Citizens' Attitudes, Knowledge, and Educational Needs in the Field of Omics Sciences: A Systematic Literature Review

Background: The huge development of omics sciences is changing the classical medical approach and making new technologies available. In this context, education of citizens is essential to allow appropriate decisions about their own health. Hence, we aimed to summarize existing literature regarding citizens' knowledge, attitudes, and educational needs on omics sciences. Methods: We performed a systematic literature review (SLR) using Pubmed, ISI Web of Science, and Embase databases. The eligibility criteria for inclusion in this review required that the studies investigated knowledge, attitudes, or educational needs regarding omics sciences among the general population. Results: We included 54 studies, published between 2006 and 2020. Most of the included studies (72%) investigated citizens' knowledge, half of them (56%) attitudes, and 20% educational needs in the field of omics sciences, while 52% investigated attitudes and perceptions about genetic and/or omics tests. Most studies (64%) reported a limited knowledge level among citizens, even though most (59%) reported participants understood the benefits of the use of omics sciences into medicine. As for omics tests, a controversial opinion toward their use into practice was reported among citizens. Most of the studies (82%) investigating citizens' educational needs highlighted a clear gap to be filled. Conclusions: Our SLR summarizes current knowledge on citizens' literacy, attitudes, and educational needs on omics science, underlining the need for strengthening public engagement on this topic. Further research is needed, however, to identify appropriate methods and models to achieve such an improvement.


INTRODUCTION
Rapid growth in genetic and genomic research has transformed our understanding of the role of genes in health and disease. The historical focus of genetic research has been on rare, single-gene disorders, in which disease risk is largely based on the presence or absence of a mutation in a single associated gene. This focus has been greatly expanded in recent years (Lea et al., 2011). Research in genomics is now examining the genetic components of common, complex diseases, such as cancer, diabetes, heart disease, etc. For these diseases, the contributions of single genes to risk are often small in comparison to the rare, inherited diseases, and disease risk is based on multiple genetic and environmental factors. These aspects highlighted the complexity of biological systems and provided new approaches to diseases diagnosis, treatment, and prevention (Lea et al., 2011).
Since the mapping of the human genome in 2003 (International Human Genome Sequencing Consortium, 2004), important progress has been made in understanding molecular and genetic pathways underpinning human health and diseases, promoting the development and the diffusion of genomics and of other omics sciences and related technologies.
In the last two decades, the use of words ending in "omics" has extended, from the initial "genomics, " to a wide range of biomolecular disciplines addressed to the study of specific aspects considered as a whole. Therefore, the omics sciences study pools of biological molecules (e.g., ions, nucleic acids, proteins, enzymes) with various functions within living organisms and have the primary objective to analyze as a whole e.g., genes contained in DNA (genomics) and their multiple functions (functional genomics), DNA transcription product-RNA-(transcriptomics), proteins encoded by DNA through RNA (proteomics), molecules that interact within an organism or metabolites (metabolomics) (Lin and Qian, 2007;Tebani et al., 2016). Among the other goals of these sciences is also to study the connections and reciprocal interactions between the pool of biological molecules (interactomics) and between these molecules and microorganisms of the intestinal flora (microbiomics), foods and/or nutrients (nutribiomics) (Coughlin, 2014).
Since then, the Human Genome Project (HGP) was followed by other relevant initiatives, such as International HapMap Project (The International HapMap Consortium, 2003), ENCyclopedia of DNA Elements (ENCODE) Project (ENCODE Project Consortium, 2004), 1'000 Genome Project (1000Genomes Project Consortium et al., 2015, and 100'000 Genome Project (Turnbull et al., 2018;Genomics England, 2019a,b). The importance of genetic factors in determining disease risk was understood by various European and not European governments and Institutions. To this end, a number of projects were put in place in the world, some of them even before HGP: for example, the Icelandic company deCODE, around 1996, announced a plan to genotype the entire national population .
Hence, an exponential growth of knowledge took place, first in genomics and later in other omics sciences too. As a consequence, new technologies, such as Next-Generation Sequencing (NGS), are nowadays available. These highthroughput omics technologies simultaneously measure thousands of data providing detailed information of cells, organisms, and populations and contributing to the definition of new diagnostic tests, new biomarkers and new drugs in the era of precision medicine (Tebani et al., 2016). These new second generation technologies led to an important cost reduction compared to the past (van Dijk et al., 2014), allowing then an increased accessibility to genomics testing and a potential improved sustainability by health systems. Therefore, during last years, a growing and uncontrolled availability of genetic tests, not only for monogenic disorders but also for multifactorial ones, took place and this progress in the genomics field had evident implications for public health, bringing important benefits but also potential risks for the population. A perfect example in this sense is given by direct-to-consumer genetic tests (DTC-GTs), which are tests sold by companies directly to consumers, without the involvement of a health professional (Su, 2013). In particular, besides potential discriminatory and privacy issues, not always properly addressed by laws and regulation (Kalokairinou et al., 2018;Hoxhaj et al., 2020), citizens don't have competencies needed to understand of results of these genetic tests, thus possibly leading to further unnecessary diagnostic investigation and, finally, waste of healthcare resources (Borry, 2010;Su, 2013). Furthermore, literature data suggest that knowing own genetic risk for specific diseases could lead to psychological distress, even though there are not clear evidence yet (Su, 2013).
All these aspects highlight the importance of counseling by trained health professionals and of appropriate citizens' education about omics sciences and new technologies related to them. Previous reviews report conflicting results about citizens' knowledge in the field of genetics, genomics, and DTC-GTs (Covolo et al., 2015;Hoxhaj et al., 2019;LePoire et al., 2019), even though with positive attitudes (Covolo et al., 2015;American Society of Human Genetics, 2020).
However, to our knowledge, no previous systematic review attempted to assess citizens' knowledge and attitudes in the wide field of omics sciences. Furthermore, we do not yet have adequate information on the educational needs of the general population in this field and on the topics of greatest interest to citizens.
Hence, to address these issues, our aim was to systematically summarize the existing evidence about knowledge, attitudes, and educational needs regarding omics sciences among the general population.
search strategy was also used as template for the search in the other databases.
Three researchers (GEC, MS, AT) independently reviewed titles, abstracts, and full texts of the retrieved papers in order to identify the eligible studies. Results were cross-checked and any disagreement was resolved through discussion until consensus was reached. The snowball strategy, a manual search of the references reported by studies retrieved from the online databases, was also adopted to identify additional studies. The systematic review was drafted in accordance with PRISMA guidelines (Moher et al., 2009).

