Background
Optimal treatment plans developed by multidisciplinary teams (MDTs) are essential for high-quality cancer care.1,2 The central position of MDTs in cancer care demands high-quality MDT meetings, including diagnosticians and treatment providers, which can be measured with a key set of quality criteria.3
A crucial criterion of MDT meetings is the availability of relevant and sufficient information about the diagnoses of patients discussed. In MDT meetings, diagnostic information is mainly provided by pathologists and radiologists.4 Research has shown that inadequate pathology and radiology information can cause MDT decision failures.5,6
Traditionally, diagnostic findings were reported with narrative reporting (NR). Currently, multiple studies have indicated that standardized structured reporting (SSR) improves the quality of oncology reporting, particularly the timely, complete, and accurate exchange of diagnostics and treatment information between medical disciplines.7–11 Within pathology, these improvements in reporting resulted in more adequate risk assessments among patients with colorectal cancer, with more patients defined as high-risk receiving adjuvant chemotherapy, leading to improved overall survival (65.0% vs 62.4%).7
Despite the clear benefits of SSR, implementation of pathologists’ reporting of diagnostic information with SSR templates is suboptimal.12 Literature shows both national and international variation in SSR use in pathology.13–17 Pathologists might be encouraged by MDT members (MDTMs) to use the available SSR templates more often to improve pathology reporting quality.
Uptake of SSR is demanding because various medical disciplines and information technology (IT) systems are involved. According to Grol and Wensing,18 a tailored implementation strategy could improve the uptake of an innovation such as SSR. Factors influencing innovation implementation should be explored and used to develop the implementation strategy and tailor it to the factors found.18 Influencing factors of pathologists’ SSR implementation have already been investigated.12 The most important barriers were lack of nuance in SSR, lack of support from MDTMs, and lack of connected IT systems. The most important facilitator was the incorporation of speech ability within SSR templates.12
The next step is to explore which factors influence SSR implementation among MDTMs to develop a combined and targeted implementation strategy. Therefore, this study aimed to qualitatively identify barriers and facilitators that MDTMs encounter in SSR implementation, especially in oncologic pathology reporting in MDT meetings; quantify influencing factors to select the most common ones in a nationwide survey; and analyze the determinants affecting these influencing factors so we could better fit the implementation strategy.
Methods
Study Design
Our multimethod study combined focus groups with a national web-based survey among MDTMs participating in urologic, gynecologic, and gastroenterologic oncology MDT meetings.
Setting
The PALGA Foundation is developing national SSR templates (see supplemental eTable 1, available with this article at JNCCN.org) to improve pathology reporting since 2009.20
MDT meetings take place in different hospital types (nonuniversity, university, specialized). The MDT discusses pathology reports to decide about diagnostics, treatments, and follow-up of patients with cancer. These reports are uploaded to the hospital information system (HIS) as fixed-text documents.
Ethical approval was obtained by the regional review board for human research (CMO Arnhem-Nijmegen dossier number 2018-4124).
Participants and Recruitment
Focus Groups
We organized 4 focus groups with MDTMs to explore barriers and facilitators in SSR implementation: 1 for gynecologic oncology, 1 for urologic oncology, and 2 for lower gastroenterologic oncology.24 We chose these oncology disciplines because almost half of the SSR templates relate to them.20 Invited MDTMs were medical oncologists, pathologists, radiologists, radiation oncologists, gynecologists, gastroenterologic surgeons, gastroenterologists, urologists, nuclear medicine physicians, and nurse practitioners.
We contacted the Netherlands Comprehensive Cancer Organization for support in contacting MDT chairs. Next, we purposively recruited participants from 4 MDT meetings (10–22 members) from different hospital types. We recruited early adapters, middle majority, and laggards of SSR.25
Survey
Analogous to the focus group recruitment, MDTMs operating in gynecologic, urologic, or gastroenterology oncologic care were included in the survey. The survey was distributed through multiple channels between October 26, 2018, and January 16, 2019 (see supplemental eTable 2, available with this article at JNCCN.org). Approached MDTMs were asked to share the survey hyperlink with their MDT comembers and colleagues. For a precise estimation of the barriers and facilitators, we aimed to include 171 participants, based on an assumed SSR implementation of 50%, α=0.05, and predication of estimation of 0.0075.26 Survey completion took 10 to 15 minutes.
