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Adult: Education| Volume 9, P162-175, March 2022

Quantitative goals for research output and scholarly impact to enhance basic science R01 grant renewal for cardiothoracic surgeons

Open AccessPublished:February 15, 2022DOI:https://doi.org/10.1016/j.xjon.2021.10.063

      Abstract

      Objectives

      Cardiothoracic (CT) surgeons with National Institutes of Health (NIH) R01 funding face a highly competitive renewal process. The factors that contribute to successful grant renewal for CT surgeons remain poorly defined. We hypothesized that renewed basic science grants are associated with high research output and scholarly impact during the preceding award cycle.

      Methods

      Using a database of academic CT surgeons (n = 992) at accredited training institutions in 2018, we identified basic science R01 grants awarded to CT surgeon principal investigators since 1985. Data for each award were obtained from publicly available online sources. Scholarly impact was evaluated using the NIH-validated relative citation ratio (RCR), defined as an article's citation rate divided by that of R01-funded publications in the same field. Continuous data are presented as medians and analyzed using the Mann–Whitney test.

      Results

      We identified 102 basic science R01 award cycles, including 33 that were renewed (32.4%). Renewed and nonrenewed awards had a similar start year and funding period. Principal investigators of renewed versus nonrenewed awards were similar in surgical subspecialty, research training, attending experience, academic rank, and previous NIH funding. Renewed awards produced more publications per year over the funding cycle (3.4 vs 1.5; P = .0010) and exhibited a greater median RCR during the funding cycle (0.84 vs 0.66; P = .0183).

      Conclusions

      CT surgery basic science R01 grants are associated with high research output and scholarly impact. At the 50th percentile among renewed grants, CT surgeons published 3.4 funded manuscripts per year with a median RCR of 0.84 during the previous award cycle.

      Graphical abstract

      Key Words

      Abbreviations and Acronyms:

      AATS (American Association for Thoracic Surgery), CT (cardiothoracic), NHLBI (National Heart, Lung, and Blood Institute), NIH (National Institutes of Health), PI (principal investigator), RCR (relative citation ratio), RePORTER (Research Portfolio Online Reporting Tools Expenditures and Results)
      Figure thumbnail fx2
      Research output and impact for basic science R01s that were renewed versus not renewed.
      At the 50th percentile among renewed basic science R01 grants, surgeons published 3.4 funded articles per year with a median relative citation ratio of 0.84 during the previous award cycle.
      Cardiothoracic surgeons pursuing basic science research face a highly competitive extramural funding environment. Aside from supporting surgeons in the grant acquisition process, it is also important to optimize grant renewal. Herein, we quantify the research output and scholarly impact of renewed versus nonrenewed basic science R01 grants to help guide surgeons in the renewal process.
      See Commentaries on pages 176 and 178.
      Clinical advances in cardiothoracic (CT) surgery are driven by research and innovation, but concerns have been raised regarding the attrition of CT surgeon-scientists,
      • Ikonomidis J.S.
      • Menasché P.
      • Kreisel D.
      • Sellke F.W.
      • Woo Y.J.
      • Colson Y.L.
      Attrition of the cardiothoracic surgeon-scientist: definition of the problem and remedial strategies.
      due in part to an increasingly difficult extramural funding environment.
      • Narahari A.K.
      • Mehaffey J.H.
      • Hawkins R.B.
      • Charles E.J.
      • Baderdinni P.K.
      • Chandrabhatla A.S.
      • et al.
      Surgeon scientists are disproportionately affected by declining NIH funding rates.
      Amidst a 16.5% decrease in National Institutes of Health (NIH) grants awarded to surgeons between 2003 and 2013,
      • Hu Y.
      • Edwards B.L.
      • Brooks K.D.
      • Newhook T.E.
      • Slingluff C.L.
      Recent trends in National Institutes of Health funding for surgery: 2003 to 2013.
      per capita NIH awards for CT surgeons in 2008 were more than 3 times less than that for other medical faculty.
      • Ratcliffe M.B.
      • Howard C.
      • Mann M.
      • del Nido P.
      National Institutes of Health funding for cardiothoracic surgical research.
      Furthermore, NIH R01 grants historically account for most research funding for cardiac surgeons, but the number of active cardiac surgery R01 grants has plateaued over the past 2 decades.
      • Narahari A.K.
      • Cook I.O.
      • Mehaffey J.H.
      • Chandrabhatla A.S.
      • Hawkins R.B.
      • Tyerman Z.
      • et al.
      Comprehensive National Institutes of Health funding analysis of academic cardiac surgeons.
      In response, considerable attention has been focused on supporting CT surgeon-scientists endeavoring to achieve the extramural funding needed to maintain an independent research enterprise, for which the R01 grant remains the standard. To this end, the importance of research training,
      • Wang H.
      • Bajaj S.S.
      • Williams K.M.
      • Heiler J.C.
      • Pickering J.M.
      • Manjunatha K.
      • et al.
      Early engagement in cardiothoracic surgery research enhances future academic productivity.
      ,
      • Narahari A.K.
      • Charles E.J.
      • Mehaffey J.H.
      • Hawkins R.B.
      • Schubert S.A.
      • Tribble C.G.
      • et al.
      Cardiothoracic surgery training grants provide protected research time vital to the development of academic surgeons.
      mentored career development grants,
      • Narahari A.K.
      • Mehaffey J.H.
      • Hawkins R.B.
      • Baderdinni P.K.
      • Chandrabhatla A.S.
      • Tribble C.G.
      • et al.
      Cardiothoracic and vascular surgeons achieve high rates of K award conversion into R01 funding.
      departmental support and start-up funding,
      • Ikonomidis J.S.
      • Menasché P.
      • Kreisel D.
      • Sellke F.W.
      • Woo Y.J.
      • Colson Y.L.
      Attrition of the cardiothoracic surgeon-scientist: definition of the problem and remedial strategies.
      and academic development programs cannot be understated.
      In addition to supporting surgeon-scientists on grant acquisition, it is also essential to optimize strategies for grant renewal to sustain funding in the long term. Indeed, the number of competitive renewal awards issued by the NIH to all surgeons declined by 60% between 2003 and 2013, representing a greater decrease than that for other specialties including medicine, pathology, pediatrics, and psychiatry.
      • Hu Y.
      • Edwards B.L.
      • Brooks K.D.
      • Newhook T.E.
      • Slingluff C.L.
      Recent trends in National Institutes of Health funding for surgery: 2003 to 2013.
      Furthermore, since 1980, only 17.3% of R01 grants awarded to thoracic surgeons were renewed for a subsequent cycle.
      • Narahari A.K.
      • Mehaffey J.H.
      • Chandrabhatla A.S.
      • Hawkins R.B.
      • Charles E.J.
      • Roeser M.E.
      • et al.
      Longitudinal analysis of National Institutes of Health funding for academic thoracic surgeons.
      Successful grant renewal plays an important role in long-term funding longevity, but the factors affecting R01 renewal for CT surgeons have not been explored in detail. Herein, we quantify the research output and scholarly impact of renewed versus nonrenewed CT surgery basic science R01 grants to help guide surgeons in the renewal process. We hypothesized that renewed grants are associated with high research output and scholarly impact during the preceding award cycle.