Eligibility Criteria
Studies that investigated knowledge, attitudes (in terms of perceived benefits and/or risks), or educational needs regarding omics sciences among the general population were deemed as eligible. We excluded commentaries, editorials, conference abstracts, reviews, case reports, case series, and book chapters, and articles addressing a population of researchers or professionals only.

Data Extraction
From each eligible study we extracted information on Country, promoter of the initiative, duration and aim of the initiative, topic, target population and age, methods/initiative description and initiative type, awareness on genetics/omics sciences, perceived benefits on the use of genetics/omics sciences in medicine, worries about the use of genetics/omics sciences in medicine, perceptions about genetic/omics tests, need for more education/information regarding omics sciences among the population.
Results are presented according to the three major areas investigated across the studies, namely knowledge, attitudes and educational needs about omics sciences and genetic and/or omics tests. and 985 from Embase). After duplicates removal and title and abstract screening, 99 articles were selected. From these, after full-text analysis 51 studies were removed, while 6 additional studies were retrieved though snowball search of reference lists of included articles.
After the latest selection process, 54 articles responded to eligibility criteria and were included in the systematic literature review. The Figure 1 shows study selection process, as indicated by PRISMA guidelines (Moher et al., 2009), while Table 1 reports main characteristics of included studies.
The articles included in this systematic review were published between 2006 and 2020. Among the 54 included studies, 44% were conducted in USA (n = 24) Goddard et al., 2007Goddard et al., , 2009Gleason et al., 2010;Hahn et al., 2010;Lemke et al., 2010;East et al., 2012;Kaphingst et al., 2012Kaphingst et al., , 2015Kaphingst et al., , 2016 Among studies investigating citizens' knowledge, 31% (n = 12) aimed to evaluate knowledge on basic concepts in genetics among the general population Skirton et al., 2006;Calsbeek et al., 2007;Ishiyama et al., 2008;Molster et al., 2009;Sturgis et al., 2010;Mai et al., 2011;East et al., 2012;Abrams et al., 2015;Simonstein and Mashiach-Eizenberg, 2016;Jones et al., 2019) (Table 2). More than half of the identified studies (72%, n = 28), instead, investigated knowledge of the population on genetic and/or genomics tests Skirton et al., 2006; USA University Assessment, through questionnaire, of effects of the type of risk assessment carried out (family history assessment or genetic test results), the type of disease (cardiovascular disease or diabetes), and ethnicity on the attitudes regarding the genetic risk for complex diseases and genetic testing   -Willingness to receive more information on genetic research, as it was considered important for reducing fears and increasing confidence. It is important to increase awareness in isolated groups (low income, minorities), young people, schools, neighborhoods and disease support groups. Suggested strategy was to target populations at greater risk for a given condition than the general population. Other proposed strategies were information via evening TV news, internet, focus groups.

