Introduction

The purpose of the U54 Partnerships to Advance Cancer Health Equity (PACHE) mechanism is to develop and maintain comprehensive, long-term, and mutually beneficial partnerships between institutions serving underserved health disparity populations, underrepresented students (ISUPSs), and national cancer institution (NCI)–designated cancer centers. The intent of partnership programs is to foster and support collaborations to develop stronger cancer programs that promote an understanding of how cancer health disparities disproportionately affect racial and ethnic minorities and socioeconomically disadvantaged populations. Partnership institutions are expected to (1) increase the cancer research and cancer research education capacity of ISUPSs; (2) increase the number of underrepresented minority (URM) students and investigators engaged in cancer research; (3) improve cancer center effectiveness in developing and sustaining research programs focused on cancer health disparities; (4) increase the number of investigators and students conducting cancer health disparities research; and (5) develop and implement cancer-related activities that benefit the surrounding underserved communities [1]. What is known about the impact of PACHE can be assessed through varied evaluative methods. Describing the scope of center publications also offers one type of insight. With that idea, and based on Behar-Horenstein, Horenstein and Richey’s research [2], we conducted a scoping review of all publications available in NIH RePORT across the funded PACHE centers [2].

As required by the National Institute of Health (NIH), annual self-evaluation is conducted through the submission of progress reports from the individual projects under the program funding mechanism. Each program monitors and reports the degree to which they have attained proposed objectives. Researchers may assess the quality of programs using outcome measures or evidence of impact. Program outcome measures may include (1) reporting the publications co-authors by trainees and mentors; (2) reporting the number of trainees who matriculate, continue in academic cancer-related research careers, or co-author publications, (3) specifying the number and list of presentations/meetings that include trainees; (4) reporting the number of program graduates who receive R01 or career development awards; or (5) documenting the number who hold positions as professors or leadership roles on NCI committees; or (6) describing the quality of mentoring, among others. Concordant with evaluation metrics focused on scholarly work, the purposes of this study were to utilize the collective set of PACHE publications to (1) determine the frequency of publications by longevity across funded programs; (2) report the frequency of studies focused on cancer health disparities; (3) determine the proportion of ISUPS co-authors; (4) determine the proportion of ISUPS lead authors; and (5) categorize the scope of studies by commonalities in their reported purposes.

Methods

Using secondary data from the NIH RePORT, we conducted a document review of all publications that were produced across the funded U54 PACHE centers as of July 2019 (Fig. 1).

Fig. 1
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Process of article identification

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Overall, the 16 PACHE programs produced 963 publications (see Table 1), ranging from 5 to 145. Criteria for inclusion were evidence-based studies that presented quantitative or qualitative results and also included a statement of purpose, an overview of methods and results, and a discussion/conclusion section. Papers that did not meet inclusion criteria such as position papers and duplications were excluded from this review. This database was developed during the third week of July 2019. Thus, it is limited solely to those publications that were accessible on the NIH Research Portfolio Online Reporting Tools (RePORT) [3].

Table 1 NIH RePORT publications by center, longevity, cancer health disparities, and ISUPS co- and lead authors by n/% of initial and final database
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The second author compiled the database. Next, the first and third authors read each of the 963 articles. We created a spreadsheet and listed each publication by each institution within the center (see Appendix A). We identified the ISUPU institutions (see Table 1). To determine if a publication was focused on cancer health disparities (CHD), first we did a keyword search for “cancer” and “health disparities” or “cancer health disparities.” Articles that listed these keywords were classified as CHD. As a validation check, next we reviewed each article; read the abstract, introduction, discussion, and conclusion; and searched for the following keywords: “cancer” and “health disparities,” “cancer health disparities” or “minority” or “minorities.” If an article did not mention cancer health disparities but was clearly focused on cancer and the health of a specific minority population, then we counted it as a cancer health disparities article. We reviewed the list of authors within each publication and noted whether each name was or was not affiliated with an ISUPS. We recorded the frequency of ISUPS first or co-first authors and the year of publication for each center. We recorded the frequency of ISUPS lead authors and year of publication for each center. Next, we reviewed the study purpose of each publications and developed brief descriptions of its purpose, which were identified as an initial category. Next, we reviewed those initial categories, to sort, group, and classify articles by commonalities in their purpose, which were designated as the final categories (see Table 2).

