Clinical Cancer Research 14, 1782, March 15, 2008. doi: 10.1158/1078-0432.CCR-07-4886
© 2008 American Association for Cancer Research
Improving the Quality of Abstract Reporting for Phase I Cancer Trials
Elizabeth L. Strevel1,
Nicole G. Chau1,
Gregory R. Pond1,
Anthony J. Murgo2,
Percy S. Ivy2 and
Lillian L. Siu1
Authors' Affiliations: 1 Princess Margaret Hospital, University of Toronto, Toronto, Ontario, Canada and 2 National Cancer Institute, Bethesda, Maryland
Requests for reprints: Lillian L. Siu, Division of Medical Oncology and Hematology, Princess Margaret Hospital, University of Toronto, 610 University Avenue, Suite 5-718, Toronto, Ontario, Canada M5G 2M9. Phone: 416-946-2911; Fax: 416-946-4467; E-mail: lillian.siu{at}uhn.on.ca.
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Abstract
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Purpose: Conference abstracts of phase I trials (P1T) communicate important anticancer drug development information. Our objectives were to determine elements essential for good P1T abstract reporting, to assess the quality of P1T abstracts submitted to American Society of Clinical Oncology (ASCO) meetings, and to propose reporting guidelines.
Experimental Design: A survey of developmental therapeutics experts established elements of P1T reporting quality, and a scoring system was generated. All P1T abstracts published in ASCO Annual Proceedings from 1997 to 2006 were reviewed, and the scoring system was applied.
Results: A survey was distributed twice to 69 experts, with a response rate of 39% (27 of 69). Experts rated 37 elements using a five-point scale, and elements with mean ratings over 3.75 were included in the final scoring system. One thousand six hundred and eighty three P1T abstracts were reviewed. A positive and linear association was observed between average expert rating of the elements and the proportion of P1T abstracts including those elements (Spearman correlation coefficient, 
= 0.60, P < 0.001). The median for all 1,683 abstracts was 62.5% (range, 25-95%; SD, 12.3%). Year of presentation was found to be significantly associated with higher quality scores ( = 0.20, P < 0.001), with later years possessing better quality scores. The quality score was statistically significant as a predictor of type of presentation (odds ratio, 1.10; 95% confidence interval, 1.02-1.19 per 10% increase; P = 0.014), with oral presentations having the highest scores.
Conclusions: The quality of P1T abstract reporting at ASCO has improved over time, although there is room for optimization. The quality of P1T abstract reporting may be enhanced using guidelines derived from our expert consensus.
Phase I trials (P1T), the first level of clinical investigation for a new drug or drug combination, provide necessary foundations for the development of safe and more effective anticancer therapies. These trials are often initially presented in abstract format at major cancer conferences, such as the annual meeting of the American Society of Clinical Oncology (ASCO). Results of P1Ts published in abstract format only frequently influence further research endeavors in higher-phase trials before full peer-reviewed publication occurs (1). Investigators often accept data from abstract reporting due to time delays incurred with publishing, failure to publish, as well as a relative sense of urgency to further examine promising agents with an efficacy-guided end point (2–5). Thus, conference abstracts of P1Ts are important records that affect future directions in oncology research and, ultimately, patient care.
Despite the importance of early-phase trial abstracts reported at ASCO meetings, no guidelines exist that specifically address their content or quality. Reporting guidelines have been issued for the publication of randomized controlled trials (RCT; CONSORT), meta-analyses (QUORUM), and cost-effectiveness analyses (6–9). There is evidence to suggest that use of these guidelines improves the quality of full-publication reporting (10–13). Conference abstract reporting standards have also been examined for RCTs (14–21). A study by Krzyzanowska et al. (22) assessing the quality of RCT abstracts reported at ASCO between 1989 and 1998 highlighted deficiencies in abstract reporting and recommended minimal reporting guidelines for these trials. These guidelines have since been endorsed by ASCO since 2004. We believe similar quality assurance measures are indicated for P1Ts.