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Frontiers in Genetics | www.frontiersin.org Heterogeneous. Level of knowledge on limits and benefits of sequencing was very variable before starting the study. Knowledge increased significantly from pre to post informed consent.
Level of knowledge related to the level of education.
- Kolor et al. (2012) Heterogeneous. DTC-GT awareness ranged from 15.8% in Michigan to 29.1% in Oregon. The most commonly cited source from which respondents read or heard of DTC-GTs was, in descending order, TV or radio, newspaper/magazine and Internet. --

Nielsen and
El-Sohemy (2012) Low. Fifty-two percentage said they had not heard "anything" about DTC genetic testing. -- --Participants called for increased public awareness about personalized medicine to increase confidence and use of new technologies, in addition to counseling services. Haga et al. (2013) Moderate. Participants scored significantly higher on questions related to heredity and causes of diseases (average score of 94.6%) compared to questions on genes, chromosomes and cells (average score of 78.6%). Most of participants (79%) said they had some knowledge of the medical applications of genetics.
Low. Awareness about genetic testing and genetic diseases did not change between 2002 and 2010. -- About a fifth of respondents heard of companies selling genetic tests directly to consumers.
Low. Less than 10% knew the average risk of breast cancer in the general population and the fraction of breast cancers due to BRCA mutations.
Knowledge of Angelina Jolie's story was not associated with better understanding. - Frontiers in Genetics | www.frontiersin.org -- Abrams et al. (2015) Moderate. Participants were "somewhat familiar" with genomics terms presented. Average score in the assessment of skills resulted 4 out of 6 correct answers, while on average participants correctly identified 8 out of 16 facts.
Level of knowledge related to the level of education.
- Dodson et al. (2015) Moderate. About 58.6% of respondents expressed some interest in whole genome sequencing, especially in those who expressed interest in having a child in the next 5 years.
Low/very low. Many participants noted they lacked knowledge about genetics and associated research.
-Participants reported the necessity for accurate information to make informed decisions both about genetic testing and participation in genetics research.
--Strong interest in receiving a genomics evaluation for reference diseases (diabetes/heart disease), in discussing genomics information with family members and a doctor, and in modifying lifestyle in relation to genomics information.
Mavroidopoulou et al. (2015) Low. 43.7% of the participants had the perception of being lacking in basic knowledge of genetics, unlike 34.5% who believed they knew enough.
On average, participants answered 3 out of 5 questions regarding genomics correctly.
Poorer knowledge in the elderly than in the youth.
One third of respondents reported having heard of personal genetic tests.
Moderate. Adopted scale and frequency of participants in each group: "High" level of knowledge: understanding of the terms genome and gene or understanding of the term "gene" and having heard of "genome" = 30.2%; "Medium" level: having heard of both terms or understanding the term "gene" and having never heard of "genome" = 35.7%; "Low" knowledge consisted of having heard of "gene" and not of "genome" or of never having heard of both terms = 34.1%.
Higher level of knowledge in those who had previous experiences in genetic education (genetics courses, website consultations and reading of books and/or articles).
Most participants did not understand basic level questions in the general understanding of genetics section. 47.6% correct answers in the general understanding section of genetics. 74.9% correct answers in the genetic risk section. -- Frontiers in Genetics | www.frontiersin.org  Among the participants, 48.0% were worried about discrimination based on genetic data.  Consumers believed that potential benefits of nutrigenomics outweigh risks. For participants, nutrigenomics could also lead to early diagnosis or disease prevention and, in general, could encourage healthy eating habits.
Toward online services and DTC genetic tests. Greater regulatory control is needed to protect consumers (in particular for sale of genetic tests).
Stewart-Knox et al.
Perceived benefits of nutrigenomics to follow a personalized diet. Concerns about how information would be used.

