Prove That T1 and T2 Are Again a Translation

Blazon

Education

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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 well-nigh broadly and simply defined equally research steps to take discoveries "from the bench to the beside and back again." What, precisely, this means in practice has been the subject of continuous, evolving give-and-take.

At the plow of the 21st century, advances in biomedical sciences and particularly genomics led to concerns that the book of new discovery could not exist "translated" into positive impacts on homo health [Reference Balas and Boren1]. These concerns were captured past the Institute of Medicine in a serial of roundtable discussions and workshops, and framed as two discrete "translational blocks" or "gaps" labeled T1 and T2, respectively, and described by Sung et al. starting in 2003 [2–Reference Salber6]. These workshops too provided the conceptual framework for the creation of the Clinical and Translational Scientific discipline Award (CTSA) programme past the National Institutes of Wellness in 2006 [7]. As institutions attempted to put translational inquiry into do, various authors began to alter and elaborate the original definitions. A T3 gap was split from T2 in 2007 [Reference Westfall, Mold and Fagnaneight], with the addition of a T4 and T0 presently post-obit [Reference Khoury9, Reference Schully10].

The evolving number of steps, and changing definition of each step, reflect changing nature and understanding of basic bioscience research and clinical medicine. However, they besides impact the description, design, conduct, and funding of inquiry. Investigators and programme coordinators demand a common vocabulary to frame intent and significance of enquiry. But put, translational researchers need to learn to speak the same language. Although a handful of papers have been instrumental in explicitly modifying the original definition, these alone are insufficient to understand how the concept of translational research is applied [Reference Schweikhart and Dembe11–Reference Trochim13]. Outside of this scattering, source definitions take been explained, adapted to dissimilar contexts (such as epidemiology) [Reference Hiattxiv], and re-explained for yet others (such as medical education) [Reference McGaghie15]. Whatever review which does non take the broader context of how these definitions are applied will fall brusque.

An breezy literature review of this topic by i of the authors (Starren) received significant interest from the CTSA community [Reference Starren16]. To expand on that preliminary work, we undertook a systematic literature review for definitions of the translational enquiry phases and assay to determine how these definitions have evolved over time. In this newspaper, we seek to better understand the differences betwixt definitions of translational inquiry, how they have inverse over time, and which sources or authors were nigh influential in those changes.

Materials and Methods

Search

Research librarians (Shaw, Gutzman) were consulted to construct searches across several literature databases. The search strategy was adult in PubMed MEDLINE and adjusted appropriately to conform to the differing controlled vocabularies and search syntax associated with each subsequent database. Databases searched were PubMed MEDLINE, Scopus, Spider web of Science, and Embase. In addition, a search of Google for non-journal literature, web pages, and presentations was conducted. Performance of search strings was evaluated with retrieval of a small aureate standard corpus identified during transmission review for preliminary work [Reference Starren16]. See Table 1 for database-specific search strings.

Table ane Database-specific search strings

Bibliographic search identified 531 papers. Full text was retrieved for all English-language articles 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 full reviewer attention. The 68 papers were each read by 2 primary reviewers. Of those, 35 papers were disqualified at this phase for various reasons such as a newspaper 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 instance where a newspaper cited a qualifying definition of translational research phases which was non in the corpus, the original defining paper [Reference Westfall, Mold and Fagnan8] was substituted for the citing newspaper. The final corpus comprised of 33 papers [Reference Westfall, Mold and Fagnan8–Reference Schully10, Reference Hiattxiv, Reference McGaghie15, 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 4 sources, deduplication, manual curation, and dual reviewer filtering produced a final corpus of 33 papers.

Review

Each paper in the corpus was read by at least 2 reviewers (Fort, Herr). Reviewers mapped each paper'due south translational phase definitions to a set of inquiry activities defined for this endeavor. In instances of wide disagreement or where consensus over pocket-size differences could not exist reached, a third reader (Starren) was used for arbitration.

