A Web Screening on Training Initiatives in Cancer Genomics for Healthcare Professionals

The disruptive advances in genomics contributed to achieve higher levels of precision in the diagnosis and treatment of cancer. This scientific advance entails the need for greater literacy for all healthcare professionals. Our study summarizes the training initiatives conducted worldwide in cancer genomics field for healthcare professionals. We conducted a web search of the training initiatives aimed at improving healthcare professionals’ literacy in cancer genomics undertaken worldwide by using two search engines (Google and Bing) in English language and conducted from 2003 to 2021. A total of 85,649 initiatives were identified. After the screening process, 36 items were included. The majority of training programs were organized in the United States (47%) and in the United Kingdom (28%). Most of the initiatives were conducted in the last five years (83%) by universities (30%) and as web-based modalities (80%). In front of the technological advances in genomics, education in cancer genomics remains fundamental. Our results may contribute to provide an update on the development of educational programs to build a skilled and appropriately trained genomics health workforce in the future.


Introduction
Cancer is the leading cause of death worldwide and a major public health issue [1]. The rampant discovery of more and more genes associated with disease risk and the rapid advancement of genomic technologies led to the wide application of genomics into clinical practice [2]. Genomics enhance the understanding of human diseases, accelerate diagnosis for patients and provide increasing opportunities to tailor prevention and treatment [3]. In clinical practice, genomics has been widely used to guide the management of cancer patients by choosing a specific treatment approach based on the genetic drivers detected in the tumour rather than its histologic classification, decreasing chemotherapy toxicity and failure [4].
Nevertheless, the rapid expansion of genomics research still engenders doubt, skepticism, and challenges for healthcare professionals to fully understand and apply genomics into everyday practice. As such, knowledge translation of genomics into oncology care is a slow, thoughtful, and complex process. The increased accessibility of genomics technology is changing the educational requirements of healthcare professionals [5]. However, there is still non-conclusive evidence whether the education and training programs are adequate for the implementation of genomics medicine [6]. It was reported that healthcare professionals' knowledge, beyond the current and projected workforce of genetic counsellors and medical geneticists, are not adequate to meet the growing demand for genomics services [6], especially in the oncology field. A recent systematic review on physicians' knowledge in clinical cancer genomics reported limited levels of genomics literacy, which varied by specialty, type of genomics services, and years of practice [7]. If physicians do not understand the nature of genomics and how it applies to clinical practice, they may not believe the impact of such advancements in clinical practice [7]. Therefore, an appropriate and effective implementation of cancer genomics requires an adequate genomics literacy of healthcare professionals, as well as implementation of well-defined genomics core competencies [8]. In this regard, several scientific societies, universities, or research centres designed and developed initiatives to train and educate healthcare professionals in this topic. In particular, cancer genomics education is a focus of a recent European project, entitled the Innovative Partnership for Action against Cancer (iPAAC) Joint Action (JA). This JA aims to develop innovative approaches to advances in cancer control, addressing cancer prevention, approaches to the use of genomics in cancer control and care, cancer information and registries, improvements and challenges in cancer care, innovative cancer treatments, and the governance of integrated cancer control [9]. Within this JA, we provided a comprehensive map of training initiatives conducted in cancer genomics field and directed to healthcare professionals at a global level.

Search Strategy
We conducted a web search of online and in-person training initiatives carried out worldwide and aimed at educating healthcare professionals in the field of cancer genomics. The search was conducted using the three most used web search engines: Google, Bing, and DuckDuckGo [10]. The search was limited to initiatives publicly available in English language, from January 2003 to October 2021. This time limit was decided with the aim at identifying any possible initiative conducted after the completion of the Human Genome Project in 2003, as that was the starting point of a new era in scientific research and medical practice omics sciences related.
We used the following terms for the web search in Google using its "advanced search" application: "cancer genomics" AND "education initiatives" AND "training" AND "course" AND "healthcare professionals". This search strategy was also used as the template for the search in Bing.
In the three search engines, after the launch of the search query, only the results in the category "All" were considered and no additional limits or filters were applied.
Two researchers (I.H. and F.B.) independently screened the identified records by title, description, and summary, whenever available, in order to identify the eligible initiatives. A database of relevant records from the screening stage was created using an Excel spreadsheet, and full texts or full web pages of these records were further assessed according to our inclusion criteria by two researchers (I.H. and F.B.) independently. Additionally, we performed a manually search on the initiatives that were suggested or mentioned in these webpages. The initiatives that satisfied the eligibility criteria were selected for inclusion in this article. Any discrepancy was solved by discussion or by the involvement of a third researcher (G.E.C.).