Hahn et al. (2010)
For disease prevention and treatment. Affordability, unanticipated physical harm, mistrust of the government and researchers, downstream effects like overpopulation, playing God/disturbing the natural order, lack of regulations, loss of privacy, genetic discrimination, and moral dilemmas posed by genetic engineering, cloning, choosing traits, and abortions resulting from genetic information.

Lemke et al. (2010)
Among perceived benefits of genomics research there were the possibility to prevent and treat diseases and potential cost savings to society.
Concerns about sharing research results with the public, possibility of discrimination by insurance companies, the government, the health care system, and employers.

Nielsen and
El-Sohemy (2012) Nutrigenomics information was considered useful for motivation to change lifestyle (prevention).
- Bombard et al. (2013) For disease prediction and treatment. Costs, accessibility, need, and feasibility of introduction into the health system. Haga et al. (2013) More than half of participants agreed with the possibility that a DNA test will change a person's future (56.3%).
More than half of participants agreed with the possibility that a DNA test will affect a person's ability to obtain health insurance (51.3%), 16% were worried about the consequences of tests on the possibility to find a job.
Henneman et al.
-Some believed that insurance companies will require genetic testing in the future to determine the premium (36%, <2002).

Nicholls et al. (2013)
The application of genomics to screenings could allow early intervention, prevention, and stricter monitoring.
Costs, educational needs regarding the probabilistic nature of the risk, access to personal genomics information.
Almeling (2014) Perception of importance/utility (indirectly: 57% agree that the federal government should spend more on researching the genetic causes of diseases).
Important to avoid discrimination (82% believe GINA-Genetic Information Non-discrimination Act 2008-is important).

Vermeulen et al. (2014)
Especially interests for preventive genomics. - Etchegary et al. (2015) Omics sciences perceived as beneficial, but not a priority for the health system.
Dangerous use of information, privacy issues. Kaphingst et al. (2015) Black women perceived fewer health benefits than white women; Hispanics had greater interest in receiving a genomics assessment than non-Hispanic whites.
Most participants expressed interest in undergoing DTC genetic testing for serious diseases, such as cancer (54.9%), or a metabolism or genealogy test (50.2%), but would prefer to consult their doctor first.
Concerns about personal data.

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Frontiers in Genetics | www.frontiersin.org Participants understood the importance of sharing data and samples and creating databases for rare diseases.
Concerns about risks to privacy and autonomy in sharing data on an international database. Need to limit access to personal data to health professionals involved in research. All participants were against access to data by private companies.  Over 80% of participants agreed that the use of genetic information for medical purposes is "useful for disease diagnosis," "useful for disease treatment" and "useful for disease prevention" Less than half of respondents showed "concerns" about the use of genomics in medicine (worries regarded the use of genomics information by companies or government agencies, possible discrimination at work and by insurance companies, problems related to cloning of humans, unexpected negative effects). (2016) Most (81.3%) believed that medicine could improve with the use of genetic engineering.

Simonstein and Mashiach-Eizenberg
Almost half of the participants agreed (22.7% partially agreed, 18.7% agreed) with the sentence "genetic engineering could destroy the human race."  Nutritional epigenomics was perceived positively compared to nutritional genomics.
Possible conflicts of interest between scientific research and the agri-food industry. Metcalfe et al. (2018) Only for health purposes. Concerns about privacy issues, potential discrimination. Cost skepticism (speculation by companies) was expressed too.

Horrow et al. (2019)
Genomic optimism was positively associated with higher health literacy.
Genomics pessimism was associated with lower health literacy.

Jones et al. (2019)
The majority (67.2%) of questionnaire respondents placed a high or very high value on using genetic data for research.
Almost half of the respondents reported moderate concern about the use of genetic data for research (48%). Most commonly expressed concern was misuse of data tied with concerns about information governance. Participants expressed the importance of informed consent for access to genetic data for research and a preference for a safe use of the data.

Middleton et al. (2020) -
The main potential harm identified was the possibility to use DNA of other individuals to blame them for a crime (45.2%), insurance discriminations (37.2%), use of genetic information by companies for targeted marketing strategies (35%).