      Methods

      In this study, we used a biographical database of 992 academic CT surgeons who were on faculty at the university hospital of the 77 accredited United States CT surgery training programs in 2018, as previously described.
      • Wang H.
      • Bajaj S.S.
      • Williams K.M.
      • Heiler J.C.
      • Pickering J.M.
      • Manjunatha K.
      • et al.
      Early engagement in cardiothoracic surgery research enhances future academic productivity.
      ,
      • Bajaj S.S.
      • Wang H.
      • Williams K.M.
      • Pickering J.M.
      • Heiler J.C.
      • Manjunatha K.
      • et al.
      New attending surgeons hired by their training institution exhibit greater research productivity.
      • Wang H.
      • Bajaj S.S.
      • Williams K.M.
      • Pickering J.M.
      • Heiler J.C.
      • Manjunatha K.
      • et al.
      Impact of advanced clinical fellowship training on future research productivity and career advancement in adult cardiac surgery.
      • Bajaj S.S.
      • Wang H.
      • Williams K.M.
      • Pickering J.M.
      • Heiler J.C.
      • Manjunatha K.
      • et al.
      National Institutes of Health R01 grant funding is associated with enhanced research productivity and career advancement among academic cardiothoracic surgeons.
      • Bajaj S.S.
      • Wang H.
      • Williams K.M.
      • Pickering J.M.
      • Heiler J.C.
      • Manjunatha K.
      • et al.
      Career research productivity correlates with medical school ranking among cardiothoracic surgeons.
      Emeritus professors, nonsurgical faculty (eg, PhD researchers), and surgeons working at affiliated satellite hospitals were excluded from our database. Data regarding each surgeon's training and professional career were obtained from department webpages, CTSNet (https://www.ctsnet.org), LinkedIn (https://www.linkedin.com), and other online sources. Each surgeon's career publication record was obtained using Scopus (https://www.scopus.com). The NIH funding rank of each surgeon's institution was determined using NIH Research Portfolio Online Reporting Tools (https://report.nih.gov).
      We defined “grant” as the overarching R01 funding mechanism, encompassing 1 or more funding cycles, whereas “award” or “award cycle” refers to the individual funding cycles that comprise a grant. To identify R01 grants awarded to the CT surgeons in our database, each surgeon's NIH funding history was obtained using Grantome (https://grantome.com) and NIH Research Portfolio Online Reporting Tools Expenditures and Results (RePORTER; https://reporter.nih.gov). All basic science R01 grants awarded since 1985 (ie, the earliest year included in NIH RePORTER), in which a CT surgeon in our database served as principal investigator (PI) for the entire duration of the funding cycle, were included for analysis. Each grant was assessed for potential renewal through the year 2019. Grants with award cycles that had not been completed by the year 2019 or that had been terminated early (and therefore were not subject to potential renewal at the time of analysis) were excluded. Funding data and articles published during each award cycle were obtained from NIH RePORTER.
      Scholarly impact was assessed using the relative citation ratio (RCR), a field-normalized metric developed and validated by the NIH.
      • Hutchins B.I.
      • Yuan X.
      • Anderson J.M.
      • Santangelo G.M.
      Relative citation ratio (RCR): a new metric that uses citation rates to measure influence at the article level.
      Briefly, the RCR represents the citation rate of an article divided by the citation rate of R01-funded articles in the same field. Thus, an article with an RCR of 1.00 has an equal number of citations per year as other R01-funded papers in the same field, whereas an article with an RCR of 2.00 has twice the number of citations per year, reflecting greater impact. The RCR of each individual publication was calculated using the NIH iCite database (https://icite.od.nih.gov), and the median and maximum RCR among the publications linked to each R01 award cycle was determined.
      All data used in this study were obtained from publicly available online sources. Statistical analyses were performed using GraphPad Prism version 9.0.0 (Graph Pad Software). The D'Agostino–Pearson test was used to assess normality. Continuous data were non-normally distributed and presented as median with interquartile range and analyzed using the Mann–Whitney test. Categorical data are presented as counts with percentages and analyzed using Fisher exact test, or the χ2 test when more than 2 categories were involved.