Eligibility Criteria
The eligibility criteria were formulated according to the PI/ECOS framework [11,12] Education or training initiatives on cancer genomics for healthcare professionals that reported information on the topic, objective, content, and target were considered eligible for inclusion. Initiatives addressing university or master students and degree courses promoted by universities were excluded.

Data Extraction and Synthesis of Results
For each included initiative, two researchers (I.H., F.B.) independently extracted the following data: name of initiative/project, year, country, organizer, topic, target, type of initiative, objective, and number of modules, if available. Any discrepancies in data extraction were solved by discussion or with the involvement of a third researcher (G.E.C.). The results were grouped in two categories: European and non-European initiatives. For each category, the results were summarized through a narrative descriptive synthesis [13], based on the available data extracted.

European Initiatives
In Europe, we identified 15 initiatives, which were conducted in the UK, Austria, Switzerland, Italy, and Germany (Table 1). Twelve initiatives were conducted online, whereas three were in-person attendance. The UK was the country with the largest number of the training initiatives (67%) on cancer genomics. Starting from 2014, the Genomic Education Program, organized by Health Education England, aimed to prepare the National Health Service (NHS) workforce to deliver the new England-wide NHS Genomic Medicine Service and to support the completion of the landmark 100,000 Genomes Project by providing annual online education opportunities in genomics, with a specific focus on genomics applications in cancer care in the module "Tumor assessment in the genomic era" [14,[50][51][52][53][54]. In 2014, the European Bioinformatics Institute organized a workshop for post-doctoral researchers to introduce cancer genomics, analytical methods for detection of genome rearrangements, network analysis, and RNA-sequencing data analysis [15]. From 2014 to 2020, the Golden Helix Foundation organized several Summer Schools on genomics medicine and medical informatics for biomedical scientists and healthcare providers, also addressing cancer genomics [16,[55][56][57][58]. The Guy's and St Thomas' NHS Foundation Trust, since 2019 and for three consecutive years, conducted online courses for healthcare professionals working in cancer care on the cancer genetic counselling, approaches to genetic testing, and the management of hereditary cancers [17,59,60].
Starting from the collaboration with Guy's and St Thomas' NHS Foundation Trust, the Medics.Academy developed a four-hour online courses available in Europe on cancer genomics and precision oncology [18].
The EMBL-EBI Training, which is part of the ELIXIR infrastructure, ran a Cancer Genomics course in May 2021. The course was made available online to be accessible any time. It is composed of pre-recorded lectures, presentations, and practical sessions to learn about cancer genomics and enhance skills in the analysis of cancer genomics data [19].