References
Perceptions about genetic/omics tests Henneman et al. (2006) Variable, almost half of respondents neither agreed nor disagreed with the statement that genetic testing carries more benefits than risks. Skirton et al. (2006) Positive, in particular for disease prevention and prevention for family members. Calsbeek et al. (2007) Positive, most participants approved genetic testing for the treatment of diseases (78% to 86%) or for early detection of diseases. However, some concerns were expressed, mostly related to the consequences of DNA-testing for taking out insurances. Morren et al. (2007) Variable. Just over two thirds said they would like to know if their disease is genetic. Thirty percentage said they did not want to know if they are at risk of a genetic disorder. If no appropriate treatment was available, over 40% of chronic patients would abstain from genetic test. Most respondents thought that the family should be informed of test results and would share the results with their children (70%) and siblings (65%). Makeeva et al. (2009) Positive, most participants stated that they would undergo tests and change their lifestyle based on the results.
Morin ( Nielsen and El-Sohemy (2012) Positive, nutrigenomics knowledge was considered useful to motivate people to change own lifestyle. Bombard et al. (2013) Variable/with doubts. Positive, but concerns for ethical issues for access to treatments based on genetics were expressed. Haga et al. (2013) Variable. 52% of participants stated they were interested in genetic testing and 45% said they were extremely interested. Most participants expressed positive attitudes toward the goals of genetic research and the use of genetic tests. Henneman et al. (2013) Variable, not everyone agreed that genetic tests make it possible to live longer or that they carry more benefits than harms.
In 2010 more people (compared to 2002) believed that the use of genetic tests should be promoted, although 37% did not agree. Nicholls et al. (2013) Variable, basically positive attitudes.
Almeling (2014) Most believed that healthcare professionals should be involved in explaining test results. Vermeulen et al. (2014) Variable. About half of the participants expressed interest in genetic testing for prevention of specific diseases (cancer, cardiovascular disease, diabetes, or dementia). According to participants, genetic tests should be performed in hospitals (66%) and addressed to curable (57%) or preventable (69%) diseases. Older participants said they wanted to know only about diseases that can be treated more often than younger ones (65% vs. 47%). Etchegary et al. (2015) Controversial, with concerns mostly related to data privacy and possible harmful uses of test results. Graves et al. (2015) Variable. The existence of a treatment (87%) and the severity of the disease (85%) were considered important in deciding which test results one wants to know. Kaphingst et al. (2015) Variable. Greater interest in genomics assessments among those with a limited health literacy. Mavroidopoulou et al. (2015) Positive. Genetic tests must be preceded by medical genetic counseling. Interest in undergoing a DTC genetic test was cost dependent. Mählmann et al. (2016) Positive, most participants were interested in undergoing genetic testing to know their own disease risk.  Variable. Positive toward genetic tests for drug susceptibility (48.5% of the interviewees showed positive attitudes, 29.7% did not know how to respond and 21.7% showed negative attitudes).

Simonstein and Mashiach-Eizenberg
Positive, most supported using genetic testing during pregnancy (86.7% believed that screening for genetic risk in potential parents is not wrong; 72.9% believed that all women planning a pregnancy should undergo a genetic test)  Mostly negative. Some interests toward nutrigenetic tests have been identified (for curiosity, scientific progress, early diagnosis), but much of the discussion has shown reluctance toward their adoption. Worries for dangerous use of the internet, criticism of science, deterministic aspect, fear of knowing, desire/right not to know, ethical issues, attachment to French food models were expressed. Metcalfe et al. (2018) Variable. Heterogeneous among participants. Positive attitude for tests for health conditions, especially for diseases for which there is treatment/cure.

Horrow et al. (2019)
Mostly positive. Most respondents attributed high value to their potential genetic test results. Some participants (35.2%) did express concern about the confidentiality of their genetic test results. Pereira et al. (2019) Mostly positive. Most patients (77%) were interested in finding out if they had pharmacogenetic variants or other genetic variants that were related to their health (73%).