      Results

      R01 Award Characteristics

      A total of 76 basic science R01 grants were identified (Table E1), encompassing 102 award cycles, of which 33 (32.4%) were subsequently renewed and 69 (67.6%) were not renewed. Among the 992 CT surgeons in our database, 49 (4.9%) had completed a basic science R01 funding cycle as PI, among whom 20 (40.8%) had renewed a basic science R01 grant.
      As presented in Table 1, the characteristics of R01 award cycles that were renewed were similar to those that were not renewed. Renewed and nonrenewed awards exhibited a similar median starting year (2001 vs 2003; P = .4680) and were disbursed over a similar funding period (4.0 years each; P = .7042). Renewed awards were associated with greater 2020 inflation-adjusted funding per year ($494,808 vs $453,676; P = .0799). Renewed awards were also associated predominantly with the National Heart, Lung, and Blood Institute (NHLBI; n = 31; 93.9%; Figure 1, A), and all other renewed awards were associated with the National Cancer Institute (n = 2; 6.1%). Among renewed awards in the NHLBI (Figure 1, B), the most common study sections were Surgery and Bioengineering (n = 12; 38.7%), Bioengineering, Technology, and Surgical Sciences (n = 9; 29.0%), and Surgery, Anesthesiology, and Trauma (n = 6; 19.4%). A similar distribution of NIH institutes (P = .6659) and NHLBI study sections (P = .4309) was observed for the renewed versus nonrenewed award cycles.
      Table 1Characteristics of cardiothoracic surgery basic science R01 awards that were renewed or not renewed
      R01 award characteristicRenewed (n = 33)Not renewed (n = 69)P value95% CI of difference
      Award start year2001 (1996-2009)2003 (2000-2009).4680−5.0 to 2.0
      Length of funding period, years4.0 (4.0-5.0)4.0 (4.0-5.0).70420.0-0.0
      2020 Inflation-adjusted funding per year, $494,808 (428,521-601,583)453,676 (402,501-539,975).0799−4088 to 107,708
      NIH Institute.6659
       NHLBI31 (93.9)58 (84.1)
       NCI2 (6.1)8 (11.6)
       National Institute on Aging0 (0)1 (1.4)
       National Institute of Allergy and Infectious Diseases0 (0)1 (1.4)
       National Institute of Neurological Disorders and Stroke0 (0)1 (1.4)
      NHLBI study section.4309
       Surgery and Bioengineering12 (38.7)22 (37.9)
       Bioengineering, Technology and Surgical Sciences9 (29.0)11 (19.0)
       Surgery, Anesthesiology, and Trauma6 (19.4)9 (15.5)
       Special Emphasis Panel2 (6.5)9 (15.5)
       Cardiac Contractility, Hypertrophy, and Failure1 (3.2)2 (3.4)
       Lung Biology and Pathology1 (3.2)0 (0)
       Clinical and Integrative Cardiovascular Sciences0 (0)3 (5.2)
       Respiratory Integrative Biology and Translational Research0 (0)2 (3.4)
      NCI study section.5044
       Clinical Oncology1 (50.0)0 (0)
       Special Emphasis Panel1 (50.0)3 (37.5)
       Medical Imaging0 (0)1 (12.5)
       Biomaterials and Biointerfaces0 (0)1 (12.5)
       Tumor Progression and Metastasis0 (0)1 (12.5)
       Cancer Etiology0 (0)1 (12.5)
       Experimental Therapeutics Subcommittee0 (0)1 (12.5)
      Data are presented as median (interquartile range) or n (%). Percentages might not sum to 100% because of rounding.
      NIH, National Institutes of Health; NHLBI, National Heart, Lung, and Blood Institute; NCI, National Cancer Institute.
      Figure thumbnail gr1
      Figure 1Distribution of (A) National Institutes of Health (NIH) Institutes and (B) National Heart, Lung, and Blood Institute (NHLBI) study sections among renewed cardiothoracic surgery basic science R01 awards (n = 33). Renewed awards were predominantly associated with the NHLBI (n = 31), whereas the remainder were associated with the National Cancer Institute (NCI; n = 2). The NHLBI study sections among renewed R01 awards included the Surgery and Bioengineering study section (SB; n = 12), the Bioengineering, Technology and Surgical Sciences study section (BTSS; n = 9), the Surgery, Anesthesiology and Trauma study section (SAT; n = 6), the Cardiac Contractility, Hypertrophy, and Failure study section (CCHF; n = 1), the Lung Biology and Pathology study section (LBPA; n = 1), and Special Emphasis Panels (SEP; n = 2).