Commendation Assay

Citation data were retrieved from Scopus title and PubMed identifier (PMID) of each newspaper in the corpus. Annual global citations for each paper were compiled to indicate relative influence of each newspaper over time. Intracorpus citations (ie, which paper in the corpus cited which other papers in the corpus) were compiled every bit a directed network and manually bundled to indicate bondage of acknowledged influence within the corpus. Nodes stand for papers and directed edges indicate a citation of the target by the source node. Node size and color are proportional to the node's in-caste, in this instance the number of citations of that paper by other papers within the corpus. In a scattering of incidents, recorded citations predate official publication of a newspaper and point prior online availability. In order to analyze chains of influence, date of original availability, be information technology online or in official publication, was used for this assay.

Consensus Analysis

An emerging consensus definition of translational research phases was derived from the label results of the main review. Label definitions were "horizontally summed" across processes to determine nearly common characterization for each process. Results are displayed as fraction of papers in the corpus and the terminal consensus reflects the nigh common label for any research activity regardless of how many papers used the given research process. Early clinical trial phases are labeled equally T2** to reflect the articulate 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. Dissimilarity matrix calculation and agglomerative clustering were performed using daisy and agnes functions of the default clustering package in R. The goal of this clustering is to evaluate chains of influence within the corpus based on definition similarity rather than the citation assay performed above.

Results

Primary Review, Consensus, Clustering, and Total Citations

Our concluding 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 Schully10, Reference Hiattfourteen, Reference McGaghie15, Reference Sung17–Reference Lam44]. Labeling of translational phase definitions and total citations for each paper in the corpus are summarized in Fig. 2. Overall, the papers identified 25 detached research activities. Early research activities (basic inquiry through Phase IV clinical trials) are assumed to be continuous, whereas afterwards categories were ordered based on common labeling and the assumption that translational phases imply continuity (ie, T4 follows T3). In the effigy, papers are horizontally ordered by similarity every bit defined by the agglomerative clustering. In instances where definitions uniquely labeled parts of the enquiry continuum as something other than a translational phase (eg, "Clinical Research" in Sung et al. [Reference Sung17]), these labels accept been preserved. Alongside the table, consensus labeling for each translational phase is presented as a line graph of the fraction of processes assigned to each characterization and results in an emerging consensus categorization.

Fig. 2 Master review results with consensus, clustering, and total citation information. The heart of the figure shows the results of primary definition labeling. Blank cells indicate that the particular paper did non mention that research activity. Target development includes 3 named activities that were categorized the same by all papers (target validation, lead optimization, and atomic number 82 evolution). The pinnacle of the figure shows a dendrogram representing the results of agglomerative clustering on the activity categories, resulting in 3 main definition families and a ready of outliers (the "Other" grouping and Blumberg on the right), and also defines the lodge 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-stage as a fraction of all papers in the corpus. Early on clinical trial phases are labeled as mixed T2**. Although historic bulk labeling is T1, since 2010 the predominant and emerging consensus label for these processes is T2. Citation counts for each paper are included below as a bar graph overlaid with the actual citation count for each paper.

The upshot of agglomerative clustering is visualized equally a dendrogram and defines the order of the presentation of definitions. Here, depth of matched pairs in the dendrogram denotes higher similarity between source definitions, and the branches announce "families" or "lineages" of similar definitions. This process identified 3 major families of definitions with an additional fix 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 traditional inquiry process; the "continuum" model originated by Khoury et al. [Reference Khouryix], where the same phases are relatively continuous beyond all research processes; and the "mixed" model originated by Woolf [Reference Woolf22], which appear to lucifer 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, the originating newspaper of each family has been cited ~10-fold more than any other paper in the family unit, suggesting that each family represents a distinct school of idea with a clear anchoring work.

Citation Frequency

Annual citation counts for each newspaper in the corpus are compiled in Tabular array 2 as a heat map. The 33 papers in the corpus have been cited 2782 times (average 82 citations per paper). 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 involvement and give-and-take 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 four 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. three to visualize influence within the published literature. Nosotros hypothesized that larger and more than strongly colored nodes represent papers with greater acknowledged influence upon the evolving definition of translational research phases. As with the citation rut map, some included papers are poorly cited or uncited. However, at that place is bear witness of bondage of influence within 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 Conwaytwenty] are notable for their influence inside the corpus.