Rebitschek et al. (2019)
Variable about epigenetic testing aimed to assess personal cancer risk. Participants' arguments in favor of epigenetic cancer risk assessment covered three major beliefs: guidance on one's individual medical strategy, the development of coping strategies (empowerment) by knowing one's risks, and a motivational push to healthier or more conscious living. Unnecessary worry about cancer risk and consequences, the uncertainty surrounding the test result, a perceived lack of test benefit were the main concerns that were brought up against testing.
Eventually, just a small number of included studies (10%, n = 4) proved a medium-high or high knowledge level Schmidlen et al., 2016;Horrow et al., 2019). Several studies included in our review reported a correlation between citizens' level of knowledge and some of their socio-demographic characteristics. Mai et al. reported that individuals living in villages had poorer awareness about the existence (61.5%) and the biological role (16.9%) of DNA compared to individuals living in cities (93.7 and 80.8% respectively) . A similar trend was observed for age, with respondents aged <35 years more likely to be aware of the existence (94.6%) and the biological role (85.5%) of DNA compared to individuals older than 60 (86.6 and 60% respectively) . Kaphingst et al. reported a significantly lower genetic knowledge among older participants compared to younger participants, but also that Black participants had lower genetic knowledge than White participants . Lastly, 2 studies investigated the correlation between citizens' educational attainment and the effects on genetic literacy. In particular, the first one reported that knowledge about limitations of genome sequencing was higher among individuals with any post-graduate education (odds ratio, OR: 8.7; 95% confidence interval, CI: 2.45-31.10) and with a college degree (OR: 3.9; 95% CI: 1.05-14.61) compared to individuals with an education level lower than a college degree . Instead, the last one reported a correlation (Pearson correlation coefficient, r: 0.357; p < 0.001) between higher education level (ranging from less than high school to bachelor or higher) and better genetic knowledge .

Sources of Citizens' Information
Two studies (5%) investigated the main sources of citizens' information Kolor et al., 2012; Table 2). Goddard et al. in a study published in 2007 and focused on DTC nutrigenetic tests, pointed out that TV (for 46% of survey respondents), magazines (35%), and newspaper (29%) were the major sources of information among study participants. Similarly, Kolor et al. (2012) showed that most commonly interviewed people read or listened about DTC-GTs on TV or radio, newspapers or magazines, and internet, in this order.
In several studies, participants reported that genetic tests would be appropriate only if used for the diagnosis of treatable or preventable diseases Vermeulen et al., 2014;Graves et al., 2015;Metcalfe et al., 2018). Furthermore, according to the study of Graves et al. (2015) the disease severity was also reported as an important parameter in deciding which test results are to be known (Covolo et al., 2015).
Furthermore, the importance of informed consent process as an educational moment  and the priority and usefulness to pay particular attention to individuals at high risk for specific diseases, "isolated groups" (e.g., low income, ethnic minorities), youth and students were underlined .
Moreover, during focus groups described by Lemke et al. several information strategies were suggested by participants, such as evening TV news, internet, and focus groups .
Lastly, 4 studies (8%) investigated methods to increase citizens' literacy, such as Science Cafés with genomics experts , education courses on specific genetic and ethic topics , short courses held by experts , and an institutional web information portal . The comparison of described experiences doesn't allow to establish the most effective method to improve general population's literacy, due to the lack of quantitative analysis and the heterogeneity of initiatives and topics dealt with.