      CT Surgeon PI Characteristics

      The characteristics of CT surgeon PIs of award cycles that were renewed were similar to those of award cycles that were not renewed (Table 2). Men accounted for nearly all PIs in both groups (97.0% vs 91.3%; P = .4233, respectively (Figure 2, A), and only 1 woman was PI of a renewed basic science R01 grant. The distribution of cardiac (60.6% vs 56.5%), thoracic (24.2% vs 27.5%), and congenital surgeons (15.2% vs 15.9%) serving as PI was similar among the renewed and nonrenewed awards (P = .9209). The PIs of the renewed and nonrenewed awards had also served as attending surgeons for a similar duration (13.0 vs 11.0 years; P = .6495), and represented a similar distribution of full professors (69.7% vs 66.7%; P = .3976) and department/division chairs (42.4% vs 34.8%; P = .5144), respectively.
      Table 2CT surgeon PI characteristics for basic science R01 awards that were renewed or not renewed
      CT surgeon PI characteristicRenewed (n = 33)Not renewed (n = 69)P value95% CI of difference
      Sex.4233
       Male32 (97.0)63 (91.3)
       Female1 (3.0)6 (8.7)
      Surgeon Subspecialty.9209
       Cardiac20 (60.6)39 (56.5)
       Thoracic8 (24.2)19 (27.5)
       Congenital5 (15.2)11 (15.9)
      Dedicated research training20 (60.6)47 (68.1).5072
      PhD degree5 (15.2)12 (17.4)>.9999
      First author basic science publication during training23 (69.7)52 (75.4).5440
      Start year as attending1988 (1979-1999)1990 (1984-1999).3413−7.0 to 2.0
      Total years as attending13.0 (7.0-19.0)11.0 (7.5-18.0).6495−2.0 to 4.0
      Academic rank.3976
       Unknown4 (12.1)15 (21.7)
       Associate professor6 (18.2)8 (11.6)
       Full professor23 (69.7)46 (66.7)
      Department or division chair14 (42.4)24 (34.8).5144
      Previous NIH K grant5 (15.2)6 (8.7).3282
      Previous NIH R grant (non-R01)7 (21.2)20 (29.0).4777
      Previous NIH R01 grant21 (63.6)37 (53.6).3964
      Top 25 NIH-funded institution23 (69.7)37 (53.6).1228
      Career first-author publications33.0 (21.5-40.0)27.0 (19.0-43.5).3348−4.0 to 9.0
      Career last-author publications69.0 (28.5-116.5)40.0 (20.5-95.0).1368−4.0 to 36.0
      Career total publications170.0 (131.0-277.5)140.0 (87.0-241.5).2385−17.0 to 71.0
      Publications per year as attending10.0 (7.6-12.3)7.7 (5.2-11.7).0745−0.18 to 3.46
      Changed institution during grant3 (9.1)7 (10.1)>.9999
      Co-PI0 (0.0)1 (1.4)>.9999
      Data are presented as median (interquartile range) or n (%). Percentages might not sum to 100% because of rounding.
      CT, Cardiothoracic; PI, principal investigator; NIH, National Institutes of Health.
      Figure thumbnail gr2
      Figure 2The characteristics of cardiothoracic surgeon principal investigators are compared for basic science R01 awards that were renewed (n = 33) versus not renewed (n = 69). Similar distributions were observed with regard to (A) surgeon gender (renewed n = 1/33 women vs nonrenewed n = 6/69 women), (B) history of previous R01 grant funding (renewed n = 21/33 vs nonrenewed n = 37/69), or (C) faculty position at a top-25 National Institutes of Health (NIH)-funded institution (renewed n = 23/33 vs nonrenewed n = 37/69).
      A similar large percentage of PIs for the renewed and nonrenewed award cycles had pursued a dedicated research fellowship during training (60.6% vs 68.1%; P = .5072) and published a first-author basic science article during training (69.7% vs 75.4%; P = .5440), although only a small percentage in each group had earned a PhD degree (15.2% vs 17.4%, respectively; P > .9999). There was no difference in the proportion of PIs for renewed and nonrenewed awards who had previously received an NIH K grant (15.2% vs 8.7%; P = .3282), an NIH R grant other than an R01 (21.2% vs 29.0%; P = .4777), or a previous R01 grant (63.6% vs 53.6%; P = .3964; Figure 2, B). The PIs for renewed awards more often represented a top-25 NIH-funded institution (69.7% vs 53.6%; P = .1228; Figure 2, C). At the end of the funding cycle (ie, at the time of potential grant renewal), the PIs for renewed awards had been more prolific over their careers (170.0 vs 140.0 total publications; P = .2385) and published more frequently as an attending (10.0 vs 7.7 publications per year; P = .0745). Finally, a similar proportion of renewed and nonrenewed awards involved a CT surgeon PI who changed institutions during the funding cycle (9.1% vs 10.1%; P > .9999), and a similar proportion of renewed and nonrenewed awards were led by a co-PI in addition to the CT surgeon (0.0% vs 1.4%, respectively; P > .9999).