In the current study, we collated common elements of oncology P1T reporting and rated their importance for inclusion in abstracts submitted to ASCO meetings based on a survey of experts in the field. Minimal reporting guidelines as well as a quality scoring system were developed from this survey. Subsequently, the scoring system was applied to P1T abstracts submitted to ASCO meetings over a 10-year period, from 1997 to 2006. Our study aimed to examine the strengths and deficiencies in the reporting of P1T abstracts submitted to previous ASCO meetings and to determine the applicability of our minimal reporting guidelines for the future selection of P1T abstracts.
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Materials and Methods
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Survey of developmental therapeutics experts. Permission and ethical approval of this project were obtained from the University Health Network's Institutional Review Board in Toronto, Canada. To develop a scoring system for P1T abstract reporting, we conducted a survey of developmental therapeutics experts who were selected from the following: principal investigators of the U.S. National Cancer Institute/Cancer Therapy and Evaluation Program phase I cooperative agreement awards (U01) and phase II contracts (N01), members of the 2006 ASCO developmental therapeutics scientific subcommittee, and editorial board members from the Journal of Clinical Oncology's phase I and clinical pharmacology committee. An electronic survey was distributed by e-mail. Each respondent was asked to rate 37 items that might be included in a P1T abstract using a scale from 1 (absolutely should not be included) to 5 (absolutely essential for inclusion). A reminder e-mail was sent 2 wk after initial contact. We then summed the expert ratings for each of the 37 items and divided by the number of responses to obtain an average expert rating. The quality score of an abstract was subsequently created by assigning weights to each of the 37 items based on its average expert rating.
Development of the quality scoring system. The average expert ratings were used to categorize the 37 P1T abstract items into four groups: (a) those items that are absolutely essential for inclusion in P1T abstract reporting (n = 7; average expert rating, 
4.5), (b) those items that should be reported (n = 8; average expert rating, 4.0-4.49), (c) those items that may be reported if space permits (n = 6; average expert rating, 3.75-3.99), and (d) those items that are unlikely to be informative (n = 15; average expert rating, <3.75). These four groups of items were then assigned various weights to reflect their importance, as deemed by the field experts, for inclusion in a P1T abstract. Specifically, 3 points were assigned for absolutely essential items, 2 points for items that should be reported, 1 point for items that may be reported if space permits, and 0 point for items that are unlikely informative. No points were deducted. Therefore, a single abstract could attain a maximum quality score of 43 points. The item "conclusion explicitly states the maximum tolerated dose (MTD) or recommended dose (RD) achieved on study" could not be answered in all cases as some studies may have been ongoing when the abstract was submitted or a trial may have closed prematurely. Therefore, it was decided to combine the items "conclusion explicitly states the MTD or RD achieved on study" and "conclusion explicitly states reason for early trial closure" into a single item for scoring purposes. Abstracts that indicated that the MTD or RD was not yet achieved because the trial was ongoing were credited as having provided this information. Additional scoring methods were investigated based on different weighting schemes with a very high correlation between each method and the above-mentioned method selected (Pearson correlation coefficient > 0.87 for all methods).
The quality score was then normalized to a percentage for ease of interpretation and comparison because some items were not applicable to all studies such that the denominator of the quality score of some abstracts can be lower than 43 points. For instance, for the item "tumor types of responders," only P1Ts that reported objective responses were eligible to obtain a score for this item. Other P1Ts that did not report objective responses were considered not evaluable for this item and the quality score denominator would have been adjusted accordingly to reflect this.
Assessment of the quality of reporting in ASCO abstracts. We reviewed the Proceedings of the ASCO Annual Meeting for years 1997 to 2006 and identified all P1T abstracts from the "Development Therapeutics" and "Clinical Pharmacology" sections. We excluded abstracts involving children or phase II trials. All remaining P1T abstracts (n = 1,683) were reviewed using a standardized data abstraction form, which we designed based on the results of the expert survey and had pilot tested on a sample of 50 abstracts. Data abstraction was done by two of the authors (E.L.S. and N.G.C.). To ensure interrater agreement, 10% of the abstracts (n = 169) were coded by both individuals for comparison and an overall agreement of 97.5% was achieved. The quality of reporting of P1T abstracts was determined by assigning a normalized quality score in percentage for each abstract.