European Initiatives
In Europe, we identified 15 initiatives, which were conducted in the UK, Austria, Switzerland, Italy, and Germany (Table 1). Twelve initiatives were conducted online, whereas three were in-person attendance. The UK was the country with the largest number of the training initiatives (67%) on cancer genomics. Starting from 2014, the Genomic Education Program, organized by Health Education England, aimed to prepare the National Health Service (NHS) workforce to deliver the new England-wide NHS Genomic Medicine Service and to support the completion of the landmark 100,000 Genomes Project by providing annual online education opportunities in genomics, with a specific focus on genomics applications in cancer care in the module "Tumor assessment in the genomic era" [14,[50][51][52][53][54]. In 2014, the European Bioinformatics Institute organized a workshop for post-doctoral researchers to introduce cancer genomics, analytical methods for detection of genome rearrangements, network analysis, and RNA-sequencing data analysis [15]. From 2014 to 2020, the Golden Helix Foundation organized several Summer Schools on genomics medicine and medical informatics for biomedical scientists and healthcare providers, also addressing cancer genomics [16,[55][56][57][58]. The Guy's and St Thomas' NHS Foundation Trust, since 2019 and for three consecutive years, conducted online courses for healthcare professionals working in cancer care on the cancer genetic counselling, approaches to genetic testing, and the management of hereditary cancers [17,59,60]. The NHS Health Education England launched a Massive Open Online Course (MOOC) in 2021 titled "Whole Genome Sequencing-Decoding the Language of Life and Health" on genome sequencing, DNA replication, next-generation sequencing, risk assessment, and data sharing directed at healthcare professionals [14]. Other MOOCs were organized in 2020-2021 by several universities on cancer genetics and pharmacogenetics [20]; epigenetics and cancer diagnosis [21]; genomics data and ethical, legal, and social related-issues; genomics in clinical practice; counselling; next-genomics sequencing; and genome-wide association studies [22,[61][62][63]. The Royal College of General Practitioners organized webinars regarding the impact of genomics in primary care and basic concepts on familial cancer, rare diseases, antenatal care, testing, and ethical issues [23].
In Austria, within the Corbel Project, a series of webinars were conducted on cancer genomics research and clinical data for data managers, researchers, and postdocs involved in clinical, translational, and biomedical research [24,64]. Precision Medicine was the focus of the MOOC organized in 2017 in Germany for researchers, policy administrators, and life science professionals [25] and of the MOOC conducted in 2021 in Switzerland, for primary care physicians, cancer and non-communicable diseases specialists, public health policy and decision makers, biomedical researchers, and drug developers [26]. Recently in Italy, a multi-disciplinary Delphi method of experts in the field defined the core competencies on cancer genomics for physicians and nurses, which were grouped into three categories: knowledge, attitudes, and practical abilities [8]. The defined competencies were then used to elaborate a distance-learning course in English language at the European level, entitled "Oncogenomics for health professionals". This online course was aimed at improving the knowledge, attitude, and practice of physicians on the fundamental principles of genetics and on the major clinical applications of genomics technologies in oncology, based on the most recent scientific evidence [27].
In addition to these initiatives at national level, the European Society of Medical Oncology organized in 2019 a workshop for its members regarding hereditary cancer syndromes, susceptibility to develop cancer, and clinical management [28,65].
In the USA, the Cancer Genomic Education Program, through different annual training modalities, aimed to equip primary care physicians and other healthcare professionals with the necessary knowledge and skills to help patients understand their personal cancer risk [42,[67][68][69]. The National Cancer Institute (NCI) and The National Institutes of Health (NIH) organized the Translational Research in Oncology Course from 2003 to 2019, designed to provide an overview of cancer biology, treatment, epidemiology, mechanisms, and the identification of novel molecular targets [29,70]. Additionally, the NIH created the Cancer Information Summaries on a wide range of cancer topics for oncologist and clinicians and, in 2013, funded the IGNITE (Implementing GeNomics In pracTicE) Network to support the development, investigation, and dissemination of the genomic medicine practice model. Within the project, the IGNITE Toolbox was created as an open source tool of peer-reviewed genomics medicine implementation. For clinicians, this tool provides background information, benefits of adopting genomics medicine in patient care, and key challenges and stakeholders to consider. For researchers, it provides sample consent forms, surveys, data dictionaries, and other resources to help the implementation of science research in genomics medicine [39,40,[71][72][73][74][75][76][77][78][79][80].
