Prove That T1 and T2 Are Again a Translation

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Introduction

Translational research as a concept has been widely used and practical in scientific literature for more than a decade. Information technology is most broadly and but defined as research steps to accept discoveries "from the bench to the beside and back over again." What, precisely, this ways in practice has been the discipline of continuous, evolving discussion.

At the turn of the 21st century, advances in biomedical sciences and particularly genomics led to concerns that the volume of new discovery could not be "translated" into positive impacts on man wellness [Reference Balas and Boren1]. These concerns were captured by the Institute of Medicine in a series of roundtable discussions and workshops, and framed every bit two discrete "translational blocks" or "gaps" labeled T1 and T2, respectively, and described by Sung et al. starting in 2003 [2–Reference Salberhalf-dozen]. These workshops as well provided the conceptual framework for the creation of the Clinical and Translational Science Honor (CTSA) program by the National Institutes of Health in 2006 [7]. As institutions attempted to put translational research into practice, diverse authors began to alter and elaborate the original definitions. A T3 gap was split from T2 in 2007 [Reference Westfall, Mold and Fagnan8], with the add-on of a T4 and T0 soon following [Reference Khoury9, Reference Schully10].

The evolving number of steps, and changing definition of each pace, reverberate irresolute nature and understanding of basic bioscience research and clinical medicine. However, they also impact the description, design, bear, and funding of inquiry. Investigators and programme coordinators need a mutual vocabulary to frame intent and significance of research. Simply put, translational researchers need to learn to speak the aforementioned linguistic communication. Although a scattering of papers take been instrumental in explicitly modifying the original definition, these alone are insufficient to understand how the concept of translational inquiry is applied [Reference Schweikhart and Dembe11–Reference Trochimxiii]. Outside of this handful, source definitions take been explained, adapted to different contexts (such as epidemiology) [Reference Hiatt14], and re-explained for yet others (such as medical education) [Reference McGaghie15]. Whatever review which does not take the broader context of how these definitions are practical will autumn brusque.

An informal literature review of this topic past one of the authors (Starren) received pregnant interest from the CTSA community [Reference Starren16]. To aggrandize on that preliminary work, nosotros undertook a systematic literature review for definitions of the translational inquiry phases and analysis to make up one's mind how these definitions have evolved over time. In this paper, we seek to better sympathise the differences between definitions of translational research, how they take changed over fourth dimension, and which sources or authors were most influential in those changes.

Materials and Methods

Search

Research librarians (Shaw, Gutzman) were consulted to construct searches beyond several literature databases. The search strategy was developed in PubMed MEDLINE and adapted accordingly to arrange to the differing controlled vocabularies and search syntax associated with each subsequent database. Databases searched were PubMed MEDLINE, Scopus, Spider web of Scientific discipline, and Embase. In addition, a search of Google for not-periodical literature, web pages, and presentations was conducted. Performance of search strings was evaluated with retrieval of a pocket-sized golden standard corpus identified during transmission review for preliminary piece of work [Reference Starren16]. See Table 1 for database-specific search strings.

Table one Database-specific search strings

Bibliographic search identified 531 papers. Full text was retrieved for all English-language manufactures either digitally or through interlibrary loan. All initial papers were manually curated to select those which discussed and defined translational research phases, resulting in 68 papers for total reviewer attention. The 68 papers were each read by two primary reviewers. Of those, 35 papers were disqualified at this stage for various reasons such every bit a paper being a review itself rather than a novel definition, or because it only replicated a pre-existing definition (eg, with a referenced figure). In the case where a paper cited a qualifying definition of translational research phases which was not in the corpus, the original defining newspaper [Reference Westfall, Mold and Fagnaneight] was substituted for the citing paper. The concluding corpus comprised of 33 papers [Reference Westfall, Mold and Fagnan8–Reference Schully10, Reference Hiatt14, Reference McGaghiefifteen, Reference Sung17–Reference Lam44]. See Fig. 1 for a menses chart summarizing search, filtering, and review.

Fig. 1 Systematic search and filtering flow chart. Bibliographic search in four sources, deduplication, transmission curation, and dual reviewer filtering produced a final corpus of 33 papers.

