and many postgraduates appear to learn about research integrity from their supervisors and senior students. However, senior researchers do not necessarily have a precise knowledge of research integrity and misconduct and they are not immune from committing misconduct (Wiwanitkit 2016), especially when some questionable research practices are not deemed questionable. Therefore, formal training on research integrity is essential at all levels to spread the correct knowledge and avoid unintended misbehaviors. Additional Studies in the Last 2 Years Following a first review of our article, we checked in the databases (now including Google Scholar, the search strategy is given in Online Resource 2) whether important articles had been published between the completion of our search (June 2016) and January 2018. This, admittedly, less rigorous search identified 8 relevant articles (1 in English, 7 in Chinese), addressing the same issues as our previously included articles, such as knowledge of academic norms, prevalence of and attitudes towards research misconduct as well as suggestions to improve research integrity (Gao et al. 2016; Guo et al. 2017; Li et al. 2016; Li and Zhang 2017; Liao et al. 2017; Miao et al. 2017; J. Wang and Jiang 2017; Wu et al. 2016). This update does not affect our conclusions. Interestingly, from a survey of biomedical researchers, Liao et  al. (2017) concluded that perceptions towards academic misconduct had not significantly changed between 2010 and 2015. To our knowledge, this is the first English language article in which Chinese biomedical research integrity has been investigated empirically. This study also shows that most participants believed that the attention Chinese 13 N. Yi et al. authorities paid to academic misconduct was not sufficient and that the sanctions for academic misconduct were not appropriate or severe enough (Liao et al. 2017). In addition, the academic assessment system was deemed as the most important factor responsible for academic misconduct, which is also in accordance with our results above (Liao et al. 2017). Moreover, whereas our first search had identified 21 studies over a period of about 10  years (2007–May 2016), this update search yielded 8 more studies over less than 2 years. This is indicative of a rising interest in the topic of biomedical research integrity among Chinese scholars, and of more attention to the application of empirical research methods. Limitations Firstly, the studies we reviewed were a mix of qualitative and quantitative research, the data from which could be heterogeneous, thus complicating the pooling of the information. Besides, bearing the goal to give a more comprehensive impression of Chinese studies in mind, we did not exclude any study based on their quality, although we made a quality appraisal of studies. Nevertheless, these studies of lower quality would more or less weaken the strength of this evidence. Furthermore, these 21 studies were conducted in different settings, with different goals and using different investigation tools, as a consequence, there was inevitably information loss in the process of data synthesis. In addition, considering the vast territory and imbalanced distribution of resources and populations in China, the generalizability of our review might be limited. Future Research Directions Our review indicates that biomedical research integrity studies in China have been mainly conducted among postgraduates and nurses. Nevertheless, more attention of future research should also be paid to senior researchers and professors, who play a leading role in scientific research. Besides, in terms of the administration, some surveys in this review were distributed and collected by the administrative staff who were in charge of the department or even the whole institution, in the format of paper–pencil survey, which might also influence the result to some extent. Therefore, to decrease study bias, future research could apply other tools or techniques, such as web-based surveys, the randomized response technique (Kays et  al. 2012; Krumpal 2013). Moreover, considering the fact that the wording used to define misbehavior could affect the findings (Fanelli 2009), the way to present questions is worth considering (Krumpal 2013). 13 Integrity in Biomedical Research: A Systematic Review of Studies… Conclusion During the search process of our review, we found that a large number of research integrity studies has been conducted in China, but empirical evidence is still limited. These 21 empirical studies we identified, using surveys and interviews, all made efforts to explore Chinese biomedical researchers’ awareness, attitudes, perceptions and experiences of research integrity and misconduct. China is one of the countries with the highest output of scientific publications. However, like many other countries and regions, Chinese scientific research is threatened by research misconduct, the existence and harm of which has been recognized by China and international scientific communities. As our review indicates, numerous studies have been conducted, especially in the last decade. The importance of research integrity has been realized by more and more Chinese scholars. So far, the Chinese government and universities have taken measures, such as releasing policies and guideline documents, organizing research integrity training to promote research integrity, however, according to our review, the effects remain to be demonstrated in the long term. Besides, with more and more safeguard measures being taken, it would be crucial to perform more research in order to explore in-depth perceptions of this issue and if possible, analyze the changes. One added value of conducting reseach on research integrity shouldn’t be forgotten as well: by these questions answered or discussed, the awareness of the importance of research integrity and the reflection of this issue among these participants were raised. 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