      Research Output and Scholarly Impact During the R01 Funding Cycle

      Research output and scholarly impact during the R01 funding cycle are presented in Table 3. Awards that were renewed produced more total publications over the funding cycle than awards that were not renewed (16.0 vs 8.0 publications; P = .0058; Figure 3, A), as well as more publications per year over the funding cycle (3.4 vs 1.5 publications per year; P = .0010; Figure 3, B). The publications linked to renewed awards also exhibited greater scholarly impact, in terms of median RCR for the funding cycle (0.84 vs 0.66; P = .0183; Figure 4, A) and maximum RCR for the funding cycle (3.22 vs 2.02; P = .0259; Figure 4, B).
      Table 3Research output and scholarly impact during the funding cycle of cardiothoracic surgery basic science R01 awards that were renewed or not renewed
      Research output and scholarly impact during funding cycleRenewed (n = 33)Not renewed (n = 69)P value95% CI of difference
      Total publications16.0 (6.0-26.0)8.0 (3.0-14.5).00582.00-11.00
      Publications per year3.4 (1.6-5.5)1.5 (0.6-3.1).00100.58-2.50
      Median RCR0.84 (0.67-1.29)0.66 (0.40-0.98).01830.03-0.39
      Maximum RCR3.22 (2.00-5.91)2.02 (0.70-4.81).02590.20-1.99
      Data are presented as median (interquartile range).
      RCR, Relative citation ratio.
      Figure thumbnail gr3
      Figure 3Research output for cardiothoracic surgery basic science R01 awards that were renewed (n = 33) versus not renewed (n = 69). A, Renewed awards yielded a greater number of total publications during the funding cycle compared with nonrenewed awards. B, Renewed awards yielded a greater number of publications per year of the funding cycle compared with nonrenewed awards. The upper and lower borders of the box define the interquartile range with the middle horizontal line representing the median. The upper and lower whiskers define the maximum and minimum values of nonoutliers, with additional dots representing outliers.
      Figure thumbnail gr4
      Figure 4Scholarly impact of manuscripts published during the funding cycle of cardiothoracic surgery basic science R01 awards that were renewed (n = 33) or not renewed (n = 69). An article with a relative citation ratio (RCR) of 1.00 indicates equal impact as other R01-funded publications in the same field. A, Renewed awards exhibited a greater median RCR among publications linked to the funding cycle compared with nonrenewed awards. B, Renewed awards exhibited a greater maximum RCR among publications linked to the funding cycle compared with nonrenewed awards. The upper and lower borders of the box define the interquartile range with the middle horizontal line representing the median. The upper and lower whiskers define the maximum and minimum values of nonoutliers, with additional dots representing outliers.