Statistical considerations. Summary statistics were used to describe the baseline abstract characteristics, characteristics of the experts and their survey responses, and the data abstraction results. Exact 95% confidence intervals were constructed for the average expert ratings and for the normalized quality score. Interrater agreement in data abstraction was assessed by calculating percent agreement across all variables from 10% of randomly selected abstracts.
Linear regression with normalized quality score as the outcome variable was used to identify factors associated with the quality of reporting, and visual inspection was used to assess the assumption of normality. Pearson correlation was used to assess potential association between year of presentation (1997-2006), and logistic regression was used to investigate whether the normalized quality score was predictive of type of presentation (oral or plenary, poster, or published).
Statistical analyses were done using Statistical Analysis System version 8.2 (SAS Institute). All tests were two sided and a statistically significant result was defined as a test with a P value of 
0.05.
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Results
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Characteristics of experts. Sixty-nine experts in oncology developmental therapeutics were surveyed and 27 replied, yielding a response rate of 39%. Demographic characteristics of our survey respondents are summarized in Table 1
. The majority of respondents had 10 to 20 years of clinical experience in P1Ts (63%), with 18.5% having 20 to 30 years of expertise. Self-reported research interests were comparably split between translational and clinical endeavors.
Characteristics of P1T abstracts. Characteristics of the 1,683 P1T abstracts included in ASCO Proceedings from 1997 to 2006 are summarized in Table 2
. The number of P1T abstracts in each year was consistent from 1998 to 2006, with slightly lower representation in 1997. Across all years, most abstracts were poster presentations (56%), with fewer being publication only (37%), and the least as oral/plenary presentations (7%). Roughly 60% of the abstracts were monotherapy trials, and just over half had multicenter involvement. Almost three quarters of P1Ts reviewed were industry funded, and 65% were U.S. based.
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Table 2. Characteristics of the 1,683 P1T abstracts reviewed from the Proceedings of ASCO meetings between 1997 and 2006
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Interrater agreement in P1T abstract data abstraction. A 10% sample of abstracts (169 abstracts) was cross-reviewed. The percent agreement for most variables was >95%, and the overall average agreement of all elements was 97.5% (6,923 of 7,098 variables). Variables for which the percent agreement was between 90% and 95% include "information related to the number of treatment cycles," "description of dose-limiting toxicity," "toxicity of all grades related to the study drug," "grade 3 toxicity related to the study drug," and "pharmacodynamic results, if applicable." No element had an overall interrater agreement of <90%.
The quality score system generation and application. The 37 items selected as elements commonly used in P1T reporting and included in our expert survey are summarized in Table 3
, along with the average expert ratings and 95% confidence interval.
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Table 3. Quality of reporting of P1T abstracts included in the Proceedings of ASCO meetings between 1997 and 2006
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A positive and linear relationship was generally observed between the average expert rating of each item and the proportion of P1Ts reporting that factor (Spearman = 0.60, P < 0.001; Fig. 1A
). Two items seemed to be outliers. "Conclusion explicitly states the MTD or RD achieved on study" was only reported in 36% of abstracts, although the average expert rating was 4.85 for this item. When studies that closed early were excluded from this analysis, reporting increased only to 38% and, thus, did not strongly influence this discordance. The second apparent outlier was the "statement about study being conducted in a single center versus multicenter setting," which was reported in 99.8% of abstracts; however, it only had an average expert rating of 3.41. The high representation of this item is explainable as study location(s) can be readily identified by reviewing the authors' affiliation list, which is included in virtually all abstracts.