Instrument Development and Data Collection
Focus Groups
We developed an interview guide to structure the focus groups. The interview guide was derived from an interview guide used in another study regarding barriers and facilitators in SSR and was assessed by the multidisciplinary project team.12
The interview guide consisted of 4 parts: (1) exploring knowledge regarding SSR, (2) exploring the amount of experience with SSR, (3) asking about the perceived barriers and facilitators with SSR during MDT-meetings, and (4) asking about how to improve SSR-implementation in oncological pathology. Perceived influencing factors were structured with the domains of the implementation science frameworks of Flottorp et al27 and Grol and Wensing18: innovation factors, individual professional factors, social setting factors, organizational factors, and political and legal factors.
Informed consent was signed prior to the focus groups. All focus groups were chaired by a junior researcher assisted by a senior researcher, who audiotaped and took notes. The focus groups lasted 20 to 46 minutes and took place after MDT meetings.
Survey
We developed an eSurvey with LimeSurvey (version 2.06+). This eSurvey was based on theoretical frameworks of Flottorp et al27 and Grol and Wensing,18 results of the focus groups with MDTMs, and results of a focus group with PALGA liaisons. We organized this additional focus group to explore communicational and technical implications of SSR implementation. Most important findings were the various methods of communicating updates, lack of connected IT systems, and the inactive role of medical associations in encouraging SSR implementation.
The survey started with 2 inclusion questions, 7 about individual characteristics, 4 about SSR-usage in the MDT-meeting, and 5 about MDT characteristics. Next, 42 theses were posited about influencing factors of MDTMs with SSR. These were classified according to the implementation science frameworks and were scored on a 4-point Likert scale (1 – strongly disagree to 4 – strongly agree). When relevant, “not applicable” was included. The survey ended with an open-ended question asking for suggestions for improvement of SSR implementation. The survey did not accept unanswered questions. As a pilot, 2 project members and 1 gastroenterology resident independently tested the survey for ease of use and content and it was approved by the multidisciplinary project team. It was validated by calculating Cronbach α per domain.
Data Analysis
Qualitative Analysis
All focus group discussions were transcribed verbatim for content analysis. Two researchers used ATLAS.ti, version 8.3.16 (ATLAS.ti Scientific Software Development) to independently extract barriers and facilitators in SSR implementation from the transcripts. The factors were allocated to the domains of the implementation science framework of Flottorp et al,27 except for the patient domain because patients are not directly involved in SSR implementation. Based on this framework, each encoder established an independent coding tree. To establish one refined coding tree, the researchers discussed both. If there were discrepancies, they discussed coding with each other and, when needed, with the senior researcher until they achieved consensus.
Quantitative Analysis
We used SPSS Statistics, version 25 (IBM Corp) for statistical analyses. We coded missing data including the answer option “not applicable” as such and excluded them from analysis. We performed descriptive statistics to determine the proportions of agreement of MDTMs with the influencing factors of SSR implementation. We considered a barrier or facilitator to be an important factor when more than one-third (33%) of the survey respondents (fully) agreed. To compare differences in agreement on the survey items between pathologists and the other MDTMs, we dichotomized the answer options (fully agree and agree; fully disagree and disagree) to perform chi-square tests. We used Bonferroni correction for multiple testing. To analyze determinants for the influencing factors, positive formulated items were reversed. We performed factor analysis to construct underlying domains. Domains with Cronbach α ≥0.7 were considered valid. We calculated mean scores, wherein a high mean score implied a barrier and a low mean score implied a facilitator. Additionally, characteristics were excluded from analysis when the sample size per group was too small (<5% of total sample size). Respondent characteristics investigated were age (years), experience (years), sex, position, medical discipline, hospital type, familiarity with existence and layout of SSR templates, and MDT type involved. MDT characteristics were SSR use by pathologists of MDT meetings (Table 1); presence, absence, and additional value of pathologists during MDT meetings; central reporting of MDT decisions; and presence of an MDT chair. We used univariate regression analyses to test the relationship between determinants affecting influencing factors for SSR implementation that emerged from the qualitative part of the study and the domain scores. Determinants with P<.20 were selected for multivariate regression analyses. One at the time, nonsignificant determinants were removed from the multivariate model until all determinants were statistically significant (P<.05), based on 2-sided tests. We used content analysis to analyze suggestions for improvement of SSR implementation provided in the open-ended question.