Review

Each newspaper in the corpus was read past at least 2 reviewers (Fort, Herr). Reviewers mapped each paper's translational stage definitions to a set of research activities defined for this effort. In instances of broad disagreement or where consensus over modest differences could not be reached, a third reader (Starren) was used for arbitration.

Citation Assay

Commendation information were retrieved from Scopus title and PubMed identifier (PMID) of each paper in the corpus. Annual global citations for each paper were compiled to betoken relative influence of each newspaper over fourth dimension. Intracorpus citations (ie, which paper in the corpus cited which other papers in the corpus) were compiled as a directed network and manually arranged to betoken bondage of best-selling influence inside the corpus. Nodes stand for papers and directed edges bespeak a citation of the target past the source node. Node size and color are proportional to the node'south in-degree, in this case the number of citations of that paper by other papers inside the corpus. In a handful of incidents, recorded citations predate official publication of a paper and indicate prior online availability. In social club to analyze chains of influence, date of original availability, exist it online or in official publication, was used for this analysis.

Consensus Analysis

An emerging consensus definition of translational research phases was derived from the label results of the primary review. Label definitions were "horizontally summed" across processes to determine almost common label for each process. Results are displayed as fraction of papers in the corpus and the last consensus reflects the most common characterization for any inquiry action regardless of how many papers used the given research procedure. Early clinical trial phases are labeled as T2** to reverberate the clear shift in labeling post-obit 2010 despite the celebrated majority of T1 labels.

Similarity Analysis

Labeled processes for each reviewed paper were compiled as vectors of nominal variables. Contrast matrix adding and agglomerative clustering were performed using daisy and agnes functions of the default clustering parcel in R. The goal of this clustering is to evaluate chains of influence inside the corpus based on definition similarity rather than the citation analysis performed higher up.

Results

Primary Review, Consensus, Clustering, and Total Citations

Our final corpus was comprised of 33 papers, filtered from 68 strong candidates out of an initial returned puddle of 531 papers [Reference Westfall, Mold and Fagnan8–Reference Schullyx, Reference Hiatt14, Reference McGaghie15, Reference Sung17–Reference Lam44]. Labeling of translational stage definitions and total citations for each paper in the corpus are summarized in Fig. ii. Overall, the papers identified 25 detached research activities. Early enquiry activities (basic research through Phase IV clinical trials) are causeless to be continuous, whereas after categories were ordered based on common labeling and the supposition that translational phases imply continuity (ie, T4 follows T3). In the effigy, papers are horizontally ordered by similarity as divers by the agglomerative clustering. In instances where definitions uniquely labeled parts of the research continuum as something other than a translational phase (eg, "Clinical Inquiry" in Sung et al. [Reference Sung17]), these labels take been preserved. Alongside the table, consensus labeling for each translational stage is presented equally a line graph of the fraction of processes assigned to each label and results in an emerging consensus categorization.

Fig. 2 Primary review results with consensus, clustering, and total citation information. The eye of the figure shows the results of primary definition labeling. Bare cells indicate that the particular paper did not mention that research activity. Target development includes 3 named activities that were categorized the same by all papers (target validation, pb optimization, and lead evolution). The top of the figure shows a dendrogram representing the results of agglomerative clustering on the activeness categories, resulting in 3 master definition families and a set of outliers (the "Other" group and Blumberg on the right), and as well defines the society of papers for presentation. The far right side of the effigy includes a consensus categorization and graph showing the frequency of assignment of each process to each T-phase as a fraction of all papers in the corpus. Early clinical trial phases are labeled as mixed T2**. Although historic bulk labeling is T1, since 2010 the predominant and emerging consensus characterization for these processes is T2. Citation counts for each paper are included below equally a bar graph overlaid with the actual citation count for each paper.