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Fig. 1. A, relationship between average expert rating on P1T items and proportion of trial abstracts reporting the item. B, distribution of percentage-normalized quality scores of 1,683 abstracts.
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The distribution of the percentage-normalized quality score of all 1,683 examined P1T abstracts is presented in Fig. 1B. The normalized quality score was symmetrically distributed around an average of 61.9% (SD, 12.3%), median of 62.5%, and range of 25.0% to 95.0%. Few abstracts had percent scores <30%, and few in excess of 90%.
Relationship between year/type of presentation and quality score. There was a statistically significant association between year of presentation and normalized quality score ( = 0.20, P < 0.001), as depicted in Fig. 2
. As can be seen, though, this trend was not strictly linear, with significant variability from 1997 to 2000, a slow steady increase from 2000 to 2004, and then large increases in normalized quality score in 2005 and 2006. This trend was most noticeable for poster presentations.
Normalized quality score was also highly statistically significant as a predictor of type of presentation (odds ratio, 1.10; 95% confidence interval, 1.02-1.19 per 10% increase; P = 0.014). To interpret this, for every 10% increase in normalized quality score, the odds of having a higher level presentation (publication to poster or poster to oral/plenary) increased by 1.10 times. Mean (SD) percentage-normalized quality score for oral/plenary abstracts across all years was 62.8% (12.9), 62.4% (12.7) for poster abstracts, and 60.9% (11.3) for publication-only abstracts.
Development of suggested P1T abstract reporting guidelines. Based on the findings of the expert survey and abstract review, essential elements for P1T abstract reporting were identified and included in our proposed guidelines (Table 4
). These elements were derived from the average expert rating results, and items that experts rated >4.0 (absolutely essential and should be reported) were included.
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Discussion
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The results of our study, the first of its kind reviewing 1,683 P1T abstracts submitted to ASCO meetings, show a need for enhanced P1T reporting. Although the quality of P1Ts presented at ASCO has improved with time, there are many striking deficiencies. Given the underreporting of the final results of oncology P1Ts, as well as significant time delays in full publication of these studies, it is essential that trial investigators and authors of P1T abstracts commit to the highest reporting standards (1). The proposed guidelines for reporting of P1T abstracts (Table 4) may help improve the quality of these important records.
Our scoring system, developed from expert consensus, correlates with ASCO's assessment of the quality of a study. A statistically significant relationship between the quality score and type of presentation at ASCO was observed (odds ratio, 1.10; P = 0.014) and supports the validity of the scoring system (i.e., P1T abstracts with a higher quality score were more likely to be awarded oral presentations than lower quality score abstracts). In RCTs, there is evidence to suggest that the quality of a research report reflects the overall quality of the research (17, 19, 20, 23, 24). This association has not been evaluated in P1Ts. However, it is likely that the quality of reporting influences reviewers' opinion of the merit of a P1T abstract for conference acceptance and presentation, albeit this decision likely more directly hinges on qualitative assessment of the scientific merit of a study in the P1T arena.
The overall median reporting quality of the reviewed P1T abstracts was mediocre at 62.5%. A small proportion of abstracts obtained a quality score of >80%, indicating that it is feasible to obtain excellent reporting with this assessment tool. In general, the elements that were weighted as "absolutely essential" by developmental therapeutics experts tended to be included in the majority of P1T abstracts. However, some salient deficiencies were noted. Major end points of P1Ts, such as MTD or RD and description of dose-limiting toxicity (25), were frequently absent. The underreporting of these primary study end points may be due to the ongoing nature of many trials at the time of abstract submission and/or conference presentation. Indeed, 52.3% of the 1,683 P1Ts reviewed were identified as ongoing. Although many investigators may present final or updated results of their P1Ts during the ASCO meeting, these updated data are typically not reflected in the published abstract report that was submitted at an earlier date. Given that P1Ts remain unpublished on average up to 3.4 years after conference presentation (1), perpetuation of this trend of incomplete reporting of unfinished trials may not be in the best interests of the oncology community. Innovative ideas to tackle this issue include maximizing the use of real-time electronic abstract submissions, shortening the time between abstract submission and acceptance, and allowing critical abstract results, such as MTD or RD, to be updated into the abstract proceedings at the time of conference presentation. Additionally, major conferences such as ASCO are minimizing acceptance of ongoing or incomplete P1Ts.