Results
Responses and Characteristics
Focus Groups
A total of 23 MDTMs participated in 4 focus groups: 14 men and 9 women, with an average work experience of 14.3 years (range, 1–31 years). Seven MDTMs participated in the gynecologic focus group, 6 in the urologic focus group, and 5 in each of the 2 lower gastroenterology focus groups (10 total). Five MDTMs (22%) worked in a university hospital, 6 (26%) in a specialized hospital, and 12 (52%) in nonuniversity hospitals.
Survey
Table 1 presents characteristics of survey participants and their MDT meetings. A total of 296 responses were received, with 212 respondents (72%) completing at least 50% of the statements of the survey. One respondent was excluded because of age exceeding the maximum criterion of 68 years, resulting in 211 remaining respondents. The respondents’ average age was 46 years (range, 28–66 years) and their average work experience was 12 years (range, 1–38 years). Of the 211 respondents, 36% were involved in gastroenterologic MDT meetings, 19% in urologic MDT meetings, 16% in gynecologic MDT meetings, and 29% in combined MDT meetings.
Survey Respondents and Their MDT Meetings Characteristics
MDTMs’ Perspective on SSR Implementation
Focus Groups
We identified 28 barriers and 28 facilitators from the focus groups in all domains. In the innovation domain, most influencing factors related to the readability and content of the SSR. In the social setting domain, most influencing factors related particularly to the workflow of pathologists with their MDT comembers. Table 2 shows influencing factors cited in ≥2 focus groups. These influencing factors are illustrated with quotes, which were translated from Dutch to English (supplemental eFigure 1).
Most Frequently Mentioned Barriers and Facilitators of SSR During Focus Group Interviews (n=4)
Survey
Barriers and facilitators were found for all domains. The barrier of external hospitals not using SSR was excluded because of too many missing values (52%). Cronbach α ranged from 0.7 to 0.8 (Table 3). Specifically, significant (P<.05) differences in perceived barriers and facilitators within these domains between pathologists and other MDTMs are shown in supplemental eTable 3.
Determinant Analyses
Innovation Factors
Various influencing factors related to the compatibility, credibility, and observability of SSR were found in the innovation domain (Figure 1). Main obstacles for MDTMs with SSR were difficulties with capturing nuances (66%; n=167), caused by a lack of use of the free text within SSR templates among pathologists, and with the formulation of the conclusion (43%; n=167). Another main barrier mentioned was lack of transparency regarding responsibilities for design of the SSR templates, inclusion of additional features, and implementation (50%; n=211). Moreover, MDTMs were unaware of an SSR template working group evaluating SSR templates (38%; n=211). Less than 25% of MDTMs stated that SSR lacked compliance with MDTMs’ information needs, although 37% (n=163) lacked information about regional arrangements or clinical trials (35%; n=164). Some mentioned facilitators of SSR compared with NR, including improvement of uniformity (98%; n=167), completeness (90%; n=166), and data usage for research and quality improvement purposes (90%; n=163). Increasing MDTMs’ involvement in the development of SSR templates (57%; n=211) and including early pathology research findings in SSR templates (55%; n=211) were other facilitators.
MDTM answers to theses about the social setting factors, organizational factors, and political and legal factors of SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
MDTM answers to theses about the social setting factors, organizational factors, and political and legal factors of SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
MDTM answers to theses about the social setting factors, organizational factors, and political and legal factors of SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
Individual Professional Factors
Figure 1 provides results of the individual professional factors. Many MDTMs had a positive attitude regarding SSR and called for increased SSR use by pathologists (84%; n=211). Less than 25% of the MDTMs were unaware of the additional value of SSR, with a difference between pathologists and other MDTMs (5% vs 28%) (supplemental eTable 3).
Social Setting Factors
In Figure 2, several barriers are displayed regarding communication and referral processes between pathologists and other MDTMs. MDTMs reported lack of communication on updates and new SSR templates from pathologists as a barrier (45%; n=131). Moreover, MDTMs inability to make correct treatment decisions due to a lack of nuances in SSR (45%; n=150) reported. Thus, MDTMs were afraid to overlook nuances in SSR because it led to black-and-white conclusions (35%; n=150).