In 2010, the Training Residents in Genomics (TRIG) Working Group was formed, aiming to develop teaching tools and promote genomics education to pathology residents. Supported by grants from the NCI, genomic workshops and courses, online modules, and the Universal Genomics Instructor Handbook and Toolkit were provided to professionals of several specialties as well, such as neurology, ophthalmology, oncology, and cardiology [32,[81][82][83].
In 2013-2014, the National Human Genome Research Institute (NHGRI) organized a series of lectures about genomics in medicine, focusing also on the application of genomics in cancer care and prevention, and created a free online repository called the "Genetics/Genomics Competency Center", which consists of more than 500 genomics educational materials that are continuous updated [31,[84][85][86][87][88][89][90][91][92].
The American Society of Clinical Oncology (ASCO) created the Genetics Toolkit in 2015 with the objective to provide oncologists with the necessary tools and resources that will assist them in effectively integrating hereditary cancer risk assessment, for the patients and their relatives, into everyday practice [38,93,94].
Empowering oncologists and clinicians to integrate genomics into their clinical practice was the objective also of the Maine Cancer Genomics Initiative. This initiative, undertaken by the Jackson Laboratory, developed several online programs and resources and in-person interactive workshops in clinical genomics, testing, and risk assessment, especially for screening protocols for hereditary tumours [37,[95][96][97]. After identifying a need for further awareness and training among primary care providers about appropriate referral for BRCA counseling and testing, the Michigan Cancer Genomics Program collaborated with federal, state, and local partners to launch in 2014 a free online continuing medical education course and other online tools for healthcare professionals for increasing cancer genetic literacy among the public and healthcare providers, improving the use of appropriate cancer risk assessment and clinical genetics services, enhancing communication, and developing partnerships with cancer genetic service providers and other key stakeholders [45].
In 2019, the American College of Medical Genetics and Genomics, through online courses, offered geneticists valid instruments to identify common genetic syndromes, provide genetic counselling for common human cancers, and explain clinical and molecular aspects of inherited cancer syndromes [35].
The Global Genetics and Genomics Community (G3C) created the learning portal "Genomic Health care Simulations" for practicing healthcare professionals, which is a bilingual collection of interactive cases that demonstrate how genetics and genomics link to health and illness [44].
In August 2009, the Cancer Genomics Consortium (CGC) was formed by a group of clinical cytogeneticists, molecular geneticists, and molecular pathologists interested in education and promoting best practices in clinical cancer genomics. In collaboration with the University of Wisconsin, the Consortium offered a series of webinar "Cancer Genomics Consortium 2020-2021" to genetic counsellors and healthcare professionals who generate or use genomics/genetics data in their practice. These webinars included resources to aid interpretation of cancer variants, germline predisposition to cancer, the use of new technologies in clinical genomic testing, and the detection of copy number abnormalities from NGS data in cancer samples [36]. In 2018, the Mayo Clinic, in collaboration with the University of Illinois, offered an intensive course for scientists and clinicians covering the basics of computational genomics, genome sequencing, and assembly, polymorphism, and variant analysis, epigenomics, and data visualization [34,98,99]. In the last years, other universities in the USA organized annual online courses on cancer genomics and sequencing, precision oncology, such as Stanford Genetics and Genomics Program, HMX Pro Genetics Cancer Genomics and Precision Oncology, and Short Courses of Genetic Analysis [33,41,43,[100][101][102][103][104][105][106][107][108][109][110][111][112][113][114].
In Africa, in 2017, the African Genomic Medicine Training Initiative was created by volunteers globally, supported by H3ABioNet, the Southern African Human Genome Programme, and the University of Pretoria. This initiative designs and develops Genomics Medicine training for African-based healthcare professionals on genomics applications in cancer care, pharmacogenomics, counselling, and clinical genomic research [48,115].
In Australia, the Genomics basics for Primary Care was created in 2019 as a joint initiative between Metro North GPLO and the Brisbane North Primary Health Network. It aimed to increase the knowledge of general practitioners of new developments in diagnostic cancer genomics so that they can understand how to support their patients if a referral is not necessary [49]. (1) Clinical genetics resources [84] (2) Ethical, legal and social implications resources [92] (3) Family history resources [86] (4) General genomics resources [87] (5) Genetic conditions resources [88] (6) Genetic counselling resources [89] (7) Genetic and genomic testing resources [90] (8) Pharmacogenomics resources [85] (9) Risk assessment resources [  (1) Genomics workshops and courses [81] (2) Online Genomic Pathology Modules [82] (   (1) Disease diagnoses, risk assessment, pharmacogenomics, for clinicians [79] (2) Data collection, laboratory testing, research tools for researchers [80] Cancer genomics and genetics Genetic counselor, nurse, pharmacists, physician, physician assistant Open-source tool Open