From 1997 to 2006, the reporting quality of P1T abstracts presented at ASCO improved with time ( = 0.20, P < 0.001). Interestingly, this trend was most striking between 2004 and 2006. Plausibly, improved P1T reporting may be related to increased competitiveness for P1T acceptance at ASCO in recent years, correlating with the molecularly targeted era and an increase in the Food and Drug Administration's Investigational New Drug applications for oncology pharmaceuticals (1). It is also possible that improved P1T reporting occurred as an offshoot of ASCO's 2004 endorsement of RCT reporting guidelines. Although the RCT guidelines do not share many elements common to P1Ts, the emphasis on improved reporting likely had a positive downstream effect.
Indeed, our study is the first of its kind assessing the quality of P1T reporting in any context. Studies examining the quality of non-P1T conference abstract reporting have described similar substandard results and have also called for better conference records (14–22). As conference P1T abstracts carry significant weight for drug development, particularly in oncology, improvement measures are indicated. The guidelines proposed in this study may act as a powerful vehicle to improve P1T reporting. The effect of improving quality of P1T abstract reporting will affect authors, reviewers, industry, and, ultimately, patient care. We realize that, inherent to abstract reporting, strict limitations for space exist; however, we believe that improving quality will make better use of the restricted space provided. Endorsement of quality assurance guidelines in the RCT setting has been shown to improve quality of reporting and also publication (10–13). We infer a similar benefit in the P1T setting. In our opinion, minimal P1T reporting guidelines may be welcomed by authors and reviewers as an objective method to facilitate peer review and fair recognition.
Limitations of this study are noted. In the P1T setting, it is possible that the quality of reporting may not be correlated with the quality of study methodology or the quality of final publication (26, 27). However, oral presentation status, which we have found to be associated with higher quality score, has also been shown to be associated with shorter time to publication. Second, the modest response rate from our expert survey raises the potential for bias. The low proportion of non-American, nonacademic, and governmental representative respondents may make our results less generalizable to these groups of investigators. Nevertheless, our results suggest that our scoring system seems to show face and content validity. Third, our guidelines have a subjective component as the list of items disseminated to field experts for assessment of pertinence in P1T abstract inclusion was generated by the authors due to the lack of existent P1T reporting standards to be used as reference. To minimize bias, we created an exhaustive list of P1T reporting items for experts to review, and developed the scoring system and guidelines based on their feedback. Fourth, as abstracts are preliminary records that do not undergo a thorough peer review process, deficiencies in conference P1T reporting may be rectified on full publication. Finally, our results apply to quality of P1T reporting at ASCO meetings and cannot necessarily be extrapolated to assess the quality of reporting of other types of trials or P1T abstracts reported in other disciplines or meetings. Despite these limitations, given the current lack of standards for P1T reporting and known deficiencies in quality of reporting and publication for such trials, we strongly recommend initiation of P1T reporting guidelines.
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Conclusion
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We have shown a vital need to improve the quality of oncology P1T reporting and strongly support the use of minimal reporting guidelines for future P1T abstracts. The guidelines that we propose may act as a vehicle to improve P1T reporting and therein improve the quality of early-phase clinical research.
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Acknowledgments
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We thank the developmental therapeutics experts who contributed to our project through participating in our survey and provision of valuable feedback.
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Footnotes
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The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Note: Presented in part at the 43rd Annual American Society of Clinical Oncology Meeting, June 1-5, 2007, Chicago, Illinois.
Received 11/12/07;
revised 12/20/07;
accepted 1/ 7/08.
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Abstract
Materials and Methods