MDTM illustrative quotes about barriers and facilitators in SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
MDTM illustrative quotes about barriers and facilitators in SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
MDTM illustrative quotes about barriers and facilitators in SSR.
Abbreviations: MDT, multidisciplinary team meeting; MDTM, multidisciplinary team member; SSR, standardized structured reporting.
Citation: Journal of the National Comprehensive Cancer Network 19, 13; 10.6004/jnccn.2021.7002
MDTMs also reported facilitators in communication, referral, and team processes. SSR use resulted in improved pathology reports (88%; n=134) and saved time (80%; n=124). Furthermore, respondents felt that both regional MDTMs (90%; n=179) and MDT chairs (81%; n=179) should encourage pathologists to start using SSR, and that local MDTMs could encourage other pathologists by explaining the additional value of SSR (74%; n=179).
Organizational Factors
MDTMs mentioned several incentives of SSR implementation (Figure 2). Among these, respondents suggested that PALGA could improve their feedback process of SSR templates’ content, for example by analyzing information entered in the open text fields (78%; n=174); medical professional associations could improve their promotion of SSR use in pathology (71%; n=174); and inclusion of mandatory SSR use in both the audit criteria of the national pathology organization (68%; n=179) and quality of care institutes (68%; n=179) could serve as nonfinancial incentives to increase SSR use. These incentives were less often perceived as facilitators by pathologists (47%–49%) compared with the other MDTMs (77%) (supplemental eTable 3).
Political and Legal Factors
Figure 2 also shows results of political and legal factors. Most respondents agreed that all national oncology guidelines should recommend SSR use in pathology (80%; n=174), and 61% (n=174) agreed that SSR use should be mandatory in these guidelines, with a difference between pathologists (45%) compared with other MDTMs (68%).
Improvements for SSR
Most frequently yielded improvements to SSR implementation by MDTMs were including mandatory use of SSR in oncologic guidelines, improving the readability of SSR, improving cooperation of MDTMs in the development process, improving the ability of providing nuances in SSR templates, and regularly mentioning the benefits of SSR to encourage use.
Determinants of Barriers and Facilitators in SSR Implementation
Mean scores of the domains were >1.8 (range, 1–4) (Table 3). Univariate regression analyses resulted in multiple determinants for all domains except the social setting. After multivariate regression analyses (Table 3), medical discipline and MDT type remained significant determinants for all 4 domains. Concerning medical discipline, pathologists were less in favor of organizational incentives and regulations regarding SSR implementation compared with oncology-treating clinicians. Regarding MDT type, gastroenterologic oncology MDTMs had a more positive attitude toward SSR than gynecologic oncology MDTMs. When MDTMs knew SSR was used by pathologists, they were more in favor of especially political and legal facilitators promoting SSR use. Age was a determinant regarding political and legal factors: when age increased, pathologists had a more positive view regarding regulations for encouraging SSR use.
Discussion
This multimethod study provides an in-depth view on MDTMs’ experiences with SSR explored in the domains of the frameworks of Flottorp et al27 and Grol and Wensing,18 and indicates several barriers and facilitators in SSR implementation. Most important barriers related to the innovation domain were difficulties with readability: extracting doubts of pathologists from SSR and formulation of the automated conclusion. A number of elements were lacking, including transparency in the development and feedback process and local information within SSR. In the social setting there was a lack of SSR-related information exchange between pathologists and MDTMs. Most important facilitators related to almost all domains, as in the innovation domain, the completeness of SSR. Other important facilitators were development of an effective feedback system in the organization domain, and were related to political and legal factors, such as establishing a policy among medical professional associations encouraging SSR use and increasing recommendations for SSR use within guidelines. Oncology-treating clinicians were more in favor of incentives and regulations regarding encouragement of SSR use than pathologists.
Readability of SSR was considered a substantial obstacle to SSR implementation in MDT settings. From the template perspective, according to Nakhleh,28 the availability to add urgent information is an important factor in effective pathology communication and reporting when using SSR. However, a recent review stated that SSR should be sufficiently self-explanatory and additional information should be provided in the additional text field.29 Renshaw et al30 already suggested the need for additional study on the use of different formats and use of available free text within SSR templates. A promising development is the integration of speech recognition within SSR templates, which may encourage pathologists’ use of these free text fields.12 Future research could be focused on testing speech recognition software within SSR templates and determining the effect on SSR implementation.
