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 (1000 Genomes 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 (An, 2017).

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 high-throughput 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.

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 than the completion of HGP in 2003 (International Human Genome Sequencing Consortium, 2004). Most of them were conducted in USA (Fomous et al., 2006; Goddard et al., 2007, 2009; Gleason et al., 2010; Hahn et al., 2010; Lemke et al., 2010; East et al., 2012; Kaphingst et al., 2012, 2015, 2016; Kolor et al., 2012; Haga et al., 2013; Almeling, 2014; Borzekowski et al., 2014; Waters et al., 2014, 2016, 2017; Abrams et al., 2015; Dodson et al., 2015; Graves et al., 2015; Schmidlen et al., 2016; Ahmed et al., 2017; Krakow et al., 2017; Horrow et al., 2019) and fewer in European Union (Henneman et al., 2006, 2013; Calsbeek et al., 2007; Morren et al., 2007; Mai et al., 2011; Smerecnik et al., 2011; Dijkstra et al., 2012; Vermeulen et al., 2014; Mavroidopoulou et al., 2015; McCormack et al., 2016; Fournier and Poulain, 2018; Rebitschek et al., 2019). The main promoters of identified initiatives were universities (Fomous et al., 2006; Henneman et al., 2006; Skirton et al., 2006; Morren et al., 2007; Morin, 2009; Stewart-Knox et al., 2009; Hahn et al., 2010; Mai et al., 2011; Smerecnik et al., 2011; Nielsen and El-Sohemy, 2012; Bombard et al., 2013; Haga et al., 2013; Nicholls et al., 2013; Almeling, 2014; Borzekowski et al., 2014; Vermeulen et al., 2014; Waters et al., 2014, 2016, 2017; Dodson et al., 2015; Etchegary et al., 2015; Graves et al., 2015; Kaphingst et al., 2015, 2016; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Miyamoto et al., 2016; Schmidlen et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Fournier and Poulain, 2018; Metcalfe et al., 2018), enlightening the high interest of the scientific community for genomics and omics science implications for citizens and patients.

Main tools used to investigate citizens' attitudes, knowledge, and educational needs were questionnaires or surveys (Henneman et al., 2006, 2013; Calsbeek et al., 2007; Goddard et al., 2007, 2009; Morren et al., 2007; Ishiyama et al., 2008; Makeeva et al., 2009; Molster et al., 2009; Stewart-Knox et al., 2009; Sturgis et al., 2010; Mai et al., 2011; Smerecnik et al., 2011; Dijkstra et al., 2012; East et al., 2012; Kaphingst et al., 2012, 2015, 2016; Kolor et al., 2012; Nielsen and El-Sohemy, 2012; Haga et al., 2013; Almeling, 2014; Borzekowski et al., 2014; Vermeulen et al., 2014; Waters et al., 2014, 2016; Abrams et al., 2015; Dodson et al., 2015; Etchegary et al., 2015; Graves et al., 2015; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Miyamoto et al., 2016; Schmidlen et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Krakow et al., 2017; Horrow et al., 2019; Jones et al., 2019; Pereira et al., 2019; Middleton et al., 2020) and, less frequently, residential events (Skirton et al., 2006; Morin, 2009; Hahn et al., 2010; Lemke et al., 2010; Bombard et al., 2013; Nicholls et al., 2013; Etchegary et al., 2015; McCormack et al., 2016; Ahmed et al., 2017; Waters et al., 2017; Fournier and Poulain, 2018; Metcalfe et al., 2018; Jones et al., 2019; Rebitschek et al., 2019). Just in few cases more innovative methods, such as a movie or a short video (Sturgis et al., 2010; Mählmann et al., 2016) or a web portal regarding genomics and its implications (Fomous et al., 2006), were adopted.

The results of the present systematic review show that citizens' knowledge on omics is generally poor or very poor (Skirton et al., 2006; Calsbeek et al., 2007; Goddard et al., 2007, 2009; Morren et al., 2007; Ishiyama et al., 2008; Molster et al., 2009; Morin, 2009; Gleason et al., 2010; Hahn et al., 2010; Lemke et al., 2010; Smerecnik et al., 2011; Dijkstra et al., 2012; East et al., 2012; Nielsen and El-Sohemy, 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 (Ricciardi and Boccia, 2017; 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 (Kaphingst et al., 2012; Abrams et al., 2015) and younger age (Mai et al., 2011; 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 (Mai et al., 2011).