Table 2 Initial and final publication categories
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For example, articles focused on biomarkers and diagnosis, cancer diagnosis and radiologic tools, cancer treatment, or cancer screening were classified as cancer diagnosis, screening, treatment, and risk factor. Studies focused on the biological basis for cancer, cell proliferation were designated as mechanistic. Studies in which the focus was psycho-social factors, biology, and cancer survival, psycho-social factors and cancer survival, psycho-social factors and suicidality, or psycho-social factors, intervention, and cancer survival were classified as impact of interventions on health promotion, prevention, and quality of life. Case-control cohort studies or publications in which instrument development was the focus were designated as epidemiological/survey outcomes. Studies in which the effectiveness of training and program impact were described were classified as Educational outcomes. Conceptual definitions for each category were developed (see Table 3).

Table 3 Categories and conceptual themes by frequencya
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Results

In this section, we report the number of publications by center longevity, the frequency of cancer health disparities studies, the proportion of ISUPS co-authored studies, and ISUPS lead-authored studies, and categorization of studies.

Publications by Center Longevity

The 16 PACHE programs described in this study have been funded for 2–18 years, on average 9.5 years, median 10.5, and mode 11. Six centers (University of Illinois Chicago, Northeastern Univ, Northwestern University Lurie CC; Tennessee State Univ, Meharry Medical College, Vanderbilt Ingram CC; Ponce Health Sciences Univ, Moffitt Cancer Center; South Carolina State Univ, Medical University of SC Hollings CC; Temple Univ Fox Chase CCC, Hunter College; and Florida A&M Univ, Univ Florida, Univ Southern California) have been funded for less than 10 years, while the remainder (Arizona CC, Northern Arizona University; San Diego State, UC San Diego Moores CC; Drew University, UCLA Jonsonn CC; New Mexico State University Las Cruces, Fred Hutchinson Cancer Research Center; U Mass Boston, Harvard Dana Farber Cancer Institute; City College of NY, Memorial Sloan Kettering CC; Tuskegee University, Morehouse School of Medicine, UABCC; University of Puerto Rico CC, MD Anderson; North Carolina Central Univ, UNC Lineberger CC; and University of Guam, University of Hawaii CC) has been funded for 10 or more years.

The total number of publications across centers ranged from 5 to 145, while the average number of publications per year ranged from 2.5 to 12.4 (see Table 1; see Fig. 2). Three partnerships (Tennessee State University/Meharry Medical College/Vanderbilt Ingram CC, 9 years; Tuskegee University/Morehouse School of Medicine/UABCC, 15 years; and University of Illinois Chicago/Northeastern Univ/Northwestern University Lurie CC, 5 years) averaged more than 10 publications per year irrespective of longevity, with 13.22, 8.73, and 12.40, respectively.

Fig. 2
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Average number of publications by longevity across PACHE center #

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Other centers with funding of 10 or more years (Arizona CC/Northern Arizona University, 11 years; San Diego State/UC San Diego Moores CC, 12 years; Drew University/UCLA Jonsonn, 11 years; New Mexico State University Las Cruces/Fred Hutchinson Cancer Research Center, 13 years; U Mass Boston/Harvard Dana Farber Cancer Institute, 10 years; City College of NY/Memorial Sloan Kettering CC, 12 years; University of Puerto Rico /MD Anderson, 18 years; North Carolina Central Univ/UNC Lineberger CC, 10 years; and University of Guam/University of Hawaii CC, 11 years, annually averaged 2.73, 4.25, 5.18, 2.15, 4.90, 7.67, 5.33, 5.80, and 2.45 publications, respectively. One other center with funding between five and less than 10 years (Ponce Health Sciences Univ/Moffitt Cancer Center, 8 years) averaged 6.50 publications per year. Centers with less than 5 years of funding (South Carolina State Univ/Medical University of SC Hollings CC, 3 years; Temple Univ Fox Chase CC/Hunter College, 2 years; Florida A&M Univ/Univ Florida/Univ Southern California, 2 years) published 2.33, 3.50, and 2.50 papers, respectively.