DISCUSSION
This review aimed to describe current literature about citizens' knowledge, attitudes, and educational needs in the field of omics sciences. We performed a systematic literature search and we identified studies published from 2006 onward, few years later Smerecnik et al., 2011;Dijkstra et al., 2012;East et al., 2012;Almeling, 2014;Borzekowski et al., 2014;Abrams et al., 2015;Etchegary et al., 2015;Mavroidopoulou et al., 2015;Mählmann et al., 2016;Simonstein and Mashiach-Eizenberg, 2016;Ahmed et al., 2017;Waters et al., 2017;Metcalfe et al., 2018;Jones et al., 2019). Thus, a clear need for improving citizens' literacy is evident, even to avoid risks deriving from inappropriate use of omics technologies Boccia et al., 2019). The long time period covered by our systematic review, starting with the beginning of the omics era interestingly shows that over some 15 years only one study from 2019 of Horrow et al. (2019) reports a high level of awareness and knowledge about genomics. As the participants in this study took part in a genome sequencing project, this result is not surprising and points out that an adequate information associated with active citizen involvement improves not only knowledge but also perception and attitudes on omics sciences and, in particular, about genetic/omics tests.
Moreover, several studies investigated which sociodemographic factors can correlate with citizens' knowledge level and literacy. In particular, a positive association was shown with education Abrams et al., 2015) and younger age Kaphingst et al., 2016). Furthermore, a lower knowledge level was shown in individuals residing in suburban and extraurban areas, compared with individuals living in cities .
Main sources of information resulted to be TV, magazines, newspapers, and internet, rather than healthcare professionals. This highlights the need for increasing literacy, not only for citizens, who should be better informed about where and from whom to seek trusted information, but for healthcare professionals too , in order to allow them interact with patients and give them satisfactory explanations .
The present systematic review provides relevant information about citizens' perceptions regarding benefits and risks related to the use of genomics or omics sciences in the medical field too. In particular, most of the studies showed that participants perceived benefits and usefulness from the use of genomic and omics science in medicine Morren et al., 2007; Moreover, the few studies investigating need or request for more education or information on genomics or omics sciences among the population highlighted a clear lack to be fulfilled Hahn et al., 2010;Lemke et al., 2010;East et al., 2012;Bombard et al., 2013;Etchegary et al., 2015;Rebitschek et al., 2019). The main identified topics to focus for citizens' education were genetic/genomic research Lemke et al., 2010;Dijkstra et al., 2012;Etchegary et al., 2015), disease etiology and susceptibility Kaphingst et al., 2015;Rebitschek et al., 2019), nutrigenomics , and genetic and omics tests Rebitschek et al., 2019).
Our results show also a set of potential information strategies, such as TV news, internet, and focus groups , Science Cafés with genomic experts , education courses on specific genetic and ethic topics , short courses held by experts , and an institutional web information portal . However, unfortunately it was not possible to establish quantitatively the most effective method to improve citizens' literacy in omics sciences field.
Notably, we found no study focusing on omics sciences other than genomics and genetics or genetic tests. This could be due to genomic applications being more widespread than other omics technologies, which are probably still less known and more difficult to understand by the general population. Based on this knowledge gap, the planning of education programs for citizens should pay more attention to these issues and provide clear and accurate definitions of the different omics sciences and related tests. Indeed, an important aspect to take into consideration in the information/training process aimed at the general population is also the terminological consistency to be used and disseminated (Martin et al., 2020). Indeed, this is a key aspect for citizen empowerment, since the terminological inappropriateness or variety of scientific definitions could cause great confusion among citizens, especially in a field as complex as that of the omics sciences.
To our knowledge, no previous systematic review attempted to assess citizens' knowledge and attitudes in the wide field of omics sciences. We included also studies related to the field of nutrigenomics, genomics research, and biobanking. Furthermore, to date we do not yet have adequate information on the educational needs of the general population in these fields.
However, our study has several limitations too. In particular, due to the high heterogeneity among studies, it was not possible to summarize quantitatively investigated issues, even though we believe we appropriately summarize here our findings qualitatively. In addition, we included studies conducted on a limited number of participants which therefore may be not representative of the general population. Another limitation of the study is represented by the heterogeneity of the "citizens" studied in the papers like patients suffering from different diseases, participants in sequencing (biobank) projects, users of DTC-GTs etc. The different "citizens" studied obviously have different knowledge levels and training needs that must be taken into account in planning a training strategy for the general population. Also, there may be an insufficient understanding by the general population of "omics sciences" as merely "genetic." This, however, seems to be kind of a general perception, also by professionals. The results of the present systematic review show that citizens' knowledge on omics is generally poor or very poor Hahn et al., 2010;Lemke et al., 2010;Dijkstra et al., 2012;Metcalfe et al., 2018) though some papers show moderate knowledge of citizens on basic genetics and genetic testing Haga et al., 2013;Schmidlen et al., 2016;Waters et al., 2016;Krakow et al., 2017) and the interest of the population on these issues is emerging Hahn et al., 2010;Lemke et al., 2010;Dijkstra et al., 2012;East et al., 2012;Bombard et al., 2013;Etchegary et al., 2015;Kaphingst et al., 2015;Rebitschek et al., 2019). These data, however, underline an important educational gap to be bridged in order to make all stakeholders (health professionals, decision makers, citizens, etc.) understand what omics sciences are and what their potential is for public health.