      Discussion

      In this study, we compared the award characteristics, the surgeon PIs, and the publications funded by basic science CT surgery R01 awards that were renewed versus those that were not renewed. We observed similar attributes among the CT surgeon PIs of renewed versus nonrenewed awards, including subspecialty type, research training, clinical experience, academic rank, and history of previous NIH funding, although renewed awards tended to be associated with a PI with greater career research output at a top NIH-funded institution. We also observed, however, that renewed awards were associated with more publications during the funding period, and that these funded publications also exhibited a greater scholarly impact. These findings suggest that research output and scholarly impact during the preceding award cycle might represent important factors for R01 grant renewal (Figure 5).
      Figure thumbnail gr5
      Figure 5On the basis of data regarding research output and scholarly impact for 102 National Institutes of Health (NIH) basic science R01 funding cycles awarded to cardiothoracic (CT) surgeons, we observed that surgeon-scientists should aim to publish 3.4 articles per year during the R01 funding cycle while maintaining a goal median relative citation ratio (RCR) of 0.84 to be at the 50th percentile among CT surgeons in the renewal process. A publication with an RCR of 1.00 indicates equal impact as a R01-funded publication in the same field. The upper and lower borders of the box define the interquartile range with the middle horizontal line representing the median. The upper and lower whiskers define the maximum and minimum values of nonoutliers, with additional dots representing outliers.
      The evaluation of R01 grant applications centers on peer review, involving a standardized scoring system and 2 levels of assessment.
      NIH Central Resource for Grants and Funding Information. Peer review.
      In the first round, reviewers from a scientific review group, also known as a study section, evaluate the scientific and technical merit of the proposal and assign a criterion score in each of 5 areas: significance, investigator, innovation, approach, and environment. Renewal status (as opposed to a first-time application) is considered as an additional review criteria at this stage. An overall impact score is then determined for the grant application. Subsequently, a second round of review is conducted by the appropriate NIH institute, which considers the relevance of each application according to the institute's mission, goals, and priorities when determining the final funding decision.
      Analyses conducted by the NIH have shown that each of the 5 criterion scores is an important contributor to an R01 application's overall impact score.
      • Lindner M.D.
      • Vancea A.
      • Chen M.C.
      • Chacko G.
      NIH peer review: scored review criteria and overall impact.
      Interestingly, the approach score appears to be the most important predictor of the overall impact score and the likelihood of funding, followed by the significance and innovation scores.
      • Eblen M.K.
      • Wagner R.M.
      • RoyChowdhury D.
      • Patel K.C.
      • Pearson K.
      How criterion scores predict the overall impact score and funding outcomes for National Institutes of Health peer-reviewed applications.
      In contrast, the environment score had the lowest association, followed by the investigator score. A follow-up analysis by the NIH, focusing exclusively on R01 renewal applications, confirmed that the approach and significance scores were the strongest predictors of the overall impact score and the ultimate renewal result, and that PI characteristics (eg, age, gender, research training background) were not correlated with success.
      • Lauer M.
      Characteristics and outcomes of R01 competing renewal applications (“type 2s”).
      On the basis of these data, the NIH has emphasized that a well designed and clearly described experimental strategy for continued high-impact research is central to a successful R01 grant renewal application.
      In parallel with the NIH data showing that the investigator and environment scores might be least influential among the 5 criterion scores, we noted similar CT surgeon PI characteristics among the renewed versus nonrenewed award cycles. However, we acknowledge the small sample size of our study, and we nevertheless observed that PIs of renewed grants tended to have a higher career publication rate and may be more likely to represent a top-25 NIH-funded institution. As such, the surgeon's academic record and the strength of the institution's research environment might be less influential than the overall impact and strategy of the proposed research, but they are nevertheless important.
      Notably, we identified only 1 renewed basic science R01 grant for which a woman in our database served as PI. Krebs and colleagues
      • Krebs E.D.
      • Narahari A.K.
      • Cook-Armstrong I.O.
      • Chandrabhatla A.S.
      • Mehaffey J.H.
      • Upchurch Jr, G.R.
      • et al.
      The changing face of academic surgery: overrepresentation of women among surgeon-scientists with R01 funding.
      recently showed that women constitute a greater than anticipated proportion of surgeon-scientists with R01 funding, and that female surgeons with R01 grants were more likely to be first-time awardees with no previous NIH funding. Although women obtain new R01 or equivalent grants with comparable success rates as men, women historically have experienced lower success rates for renewal applications,
      NIH RePORT
      NIH Data Book. R01-equivalent grants: success rates, by gender and type of application.
      in part because of lower approach, significance, and overall impact scores than men during peer review.
      • Kaatz A.
      • Lee Y.G.
      • Potvien A.
      • Magua W.
      • Filut A.
      • Bhattacharya A.
      • et al.
      Analysis of National Institutes of Health R01 application critiques, impact, and criteria scores: does the sex of the principal investigator make a difference?.
      To sustain the women who represent an essential, enlarging group of surgeon-scientists, additional support and attention must be directed toward facilitating research training opportunities and expanding mentorship and sponsorship networks for women in CT surgery.
      • Williams K.M.
      • Hironaka C.E.
      • Wang H.
      • Bajaj S.S.
      • O'Donnell C.T.
      • Sanchez M.
      • et al.
      Women in thoracic surgery scholarship: impact on career path and interest in cardiothoracic surgery.
      In addition, women remain under-represented in CT surgery department leadership,
      • Singh S.K.
      • Bi A.
      • Kurlansky P.A.
      • Argenziano M.
      • Smith C.R.
      A cross-sectional review of cardiothoracic surgery department chairs and program directors.
      and previous reports indicate that female surgeons with R01 funding are significantly more likely to be from surgery departments led by women.
      • Krebs E.D.
      • Narahari A.K.
      • Cook-Armstrong I.O.
      • Chandrabhatla A.S.
      • Mehaffey J.H.
      • Upchurch Jr, G.R.
      • et al.
      The changing face of academic surgery: overrepresentation of women among surgeon-scientists with R01 funding.
      Women are also under-represented among the leadership of our specialty's national societies,
      • Olive J.K.
      • Preventza O.A.
      • Blackmon S.H.
      • Antonoff M.B.
      Representation of women in the society of thoracic surgeons authorship and leadership positions.
      as well as on the NIH study sections that evaluate R01 grant applications.
      • Lewit R.A.
      • Black C.M.
      • Camp L.
      • Brott N.
      • Cottrell J.M.
      • Herman T.
      • et al.
      Association of surgeon representation on NIH study sections with receipt of funding by surgeon-scientists.
      The correction of these gender disparities at the level of local and national leadership might further help female surgeon-scientists maintain long-term research funding.
      Importantly, our analysis of publications linked to each R01 funding cycle provides a new quantitative dimension of the R01 renewal application not captured by the 5 criterion scores. Awards that were renewed produced a median of 3.4 publications per year during the funding cycle, translating to a median of 16.0 publications over the course of the award. Although nonrenewed awards were also highly productive in terms of research output, our data suggest that CT surgeons should aim to publish 3.4 funded manuscripts per year during the R01 funding cycle to be at the 50th percentile in the renewal process.
      In addition to quantity, we also observed that the impact of research published during an R01 funding cycle might be an important factor distinguishing renewed and nonrenewed awards. Compared with a reference RCR of 1.00 for other R01-funded articles in the same field, we calculated a median RCR of 0.84 among publications linked to each renewed CT surgery R01 award. This result indicates that the scholarly impact of articles funded by renewed CT surgery basic science R01 grants was approximately on par with the expected impact of R01-funded articles in the field, and that CT surgeons should aim to maintain a median RCR at least 0.84 during the R01 funding cycle to be at the 50th percentile in the renewal process.
      In our study, the overall R01 renewal rate for CT surgeons was 32.4%, whereas the success rate for renewal applications across the entire NIH was as high as 45% in recent years.
      NIH RePORT
      NIH Data Book. R01-equivalent grants: success rates, by gender and type of application.
      However, of the 14 CT surgery R01 awards that published at least 3.4 articles per year with a median RCR at least 0.84, 10 were renewed, yielding an impressive renewal rate of 71.4%. In contrast, the renewal rate for awards with at least 3.4 papers per year but median RCR <0.84 was 7 of 15 (46.7%), on par with the NIH average, whereas the renewal rate for awards with <3.4 articles per year but median RCR of at least 0.84 was 7 of 25 (28.0%). Among the remaining 48 awards with research output of <3.4 articles per year and a median RCR of <0.84, only 9 were renewed (18.8%). These data suggest that high research output alone might be insufficient to enhance the likelihood of renewal compared with the NIH average. Instead, both research output and scholarly impact appear to be important, as high-impact research proposals might have stronger significance, innovation, and approach criterion scores.
      • Lindner M.D.
      • Vancea A.
      • Chen M.C.
      • Chacko G.
      NIH peer review: scored review criteria and overall impact.
      Awareness of how research output and scholarly impact relate to R01 grant renewal might help CT surgeon-scientists develop a multiyear research plan that optimizes the balance of output and impact. Such planning might be particularly important in basic science research, in which the highest-impact studies might require substantial time to complete supporting experiments to confirm an initial discovery. As a result, pursuing only the highest-impact experiments might result in fewer publications, whereas aiming to publish prolifically but with lower scholarly impact might risk an unfavorable overall impact score.
      It is important to note that the research produced by CT surgery basic science R01 grants was highly impactful regardless of renewal status, as the 50th percentile of maximum RCR among nonrenewed award cycles was 2.02, which compares favorably to the reference value of 1.00 for other R01-funded publications in the same field. Renewed awards exhibited an even greater maximum RCR of 3.22 at the 50th percentile. To maintain the high impact of CT surgery basic science research in the future, support for residents and early-career surgeons who represent the next generation of independent surgeon-scientists must be a top priority, at the institutional and national levels.
      • Ikonomidis J.S.
      • Menasché P.
      • Kreisel D.
      • Sellke F.W.
      • Woo Y.J.
      • Colson Y.L.
      Attrition of the cardiothoracic surgeon-scientist: definition of the problem and remedial strategies.
      Indeed, in our database, only 7.4% of CT surgery faculty are currently leading basic science research.
      • Wang H.
      • Bajaj S.S.
      • Krishnan A.
      • Heiler J.C.
      • Williams K.M.
      • Pickering J.M.
      • et al.
      Characterization of cardiothoracic surgeons actively leading basic science research.
      Aside from providing laboratory training, mentorship, protected research time, career advancement incentives, and recognition of research accomplishments, institutional leaders should facilitate multidisciplinary collaborations to encourage the exchange of innovative ideas and novel experimental techniques. In addition, through scholarships and fellowships, national organizations such as the American Association for Thoracic Surgery (AATS; https://www.aats.org/aatsimis/AATSWeb/Scholarships/AATSWeb/Scholarships/Scholarship_Overview.aspx) and the Society of Thoracic Surgeons and Thoracic Surgery Foundation (https://thoracicsurgeryfoundation.org/awards) are actively supporting high-impact CT surgery research and are working to further expand funding for CT surgeon-scientists by hosting communications with the NIH and other funding sources (eg, through the AATS Scientific Affairs and Government Relations Committee), and by continuing to feature academic development programs (eg, AATS Grant Writing Workshop, Clinical Trials Methods Course, and Innovation Summit) and dedicated conference sessions focused on academic career development during the annual AATS and Society of Thoracic Surgeons meetings.