The event of agglomerative clustering is visualized as a dendrogram and defines the order of the presentation of definitions. Hither, depth of matched pairs in the dendrogram denotes college similarity between source definitions, and the branches denote "families" or "lineages" of similar definitions. This process identified 3 major families of definitions with an additional set of outliers for discussion. These families are the "gap" model originated by Sung et al. [Reference Sung17], where translational research is conceptualized as bridging gaps in a more than traditional inquiry process; the "continuum" model originated by Khoury et al. [Reference Khourynine], where the same phases are relatively continuous across all enquiry processes; and the "mixed" model originated by Woolf [Reference Woolf22], which announced to match the gap definitions in early structure and the continuum definitions in the inclusion of later phases. With the exception of Shekhar et al. [Reference Shekhar35], the mixed definitions are notable for non mentioning clinical trial phases at all. Every bit will be expanded on later on, the originating paper of each family has been cited ~x-fold more any other paper in the family unit, suggesting that each family represents a distinct school of thought with a clear anchoring piece of work.

Citation Frequency

Almanac commendation counts for each newspaper in the corpus are compiled in Table 2 every bit a heat map. The 33 papers in the corpus have been cited 2782 times (average 82 citations per newspaper). Sung et al. [Reference Sung17] and Woolf [Reference Woolf22] are the most-cited papers, despite Sung et al. (2003) predating Woolf (2008) by 5 years. These citation data strongly suggest an explosion of interest and word on the topic of translational research gaps in 2008 and 2009, with full annual citations of the corpus doubling each of these years. Overall, 67% of the citations of the corpus, including iv of the 5 most-cited papers, were published in the Journal of the American Medical Association.

Table 2 Annual citation frequency and journal summary

Directed Citation Network

Citations within the corpus were converted into the directed network in Fig. iii to visualize influence within the published literature. We hypothesized that larger and more strongly colored nodes stand for papers with greater acknowledged influence upon the evolving definition of translational research phases. As with the citation heat map, some included papers are poorly cited or uncited. However, there is evidence of chains of influence inside the corpus. Sung et al. [Reference Sung17], Westfall et al. [Reference Westfall, Mold and Fagnan8], Woolf [Reference Woolf22], and Dougherty and Conway [Reference Dougherty and Conway20] are notable for their influence within the corpus.

Fig. 3 Directed commendation network. Nodes represent papers in the corpus. Directed edges stand for a commendation of the target by the source. Size and color of each node reflects the number of times that paper was cited past other papers in the corpus (red, big—high citation count; yellow, small—low citation count; and light-green, tiny—no citation count). Height of a node corresponds to year of commencement availability either in impress or online.

Discussion

The definition of translation phases has shown remarkable evolution in a relatively brusk time. Not only take the number of translation phases increased from 2 to 5, only the activities assigned to each phase have also changed. This assay makes every bit clear that the definition of translational research phases remains an area of disagreement within the translational enquiry community. In spite of the lack of unanimity regarding translational inquiry phases, a number of consensus patterns exercise emerge.

Emerging Consensus Definition of Translational Research

The definition of T1 translational research demonstrates the highest degree of consensus, with 75% of papers agreeing that T1 research comprises processes from basic research to initial testing in humans. Approximately half of these agree that T1 continues through early clinical trial phases, whereas the remainder put fifty-fifty these early clinical trial phases in the realm of T2. Most definitions put the end of T1 at the establishment of clinical efficacy of an intervention, or the Phase Ii clinical trial. While the T1 characterization is historically dominant, T2 has emerged as the most common label for these enquiry processes later 2010. Therefore nosotros take labeled early stage clinical trials as T2** in our emerging consensus definition.

Following early clinical trial phases, T2 is broadly agreed upon to relate to the institution of effectiveness of an intervention and particularly the institution of clinical guidelines. T3 is broadly agreed to focus on implementation and dissemination inquiry. T4, when it appears in definitions, is concerned with outcomes and effectiveness inquiry. Definitions including a T0 phase are relatively rare, simply define it as steps which close the research cycle back to T1, such as genome-wide association studies. Although a few CTSA institutions have included a T5 phase in their descriptions [Reference Kiefe45], we were unable to locate a mention of T5 in the peer-reviewed literature using our search strategy. Every bit originally conceived, T1 and T2 translational inquiry bridged the "gaps" between the endpoints of traditional bench and clinical enquiry and this is evident in the early papers by Sung et al. [Reference Sung17], Hait [Reference Hait18], and Westfall et al. [Reference Westfall, Mold and Fagnan8]. These definitions persist into later on discussions by Morris et al. [Reference Morris, Wooding and Grant33] and Rubio et al. [Reference Rubio27], and are besides supported by heavy ongoing citation of these original papers. However, by the time discussion of the topic exploded in 2008/2009 the consensus definition of translational enquiry had evolved to a "continuum" of translational research.