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 (Ricciardi and Boccia, 2017), in order to allow them interact with patients and give them satisfactory explanations (Boccia et al., 2017).

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 (Skirton et al., 2006; Morren et al., 2007; Makeeva et al., 2009; Morin, 2009; Stewart-Knox et al., 2009; Hahn et al., 2010; Lemke et al., 2010; Nielsen and El-Sohemy, 2012; Bombard et al., 2013; Nicholls et al., 2013; Almeling, 2014; Mählmann et al., 2016; McCormack et al., 2016; Miyamoto et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Metcalfe et al., 2018). In detail, perceived benefits concentrated in the fields of prevention and treatment (Morren et al., 2007; Morin, 2009; Hahn et al., 2010; Nielsen and El-Sohemy, 2012; Bombard et al., 2013; Nicholls et al., 2013; Miyamoto et al., 2016), and in general were related to a potential improvement in life expectancy (Henneman et al., 2006; Makeeva et al., 2009). Instead, the main concerns of citizens relate to the privacy and use, sharing and access to data (Stewart-Knox et al., 2009; Lemke et al., 2010; Nicholls et al., 2013; Etchegary et al., 2015; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Miyamoto et al., 2016; Metcalfe et al., 2018; Jones et al., 2019; Middleton et al., 2020), job discriminations (Henneman et al., 2006; Makeeva et al., 2009; Lemke et al., 2010; Almeling, 2014; Metcalfe et al., 2018), and the insurance issues (Calsbeek et al., 2007; Morren et al., 2007; Lemke et al., 2010; Haga et al., 2013; Henneman et al., 2013; Miyamoto et al., 2016; Middleton et al., 2020). Other concerns are related to potential consequences of genetic information on working and professional life (Morren et al., 2007; Haga et al., 2013; Miyamoto et al., 2016), costs (Bombard et al., 2013; Nicholls et al., 2013; Metcalfe et al., 2018), access to tests and feasibility of the introduction of genetic tests into clinical practice (Bombard et al., 2013). Few studies have also reported psychological distress in citizens potentially caused by genetic test results (Skirton et al., 2006; Mählmann et al., 2016).

Overall, a positive attitude toward genetic or omics tests was described (Skirton et al., 2006; Calsbeek et al., 2007; Makeeva et al., 2009; Morin, 2009; Stewart-Knox et al., 2009; Mai et al., 2011; Nielsen and El-Sohemy, 2012; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Horrow et al., 2019), even though with some concerns (Henneman et al., 2006, 2013; Morren et al., 2007; Hahn et al., 2010; Bombard et al., 2013; Haga et al., 2013; Nicholls et al., 2013; Vermeulen et al., 2014; Kaphingst et al., 2015; Miyamoto et al., 2016; Metcalfe et al., 2018; Rebitschek et al., 2019). Furthermore, the important role of pre- and post-test genetic consultation was underlined (Morin, 2009; Mai et al., 2011; Almeling, 2014; Mavroidopoulou et al., 2015). Some studies highlighted that key points for appropriateness of genetic tests are curability and preventability of the disease they are addressed to Morren et al. (2007); Vermeulen et al. (2014); Graves et al. (2015); Metcalfe et al. (2018).

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 (Skirton et al., 2006; Morin, 2009; Hahn et al., 2010; Lemke et al., 2010; East et al., 2012; Bombard et al., 2013; Etchegary et al., 2015; Fournier and Poulain, 2018; Rebitschek et al., 2019). The main identified topics to focus for citizens' education were genetic/genomic research (Hahn et al., 2010; Lemke et al., 2010; Dijkstra et al., 2012; Etchegary et al., 2015), disease etiology and susceptibility (Hahn et al., 2010; Kaphingst et al., 2015; Rebitschek et al., 2019), nutrigenomics (Morin, 2009), and genetic and omics tests (Fournier and Poulain, 2018; Rebitschek et al., 2019).

Our results show also a set of potential information strategies, such as TV news, internet, and focus groups (Lemke et al., 2010), Science Cafés with genomic experts (Ahmed et al., 2017), education courses on specific genetic and ethic topics (Gleason et al., 2010), short courses held by experts (East et al., 2012), and an institutional web information portal (Gleason et al., 2010). 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 (Morin, 2009; 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 (Mai et al., 2011; 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 (Skirton et al., 2006; Morin, 2009; 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; Fournier and Poulain, 2018; 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:

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.

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.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.