      Limitations

      Our study has several limitations that must be carefully considered. First, because our analysis is focused only on NIH basic science R01 funding, our study does not represent a comprehensive assessment of CT surgery research funding, because other funding sources (eg, National Science Foundation, American Cancer Society, Department of Defense, Veterans Affairs) were not included. Future studies will endeavor to incorporate non-NIH funding sources as data become available. Next, our database of CT surgeons is derived from the university faculty at accredited CT surgery training hospitals, excluding surgeons working at affiliated satellite hospitals (eg, Veterans Affairs hospitals, county/community hospitals) and those working at university hospitals without accredited CT surgery training programs. As a result, our database does not include all of the academic CT surgeons in the country, does not include a control group of other surgeons or physician-scientists to which to compare our results, and does not capture every NIH R01 grant awarded to CT surgeons. Because clinical research grants often are not renewed after project completion, we chose to focus our analysis only on basic science R01 grants. With 102 award cycles identified, of which only 33 were renewed, it is possible that our sample size limited the statistical power of some analyses, although our findings regarding the association of high research output and scholarly impact to grant renewal would not be expected to change. Nevertheless, we recognize that during the NIH's evaluation process, the determination of which grants are renewed is on the basis of numerous factors beyond simply the research output and scholarly impact of the previous funding cycle. Thus, further studies with multivariable models including the criterion scores from peer review are required to clarify the relative weight of these factors during R01 renewal evaluation. In addition, we assumed that all R01 awards were intended for renewal, whereas some might have been intended only for a single cycle, leading to an underestimated overall renewal rate. Unfortunately, with the publicly available resources at our disposal, we have access only to data for funded grants and not the full list of grant applications. Finally, we determined the research output of each R01 award cycle using NIH RePORTER, which links publications to the grant on the basis of documentation of funding in each article or by direct PI reporting. Thus, it is possible that some publications supported by an R01 grant were not linked to the funding cycle, leading to underestimates for research output.