Fig. 3 Directed citation network. Nodes correspond papers in the corpus. Directed edges represent a commendation of the target by the source. Size and color of each node reflects the number of times that newspaper was cited past other papers in the corpus (red, large—loftier citation count; yellowish, small—low citation count; and dark-green, tiny—no commendation count). Meridian of a node corresponds to year of beginning availability either in print or online.

Discussion

The definition of translation phases has shown remarkable evolution in a relatively curt time. Not only have the number of translation phases increased from 2 to five, merely the activities assigned to each stage have also changed. This assay makes equally articulate that the definition of translational research phases remains an surface area of disagreement within the translational research community. In spite of the lack of unanimity regarding translational research phases, a number of consensus patterns exercise emerge.

Emerging Consensus Definition of Translational Enquiry

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

Following early clinical trial phases, T2 is broadly agreed upon to relate to the establishment of effectiveness of an intervention and particularly the establishment of clinical guidelines. T3 is broadly agreed to focus on implementation and broadcasting research. T4, when it appears in definitions, is concerned with outcomes and effectiveness enquiry. Definitions including a T0 stage are relatively rare, but 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. As originally conceived, T1 and T2 translational inquiry bridged the "gaps" between the endpoints of traditional bench and clinical research 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 Fagnanviii]. These definitions persist into later on discussions by Morris et al. [Reference Morris, Wooding and Grant33] and Rubio et al. [Reference Rubio27], and are too supported past heavy ongoing citation of these original papers. However, past the time discussion of the topic exploded in 2008/2009 the consensus definition of translational research had evolved to a "continuum" of translational enquiry.

In the newer definitions, traditional demote and clinical research become part of a process where scientific ideas are translated across a continuous research spectrum and phases in this continuum are labeled by common setting or inquiry methods. Although there is still significant disagreement in labeling of these phases, dating back to their originators (eg, Khoury et al. [Reference Khouryix] vs. Chesla [Reference Chesla19]), continuum definitions of translational enquiry (n=13) are more prevalent than the original gap definitions (n=8).

Of farther interest is that the departure betwixt these ii 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 construction where they exclude clinical enquiry from all labeling (particularly notable in the transition from Sung et al. [Reference Sung17] to Woolf [Reference Woolf22]), but ameliorate resemble the continuum definitions in terms of later translational research phases.

Evolution of Translational Research Definitions

The development from gap to continuum definitions of translational enquiry represents the unmarried most obvious stride in the discussion of this topic. Beyond that commonality, however, there are detectable points of consensus regarding definitions of private translational research phases discussed above. Also notable is that while additional 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 on equally 2007 [Reference Khoury9], roughly concurrent with the ameliorate-cited papers by Woolf [Reference Woolf22] and Westfall et al. [Reference Westfall, Mold and Fagnaneight], and predates the explosion in discussion on this topic around 2008/2009.

The improver of college translational research phases appears to serve 2 purposes. Points where agreement is muddy, such every bit the range of outcome and effectiveness inquiry 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 apparently solved by assigning these processes to a 4th translational phase. This is in contrast to the addition of step (T0) which adds a fundamentally new idea to the enquiry continuum. Before the advent of the T0 translational research phase, there is very little credible discussion of closing the inquiry wheel back to T1.

Finally, Phase IV clinical trials and comparative effectiveness inquiry, the processes at which research moves into establishing real-earth effectiveness of interventions, represent a point of virtually maximum disagreement or flux within our results. Well-nigh definitions before 2011 put Phase IV clinical trials as part of T2 or T3 research where subsequently information technology is more likely to appear as T4. We hypothesize that this outcome may be an artifact of the Patient-Centered Outcomes Research Institute (PCORI) publicizing comparative effectiveness inquiry both as an important research topic and as subtly singled-out concept than what it had been before [Reference Patel and McDonough46]. Notwithstanding, at that place was not enough momentum in these changes for us to deviate from the historic majority label on these processes at this time.