In the newer definitions, traditional bench and clinical research get part of a process where scientific ideas are translated beyond a continuous research spectrum and phases in this continuum are labeled by common setting or research methods. Although there is still significant disagreement in labeling of these phases, dating back to their originators (eg, Khoury et al. [Reference Khoury9] vs. Chesla [Reference Cheslanineteen]), continuum definitions of translational research (northward=13) are more prevalent than the original gap definitions (northward=8).

Of farther involvement is that the departure between these 2 approaches is readily visible in an agglomerative clustering of definitions. The aforementioned clustering also reveals an almost hybrid group of definitions, labeled as the mixed model family. These are interesting for matching the gap definitions in early structure where they exclude clinical research from all labeling (specially notable in the transition from Sung et al. [Reference Sung17] to Woolf [Reference Woolf22]), but better resemble the continuum definitions in terms of later translational research phases.

Development of Translational Research Definitions

The evolution from gap to continuum definitions of translational research represents the single virtually obvious step in the give-and-take of this topic. Beyond that commonality, however, there are detectable points of consensus regarding definitions of individual translational research phases discussed above. Also notable is that while boosted translational phases (T3, T4, T0) are widely understood to have been added over time, a 4-phase continuous definition from Khoury et al. appears as early equally 2007 [Reference Khoury9], roughly concurrent with the better-cited papers past Woolf [Reference Woolf22] and Westfall et al. [Reference Westfall, Mold and Fagnaneight], and predates the explosion in discussion on this topic effectually 2008/2009.

The addition of college translational research phases appears to serve 2 purposes. Points where understanding is dirty, such as the range of outcome and effectiveness research processes, demonstrate where the addition of an extra phase (T4) has added clarity. Early T2 and T3 definitions are evenly reported for these processes, demonstrating a lack of clarity which was plain solved past assigning these processes to a fourth translational stage. This is in contrast to the addition of step (T0) which adds a fundamentally new idea to the enquiry continuum. Before the appearance of the T0 translational research phase, in that location is very little apparent discussion of closing the inquiry cycle back to T1.

Finally, Phase Four clinical trials and comparative effectiveness enquiry, the processes at which research moves into establishing real-world effectiveness of interventions, correspond a betoken of almost maximum disagreement or flux within our results. Most definitions before 2011 put Phase IV clinical trials as part of T2 or T3 research where afterwards it is more likely to appear as T4. We hypothesize that this effect may be an antiquity of the Patient-Centered Outcomes Inquiry Institute (PCORI) publicizing comparative effectiveness enquiry both every bit an important research topic and as subtly distinct concept than what information technology had been before [Reference Patel and McDonough46]. Withal, there was not enough momentum in these changes for united states to deviate from the celebrated majority label on these processes at this time.

Citation Patterns and Influence

The originating paper in each definition family unit has been cited ~10-fold more than than any other newspaper, suggesting an best-selling lineage and anchor within each family. This lends credence to the idea that the mixed model family unit is as defined as the gap and continuum models. What also stands out is that 2 of the five nigh-cited papers (Westfall et al. [Reference Westfall, Mold and Fagnaneight] and Dougherty and Conway [Reference Dougherty and Conwaytwenty]) have no corresponding families. As seen in the citation network and in full citations, these papers take an acknowledged historical influence on the word around translational inquiry, but the influence never extended to propagating their specific conceptual definitions.

The results pertaining to citations, influence, and similarity also lend themselves to pocket-size commentary on the publication and dissemination of new ideas. The paper past Sung et al. [Reference Sung17], a report on a series of workshops held by the so Establish of Medicine, is widely considered the originating manuscript on this topic. However, it is the after paper by Woolf [Reference Woolf22] in the same journal which is cited well-nigh frequently even though Woolf repeats nearly the exact same definition. The reason for this difference is not obvious. It may be that Sung'southward paper was overlooked as a workshop study. Perhaps Woolf'due south newspaper appeared at a more than opportune fourth dimension. Finally, Woolf'southward paper may have been more than prominent in electronic searches because the championship contained the words "translational enquiry."