      Conclusions

      Overall, we observed that CT surgery basic science R01 awards are associated with high research output and scholarly impact. At the 50th percentile among renewed basic science R01 grants, CT surgeons published 3.4 funded manuscripts per year with a median RCR of 0.84 during the previous award cycle. These goals for research output and scholarly impact might help guide CT surgeon-scientists aiming to renew a basic science R01 grant.

      Webcast

      Conflict of Interest Statement

      The authors reported no conflicts of interest.
      The Journal policy requires editors and reviewers to disclose conflicts of interest and to decline handling or reviewing manuscripts for which they may have a conflict of interest. The editors and reviewers of this article have no conflicts of interest.
      The authors thank Dr Christian T. O'Donnell, Joshua M. Pickering, Keerthi Manjunatha, and Mark Sanchez for their assistance with data collection for our database of CT surgeons.

      Appendix

      Table E1List of 76 National Institutes of Health R01 grants included for analysis, with the corresponding cardiothoracic surgeon principal investigator(s)
      Grant identification numberPrincipal investigator(s)
      1R01AG036954Ikonomidis, John S.
      2R01AI044078Pierson, Richard N.
      3R01CA045187Roth, Jack
      4R01CA090665Luketich, James D.
      5R01CA093708Jablons, David M.
      6R01CA131044Colson, Yolonda L.
      7R01CA132566Jablons, David M.
      8R01CA136705Jones, David R.
      9R01CA149561Colson, Yolonda L.
      10R01CA163256Singhal, Sunil
      11R01CA176568Roth, Jack
      12R01HL026640Foker, John E.
      13R01HL029589Miller, D. Craig
      14R01HL032257Damiano, Ralph J.
      15R01HL037499Miller, D. Craig
      16R01HL038078Magovern, George J.
      17R01HL038791Verrier, Edward Donald
      18R01HL041163Spotnitz, Henry Michael
      19R01HL041281Patterson, George Alexander
      20R01HL043357Hanley, Frank
      21R01HL046207Del Nido, Pedro
      22R01HL046242Glower, Donald D.
      23R01HL047078Mentzer, Steven J.
      24R01HL047191Cameron, Duke
      25R01HL047604Pasque, Michael K.
      26R01HL048091Griffith, Bartley Perry
      27R01HL048109Spotnitz, Henry Michael
      28R01HL051032Damiano, Ralph J.
      29R01HL056227Glower, Donald D.
      30R01HL057310Jessen, Michael E.
      31R01HL057431Cochran, Richard P.
      32R01HL058781Bolling, Steven F.
      33R01HL060463Mayer, John E.
      34R01HL061762Verrier, Edward Donald
      35R01HL063095Del Nido, Pedro
      36R01HL063159Egan, Thomas M.
      37R01HL064950Griffith, Bartley Perry
      38R01HL066015Holman, William L.
      39R01HL066981Rosengart, Todd K.
      40R01HL067025Miller, D. Craig
      41R01HL067110Allan, James S.
      42R01HL069949Moon, Marc R.
      43R01HL070852Thistlethwaite, Patricia A.
      44R01HL071128Del Nido, Pedro
      45R01HL071541Bull, David Andrew
      46R01HL072183Milano, Carmelo A.
      47R01HL073647Del Nido, Pedro
      48R01HL074150Colson, Yolonda L.
      49R01HL075426Mentzer, Steven J.
      50R01HL075488Ikonomidis, John S.
      51R01HL080152Spotnitz, Henry Michael
      52R01HL081106Griffith, Bartley Perry
      53R01HL082631Griffith, Bartley Perry
      54R01HL083118Mann, Michael J.
      55R01HL085095Rosengart, Todd K.
      56R01HL085341Coselli, Joseph S.; Lemaire, Scott A.
      57R01HL089269Del Nido, Pedro
      58R01HL089315Woo, Y. Joseph
      59R01HL089592Selzman, Craig Harold
      60R01HL090862Chen, Frederick Y.
      61R01HL092088Moon, Marc R.
      62R01HL093097Mulligan, Michael Scott
      63R01HL094567Mentzer, Steven J.
      64R01HL094601Kreisel, Daniel
      65R01HL098182Lawton, Jennifer S.
      66R01HL098353Rodefeld, Mark D.
      67R01HL098634Eghtesady, Pirooz
      68R01HL102121Ikonomidis, John S.
      69R01HL109132Gleason, Thomas Gillette
      70R01HL110997Del Nido, Pedro
      71R01HL113931Kreisel, Daniel; Krupnick, Alexander
      72R01HL118372Griffith, Bartley Perry
      73R01HL118491Kaushal, Sunjay
      74R01HL119543Thistlethwaite, Patricia A.
      75R01HL124170Griffith, Bartley Perry
      76R01NS039499Kern, John A.
      Grants are listed in alphabetical order according to identification number.

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