Additionally, the studies included in our systematic review were conducted in North America, the EU, the United Kingdom, Switzerland, Russia, Australia, Japan and Israel, and three studies were conducted "in various countries." Therefore, our results are clearly biased toward Western culture and may not be representative of the world population. Due to the high heterogeneity among studies, it was not possible to give a clear differentiation of the range of application of our findings for the different world parts and cultures and further research will be needed aimed at defining the educational needs of citizens in the various countries. However, the aim of our study was to highlight current knowledge on citizens' literacy, attitudes, and educational needs on omics sciences, underlining the need for strengthening public engagement on this topic.
Despite the limitations described, our study provides important indications for fostering research and innovation in the field of omics sciences. In particular, it allows us to confirm citizens' literacy but also the capacity building of healthcare professionals in omics sciences field as a priority for action for health systems around the world. Healthcare professionals should be the main actors in the information process of citizens, especially in complex fields such as that of the omics sciences. The results of our review show that main sources of information for citizens resulted to be TV, magazines, newspapers, and internet. Therefore, an adequate training of health professionals is necessary not only to ensure the correct application of omics sciences in clinical practice, but also for correct information for end users and, therefore, for patients and citizens.
Furthermore, our systematic review identified the main elements to be considered for the development and implementation of new training strategies for citizens in the field of omics sciences. Specifically, based on the evidence collected (Tables 1-4), a training activity on omics sciences aimed at citizens must take into account the following items: 1. Target population to be trained. Training can be aimed at the general population or at specific population groups such as young or old people, students, individuals with specific diseases (e.g., patients with multifactorial diseases, chronic diseases, rare diseases, etc.), populations at greater risk for a given condition than the general population, workers, etc. 2. Topics on which to train citizens. Main topics on which to train citizens emerge from our study as the following: scientific basis of genetics, disease etiology and genetic susceptibility, genetic and non-genetic risk factors (environmental, lifestyle, etc.) on the risk of disease; possibilities, implications and future developments of genomics/omics research; genetic and omics tests with particular focus on DTC-GTs; importance of pre-and post-test genetic counseling; nutrigenomics and correlated tests; "genomic medicine, " "personalized medicine, " personalized approaches in the prevention of diseases; role of the omics sciences in specific fields (e.g., oncology, aging, cardiovascular, forensics); ethical implications associated with genetic/omics research and the use of genetic/omics tests, etc. 3. Tools with which to train the population. Our results show also a set of potential information strategies, such as TV news, internet, focus groups, Science Cafés with genomics experts, education courses on specific topics, short courses held by experts, and institutional web information portal. 4. Professionals to be involved in the training of the population.
This aspect was not investigated in our review however our study reveals that the main source of information for citizens are TV, magazines, newspapers, and internet. These data associated with the low level of citizens' knowledge in the omics sciences field further underlines the central role that health professionals must have in the education of citizens.
The general understanding of omics and its benefits for medicine, particularly in the context of personalized medicine, still appears to be quite limited despite important scientific advances in this field and the broad marketing of DTC tests. However, considering the broader context of "big" health data, understanding the omics issues is even more complex and for the future implementation of omics sciences in healthcare systems, educating of both citizens and health professionals will be essential. Indeed, not all "experts" could fully grasp the potential, challenges and issues at stake if not properly trained. Healthcare is increasingly data-driven, including omics. Therefore, health professionals will need to be properly trained in order to enable to the patients more informed health choices and ensure greater quality of healthcare (Fiske et al., 2019). Therefore, omics-based knowledge will be of utmost importance for every healthcare practitioner, regardless of the field of practice, as well as for citizens. Education will be crucial for the effective and successful implementation of omics sciences and it will have to evolve along with the changing scientific landscapes.

Conclusions
Progress in genomics has clear and crucial implications for public health. The current scientific context suggests a rapid transition from conventional to personalized medicine. Therefore, a strategic line to define the promotion and governance of omicsrelated innovation is necessary.
In order to achieve this change, the involvement of all stakeholders such as healthcare professionals, leaders, decision and policy makers, and citizens, will be necessary. In addition, the progress of the omics sciences is linked to the need to develop a solid literacy of both healthcare professionals and citizens. For this reason, effective tools of knowledge on the omics sciences field, especially for citizens, will have to be identified and implemented. Hence, further research should be fostered in the future to allow the identification of appropriate and effective methods for the design and implementation of largescale interventions aimed at improving citizens' literacy and engagement in the rapidly changing field of omics sciences.

AUTHOR CONTRIBUTIONS
SB and GEC conceived the study and MS and AT participated in its design. GEC, MS, and AT identified the studies through a search of MEDLINE, ISI Web of Science, and Embase online databases and performed the data extraction from the papers. SB and GEC supervised MS and AT. GEC, MS, and AT critically discussed and interpreted the results of the review. GEC and MS contributed equally to the drafting of the paper. SB critically reviewed this manuscript. All the authors approved the final version.