Discussion
The need to train healthcare professionals in cancer genomics is a natural consequence of the disruptive development in this field since the sequencing of the human genome. From an oncologic perspective, major results were achieved in the last decades, enabling medicine to offer cancer patients targeted treatments and innovative approaches [116]. These rapid changes require skilled healthcare professionals for the provision of the optimum care to patients. In this context, the objective of our study was to summarize the initiatives aimed at improving healthcare professionals' literacy in cancer genomics field. Even though the aim was not to assess which countries are at the forefront in healthcare professionals training on cancer genomics, the results suggest that greater attention to this topic was paid in the USA and the UK, although the results might be influenced by the search strategy adopted. Most of the initiatives were directed to non-geneticist healthcare professionals and were offered in web-based modalities, such as online lectures, courses, resources, or tools. Online training format was considered as the more effective modality to enhance knowledge, skills, and confidence [117][118][119].
The technological innovations of genomics and other omics sciences allow physicians to offer personalized diagnosis and treatments, especially in the oncology field [120][121][122]. Through personalized medicine based on genomics, it has been possible to achieve an improvement in risk stratification, for example, in hereditary breast cancer. Carriers of BRCA1/2 pathogenic variant carriers and their relatives have an increased risk of breast cancer due to their genetic predisposition and are a well-established sub-group of individuals with needs for targeted prevention and care pathways based on a risk-based approach [123].
Furthermore, researchers are using whole exome analysis to characterize the genomic landscape of responders and non/responders to anti-HER2 treatment among metastatic breast cancer patients [124]. Genomics is contributing to the understanding of the polygenic nature of certain diseases, such as cardiovascular disease or diabetes. Polygenic score models are being developed for specific subgroups of cardiovascular disease, such as CAD, stroke, and hypertension, that are currently used for screening and risk assessment to provide inform decisions for targeted treatments or tailored lifestyle modifications. Polygenic scores might be integrated into national programs to improve the predictive accuracy of cardiovascular risk assessment at population level [125].
However, due to the shortage of genetic professionals, citizens and patients were mostly directed to non-geneticist healthcare professionals, regardless of their field of expertise, for genomics test interpretation or counselling [126]. Therefore, in this context, it is necessary to increase training efforts for all the healthcare professionals, enabling them to better support their patients with appropriate evidence-based health decisions. In particular, training initiatives should focus on general practitioners and primary care physicians, as the first contact point for patients for counselling, genomics test interpretation, or family risk assessment. Primary care practitioners expressed the necessity for education activities in cancer genomics in order to answer adequately citizens' questions [127][128][129], especially for direct-to-consumer genetic tests that are purchased online without medical supervision or counselling [130][131][132][133][134].
Education strategies should cover the challenges posed by the increasing demand for cancer genomics competencies in clinical care regarding the use, implementation, and validity of genomic tools. Therefore, in response to these challenges, several organizations, such as the Inter-Society Coordinating Committee for Practitioner Education in Genomics (ISCC-PEG), have been created to identify educational needs and potential solutions. Regardless of the increased attention by different organizations, further training efforts are needed in the field.
Furthermore, several researchers have suggested the integration of genomics into curricula for undergraduate and postgraduate studies and their continuous update [135,136]. A survey conducted at the global level in 2018, only three countries (USA, the UK, and Japan) incorporated genomics into nursing education [137]. A systematic review included 41 articles, summarized the characteristics of genomics curricula for health professional students, reported that the majority of the curricula were offered to medical and pharmacy students and were not theory-based, and 85.4% of the studies did not report follow-up data regarding the evaluation outcomes [138]. Despite the increased interest in evaluating genomics knowledge, it remains substantial to understand the possibilities of healthcare professionals to undertake training options, given the time restrains in their healthcare practice. In order to develop effective training opportunities, the impact of such initiatives on healthcare professionals' knowledge, abilities, attitudes, and skills should be explored. In this context, future studies should evaluate the outcomes of the training options, reporting measured indicators, that could help to improve the development of new initiatives, based on education needs.
Given that cancer genomics is a developing field, curricula should be elaborated based on basic concepts and competences required for the accurate use, interpretation, and dissemination of genomics information. Future studies should pay attention to the current structure of curricula to better understand whether the new healthcare professional figures will have the required core competencies to cope with the challenges that genomics has been posing to healthcare systems.
Notwithstanding, in front of the rapid evolving knowledge in cancer genomics, constant training and updating of such curricula and education initiatives remain fundamental, as it is shown in the Italian example [27].
This work has some limitations that should be mentioned. Using only search terms in the English language, we might have not been able to identify initiatives that were conducted at in national language by different countries. It should be noted that not all the conducted initiatives could be publicly available across the Internet or presented in organizational repositories, thus suggesting that not all of them were possible to identify. Additionally, although we performed the search in the most used search engines worldwide, we might have lost initiatives available at other search engines, such as WeChat or Baidu, mostly used in Eastern countries, suggesting that our results might not be representative of all European countries. Moreover, the high heterogeneity of the identified initiatives, in terms of methodology and topics, and the lack of detailed information in some of them, did not allow us to make an accurate comparison among them. Furthermore, it was not possible to assess the effectiveness of the initiatives, since they did not provide any quantitative data, measures, or indicators.
Despite these limitations, our work is the first attempt to summarize past and ongoing initiatives addressing healthcare professionals in the cancer genomics field using a web search with a systematic and scientific approach. This innovative web-based screening methodology was recently applied in a previous study aimed at mapping educational initiatives to increase citizens' literacy in genomics and genetics field [139]. Focusing on both healthcare professionals and citizens' literacy is a priority strategy for implementing PM in clinical care and improving the public understanding of its value for heath.

Conclusions
Understanding and appropriately being able to apply genomics tools in the management of cancer, in terms of prevention, diagnosis, and treatment, is the key to coping with innovation to provide quality in care. Our results may contribute to provide an update on the development of educational programs to build a skilled and appropriately trained genomics health workforce in the future.