Citation Patterns and Influence

The originating paper in each definition family has been cited ~x-fold more than than whatsoever other paper, suggesting an acknowledged lineage and anchor within each family. This lends acceptance to the idea that the mixed model family is as defined every bit the gap and continuum models. What also stands out is that 2 of the 5 about-cited papers (Westfall et al. [Reference Westfall, Mold and Fagnaneight] and Dougherty and Conway [Reference Dougherty and Conway20]) have no respective families. As seen in the citation network and in total citations, these papers have an acknowledged historical influence on the give-and-take around translational enquiry, but the influence never extended to propagating their specific conceptual definitions.

The results pertaining to citations, influence, and similarity likewise lend themselves to minor commentary on the publication and dissemination of new ideas. The paper by Sung et al. [Reference Sung17], a report on a series of workshops held by the then Establish of Medicine, is widely considered the originating manuscript on this topic. However, it is the later paper past Woolf [Reference Woolf22] in the same periodical which is cited most ofttimes even though Woolf repeats most the exact same definition. The reason for this difference is not obvious. It may be that Sung'due south paper was overlooked as a workshop report. Perchance Woolf's newspaper appeared at a more opportune time. Finally, Woolf's newspaper may have been more prominent in electronic searches because the title independent the words "translational research."

Also notable is that 4 of the peak 5 near-cited publications appear in a unmarried periodical—the Periodical of the American Medical Clan. The exception, Khoury et al. [Reference Khoury9], also serves every bit 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 every bit the subsequently consensus on translational research. Notwithstanding this first Khoury paper shows little prove of direct influence within our corpus and 4 out of 5 of the citing papers feature Khoury every bit first or senior author [Reference Schully10, Reference Khoury, Gwinn and Ioannidis26, Reference Khoury32, Reference Lam44]. It is not for iv years (2011), and appearance of these boosted papers later, that we observe adoption of these ideas. Again, we can only speculate whether the original Khoury newspaper found publication in a less visible journal or was merely alee of its time.

Limitations

This piece of work has 4 primary limitations. First, every bit with whatever systematic review, our analysis was express to those papers we retrieved and, therefore, relied entirely on the strength of our search strategy. With that in listen, we designed our search strategy in consultation with professional enquiry librarians and evaluated it using a gold standard fix which was manually identified during preliminary work [Reference Starren16]. The 2d limitation involves our research procedure categories and labeling. Categories were derived through an iterative approach where enquiry processes were bathetic from definitions in our final corpus. A limitation of this is that 2 papers may use slightly different words to describe the same process and synonymy is based on human judgment. To minimize variation, nosotros employed two independent reviewers with a third interim as an adjudicator to facilitate consensus categorization. Third, our conclusions about citation frequency and dissemination of ideas practice not have into account citation context. We 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 uncomplicated majority labeling rather than a formal consensus development procedure involving active participation of the diverse authors. Thus, it is possible that the more than mutual, rather than the more persuasive, consignment for a particular category may have been chosen. Such a procedure was outside the scope of this investigation, though exceptions such as the T1/T2 overlap in early on clinical research phases have been noted. Nosotros promise that this analysis could provide a starting point for such an practice.

Conclusions

We used systematic review and analysis to identify emerging consensus between definitions of translational enquiry phases. T1 involves processes that bring ideas from bones research through early on 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 inquiry such as genome-wide association studies which wrap back around to bones research. Within the field of translational research, nosotros have also been able to draw evolution of definitions over time and families of definitions based on similarity. In addition, nosotros accept demonstrated that while citations are an of import tool to describe the influence of whatever particular newspaper, acknowledgment of this influence does not mean broadcasting of the ideas of the paper. Finally, while our techniques have been useful within the field of translational research, nosotros do promise they prove useful in similar assay of other complex topics.

Acknowledgments

Inquiry reported in this publication was supported, in function, past the National Institutes of Health'south National Center for Advancing Translational Sciences, grant number UL1TR001422 (D.G.F., J.B.South.), and the Electronic Medical Records and Genomics (eMERGE) Consortium, grant number U01HG008673-01 (T.Grand.H.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Wellness.

Author Contributions

D.M.F. is the primary author of the text, congenital on preliminary work past J.B.S. D.G.F. and T.Yard.H. were primary reviewers of papers, adjudicated by J.B.Southward. when necessary. P.L.S. and M.E.G. 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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