Too notable is that 4 of the top 5 most-cited publications announced in a single journal—the Periodical of the American Medical Association. The exception, Khoury et al. [Reference Khoury9], also serves as something of a cautionary tale. In 2007, predating both Woolf [Reference Woolf22] and Westfall et al. [Reference Westfall, Mold and Fagnan8], Khoury presented a 4-stage translational research continuum which highly predicts what would emerge as the later consensus on translational research. Yet this showtime Khoury paper shows little testify of straight influence within our corpus and iv out of 5 of the citing papers feature Khoury equally first or senior author [Reference Schully10, Reference Khoury, Gwinn and Ioannidis26, Reference Khoury32, Reference Lam44]. Information technology is not for 4 years (2011), and advent of these additional papers later, that we observe adoption of these ideas. Again, we tin merely speculate whether the original Khoury paper constitute publication in a less visible journal or was only ahead of its time.

Limitations

This work has 4 primary limitations. First, every bit with any systematic review, our analysis was limited to those papers nosotros retrieved and, therefore, relied entirely on the strength of our search strategy. With that in mind, we designed our search strategy in consultation with professional enquiry librarians and evaluated information technology using a gold standard set which was manually identified during preliminary work [Reference Starrensixteen]. The 2nd limitation involves our research process categories and labeling. Categories were derived through an iterative approach where inquiry processes were abstracted from definitions in our final corpus. A limitation of this is that two papers may use slightly dissimilar words to describe the aforementioned process and synonymy is based on human judgment. To minimize variation, we employed two independent reviewers with a third acting as an adjudicator to facilitate consensus categorization. 3rd, our conclusions well-nigh commendation frequency and dissemination of ideas practise not take into account commendation context. Nosotros contend that the intersection of agglomerative clustering and commendation frequency are sufficient for our conclusions, but our results are limited by not examining citation context. Finally, our consensus assignments of processes to categories represent, primarily, a voting based on simple majority labeling rather than a formal consensus development process involving active participation of the various authors. Thus, information technology is possible that the more common, rather than the more than persuasive, assignment for a detail category may have been chosen. Such a procedure was exterior the telescopic of this investigation, though exceptions such as the T1/T2 overlap in early clinical inquiry phases take been noted. We promise that this analysis could provide a starting point for such an exercise.

Conclusions

We used systematic review and analysis to identify emerging consensus between definitions of translational research phases. T1 involves processes that bring ideas from basic research through early testing in humans. T2 involves the establishment of effectiveness in humans and clinical guidelines. T3 primarily focuses on implementation and dissemination research while T4 focuses on outcomes and effectiveness in populations. T0 involves research such every bit genome-wide association studies which wrap back effectually to basic inquiry. Within the field of translational research, nosotros have also been able to describe evolution of definitions over time and families of definitions based on similarity. In addition, nosotros have demonstrated that while citations are an important tool to depict the influence of whatever particular newspaper, acknowledgment of this influence does not mean dissemination of the ideas of the paper. Finally, while our techniques accept been useful within the field of translational research, nosotros do hope they testify useful in similar analysis of other complex topics.

Acknowledgments

Inquiry reported in this publication was supported, in part, by the National Institutes of Wellness's National Centre for Advancing Translational Sciences, grant number UL1TR001422 (D.Chiliad.F., J.B.S.), and the Electronic Medical Records and Genomics (emerge) Consortium, grant number U01HG008673-01 (T.M.H.). The content is solely the responsibility of the authors and does not necessarily stand for the official views of the National Institutes of Wellness.

Writer Contributions

D.G.F. is the chief author of the text, built on preliminary work past J.B.Due south. D.G.F. and T.Yard.H. were principal reviewers of papers, adjudicated past J.B.S. when necessary. P.L.S. and K.Eastward.K. are research librarians responsible for systematic search strategy and retrieved and compiled all citation information.

Declaration of Interest

The authors report that they have no conflicts of interest.

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