Cancer Health Disparities Studies

Overall, 167 (19%) of studies focused on cancer health disparities (see Table 1).

ISUPS Co-authors

Six hundred twenty-four (72%) of the publications included an ISUPS co-author (see Table 1). Center 8 and 10 had the largest number of ISUPS co-authors. Looking at frequency by year, the largest number of co-authored publications occurred in 2017 (149), 2018 (142), 2016 (124), 2015 (111), and 2019 (88) (see Fig. 3).

Fig. 3
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Number of ISUPS co-authors by year and center #

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ISUPS Lead Authors

ISUPS lead authors were seen in 415 (48%) of the publications. (see Table 1). Looking at frequency by year, the largest number of lead-authored publications occurred in 2017 (100), 2018 (89), 2015 (79), 2016 (76), and 2019 (66) (see Fig. 4).

Fig. 4
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Number of ISUPU lead authored publications by year and center #

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Categorization of the Studies

Categories and conceptual themes along with corresponding representative publications are shown in Table 3. The focus of 53 publications (6.07%) was on (cancer diagnosis, screening, treatment, and risk factors). Purposes of publications in this category included the effectiveness of teamwork or treatment efficacy, radiologic tools, biomarkers, and diagnosis or risks associated with developing cancer. Five hundred and two (57.5%) studies focused on mechanisms relating to the biological aspects of cancer, novel treatments, and cell proliferation and were designated as mechanistic. One hundred and eighty-eight (21.53%) focused broadly on the impact of interventions on health promotion, prevention, and quality of life. In these studies, researchers explored the effect of psychosocial factors and interventions on cancer survival; measured the impact of behavioral interventions towards health promotion, vaccine practices, and prevention; measured screening attitudes; and assessed care-seeking experiences. Forty-nine (5.62%) studies were related to educational outcomes. Researchers in these studies explored the effectiveness and career outcomes among training program participants or assessed educational materials and interventions. The remaining 81 (9.28%) studies were classified as epidemiological/survey outcomes. In these studies, researchers reported comparative outcomes among groups by casual attributes or reported the outcomes of surveys designed to measure behaviors, attitudes, and experiences.

Discussion

In this study, we analyzed 868 evidence-based research publications accessible in NIH RePORT that met criteria and were produced across the 16 funded U54 PACHE programs. Intuitively, it would seem that centers funded for more years would have a proportionately higher number of publications. Our findings suggest that this was not always the case.

Less than one fifth of studies focused on cancer health disparities (CHD). Since the primary purpose of PACHE centers is CHD research, increasing the frequency of CHD-focused publications is advised.

The proportion of papers co-authored by ISUPS investigators was markedly higher, slightly less than three quarters in comparison with papers led by NCI-designated cancer centers, which were less than half. Given that a strong purpose of PACHE centers is to promote research at the ISUPS, the frequency of ISUPS co-authored papers suggests that PACHE is, in part, meeting its goal of supporting ISUPS researchers. The lower proportion of ISUPS first- or co-first authored papers may suggest a gap in productivity. However, there is a caveat. Although it is expected that PACHE-funded research projects need to focus on cancer health disparities, the same expectation is not true for all underrepresented minority trainees, who may also contribute to center productivity. Per the guidelines of the PACHE centers, some trainees have not worked on cancer health disparities to fulfill the mission of the center. For example, a minority ESI who is a member of a PACHE center may be working on a basic science project, or any other project, not focused on disparities and may cite the center because they received support from it for their career development, yet the paper is not on cancer health disparities. However, if the ESI is publishing and their career advancing, then the PACHE center’s mission of increasing the workforce of underrepresented minority scientists is being upheld. In future studies, researchers might wish to explore distinctions between the number of papers led by ESIs in comparison with papers led by PACHE center core/project leaders and explore the number of ESI-led papers who cite the center because they received support from it for their career development, by those papers that were not on cancer health disparities.