From the report view, although graphic representation of data within SSR may also improve readability,28 the layout of SSR currently depends on the type of HIS used during MDT meetings. Use of multiple HIS and laboratory information systems is a known obstacle in SSR implementation12,30,31 and highlights the conclusion of Lankshear et al,32 who emphasized the importance of technologic considerations in SSR’s usability and design. When connecting data resources to improve multidisciplinary exchange of diagnostic findings, it will be essential to review the readability and layout of the output. Moreover, regarding the conclusion formulation, it is already possible to adjust the automatic generated conclusion or to draft one from scratch. However, this depends on the laboratory setting and effort of the pathologist to adapt or draft this improved version of the conclusion. Several suggestions are made by Renshaw et al30 to improve readability of pathology reports established by the use of SSR templates. Future research could be aimed at finding a general, instead of a local, solution to improve the generated conclusion.
Lack of transparency and involvement in development and feedback processes, and improved alignment of information provision between pathologists and other MDTMs were important factors influencing MDTMs’ perspectives regarding SSR. Lack of stakeholder involvement, such as by clinicians, was an important obstacle to SSR implementation in Canada.33 In the United States, pathologists can customize the SSR templates developed by the College of American Pathologists to improve clinicians’ satisfaction with SSR. Consequently, addendums for additionally requested information have increased significantly. Web-based technology is used to easily update templates and to keep them customized after updates. However, pathology laboratories must be aware of interferences in case of national updates, which can cause technical challenges locally.34 Therefore, adding customized questions to SSR templates is not possible in the Netherlands. To keep SSR template content up to date and thus continue to comply with the MDTMs’ information need, it will be essential to collect feedback on SSR template content. To collect feedback from medical device users (eg, postmarket surveillance) will also be an important criterion of the new European regulation for medical devices.35 Therefore, future research could focus on the development of a structured, transparent, and reliable feedback procedure, aiming to improve the alignment of SSR output with MDTMs’ needs.
Related studies exploring the perspectives of treating clinicians receiving SSR reported mainly positive feedback.14,15,32,36 Results about facilitators of SSR implementation in our study, such as improved completeness, are in line with the findings of Lankshear et al.32 Additionally, Lankshear et al32 found treating physicians were more satisfied with the overall SSR process compared with pathologists. This may explain why MDTMs in our study had a more positive attitude regarding incentives and mandatory regulations of SSR use compared with pathologists, because Dutch pathologists also encounter obstacles in implementing SSR.12 This indicates the need for implementation tools to overcome the perceived barriers of SSR among pathologists.
Strengths of this study are that the perspectives of MDTMs from all oncology-related disciplines were involved in the analysis, and a broad and in-depth view of SSR implementation was gained in a structured manner via multimethod.
This study also has limitations. First, we could not calculate a survey response rate because of privacy regulations; we were not allowed to invite MDTMs individually. Furthermore, national data on the number of MDTMs, and more specifically, numbers of MDTMs exposed to the survey, are lacking. Because SSR is more developed within pathology compared with other disciplines involved in MDT meetings, it is possible that individuals who did not respond were less familiar with SSR. However, by collecting data through a wide variety of channels and encouraging receivers of the survey to share the link with their MDT comembers and colleagues, we attempted to include as many MDTMs as possible and to minimize selection bias. As the study was focused on SSR in pathology, more pathologists were involved. Therefore, we added an additional analysis comparing pathologists with the other MDTMs, showing the differences in experienced barriers and facilitators of SSR. Furthermore, by incorporating the “not applicable” answer option, people not using SSR were also able to complete the survey and were able to skip questions for which additional knowledge about SSR was needed. Second, this study was conducted in the Netherlands. However, these findings can be translated to settings in which a national or regional organization is present to coordinate SSR implementation.
Conclusions
Although MDTMs benefit from SSR use by pathologists, barriers related to SSR implementation were perceived. The most important influencing factors for SSR implementation must be used to develop and execute strategies in close collaboration with stakeholders to improve SSR implementation in pathology, both for pathologists as well as other MDTMs.
Acknowledgments
We thank the participants of the focus group and the respondents of the survey for their contribution to this study. We thank Angelique Schlief for her assistance regarding data collection and data analysis and Reinier Akkermans for his assistance regarding data analysis.
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