We classified studies to offer insight into the types of foci among these publications. The majority of publications were mechanistic. Less than one quarter focused on the impact of interventions on health promotion, prevention, and quality of life; less than one tenth focused on epidemiological/survey outcome studies. Slightly more than one twentieth (1/20) focused on cancer diagnosis, screening, treatment, and risk factors, while even less focused on educational outcomes. To align with the PACHE mission, we suggest increasing the number of studies focused on cancer diagnosis, screening, treatment, and risk factors and the impact of interventions on health promotion, prevention, and quality of life. Findings related to the classification of publications are similar to a previous review conducted using of R25 publications between 2016 and 2019 [2]. Three of the PACHE purposes explicitly focus on cancer research education capacity, increasing the number of URMs engaged in cancer research and improving cancer center effectiveness in developing and sustaining research programs focused on cancer health disparities. Thus, we recommend increasing the number of future studies that focus on the quality and effectiveness of training.

We acknowledge use of NIH RePORT as a limitation since citations potentially discoverable in other databases (i.e., PubMed, Google Scholar), were not utilized. We acknowledge the limitations of a scoping review as it represents a single, albeit indirect, way to assess the impact of the PACHE programs. Also, not all programs were funded for the same number of years. Thus, proportionally some centers have a large number of publications compared with centers that have been funded for less than 5 years. All NIH RePORT publications were included in the database irrespective of the center’s funding duration. Cited studies are inclusive through the 3rd week of July 2019, which is six to 10 weeks before the end of the funding period depending on whether a center’s funding begins in August or September. We acknowledge that there is a delay between publication and the paper appearing in NIH RePORT, although the length of delay is beyond the scope of our analyses. We acknowledge rounding up to the next year as study limitation. To avoid biases in interpretation, we encourage the reader to view the results of our study with this in mind. Additionally, in this study, ISUPS “leading” a paper refers exclusively to someone is a first or co-first author. Despite these limitations, study findings revealed important insights.

This paper presents a scoping review focused on evaluating the productivity of U54 PACHE centers, as an indirect way to assess the impact of U54 PACHE programs. The findings offer useful approach to evaluate the impact of this funding program mechanism. Presumably, the audience of this paper are current members of U54 PACHE centers. We postulated that by evaluating manuscript productivity, we could gauge whether the U54 PACHE program is achieving its goal of increasing cancer research and capacity of ISUPS by increasing the pool of investigators conducting cancer health disparities research.

Conclusions

The federal cancer science agency often uses research publications as one indicator for determining scientific progress towards the objectives of funded programs [4]. Determining the merit of cancer-related publications to scientific discoveries can be assessed through varied methods such as bibliometrics, reviews, or quantitative syntheses. Another approach is to describe the nature of a collective body of work is a scoping review. A scoping review is undertaken to systematically identify key concepts or sources of evidence in a body of literature. It can be used to quantify the frequency of work as well as identify commonalities in topics and study purposes. In this study, we report the number of papers co-authored and led by ISUPS investigators in comparison with papers led by NCI-designated cancer centers. We also report whether publications are contributing to cancer health disparities research. The findings showed the gaps in productivity. In the future, researchers wish to use these findings as a baseline to assess changes in the frequency of papers co-authored and led by ISUPS investigators, to determine changes in the number of studies focused on cancer health disparities research studies, and to assess the proportional scope of studies centered on cancer diagnosis, screening, treatment, and risk factors, the impact of interventions on health promotion, prevention, and quality of life, and educational outcomes. Developing an understanding of the type of cancer publications disseminated offers researchers an opportunity to evaluate past scientific progress and to identify prospective projects.