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Systematic Review ARTICLE

Front. Genet., 23 October 2020 | https://doi.org/10.3389/fgene.2020.570649

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

  • 1Section of Hygiene, University Department of Life Sciences and Public Health, Università Cattolica del Sacro Cuore, Rome, Italy
  • 2Department of Woman and Child Health and Public Health–Public Health Area, Fondazione Policlinico Universitario A. Gemelli Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Rome, Italy

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 (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.

Methods

Search Strategy

An online search was conducted using the following electronic databases: Pubmed, ISI Web of Science and Embase. The search was limited to articles published in English language from January 1, 2003, until May 31, 2020. We used the following terms for the literature search in MEDLINE database: (“omics” OR “genomics” OR “omics sciences”) AND (“knowledge” OR “opinion” OR “perception” OR “awareness” OR “education” OR “literacy”) AND (“citizen*” OR “population” OR “public”). This 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.

Results

Study Selection and Characteristics of Included Studies

Electronic databases search led to the identification of 1,948 articles (381 from Pubmed, 582 from ISI Web of Knowledge, 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.

FIGURE 1
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Figure 1. Study selection process flowchart.

TABLE 1
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Table 1. Studies included in the systematic literature review and their main characteristics.

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) (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), 22% (n = 12) in the European Union (EU27) (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), 9% (n = 5) in Canada (Morin, 2009; Nielsen and El-Sohemy, 2012; Bombard et al., 2013; Nicholls et al., 2013; Etchegary et al., 2015), 6% (n = 3) in UK (Skirton et al., 2006; Sturgis et al., 2010; Jones et al., 2019), 6% (n = 3) in various countries (Stewart-Knox et al., 2009; Pereira et al., 2019; Middleton et al., 2020), 4% (n = 2) in Australia (Molster et al., 2009; Metcalfe et al., 2018), 4% (n = 2) in Japan (Ishiyama et al., 2008; Miyamoto et al., 2016), 2% (n = 1) in Israel (Simonstein and Mashiach-Eizenberg, 2016), 2% (n = 1) in Russia (Makeeva et al., 2009) and, eventually, 2% (n = 1) in Switzerland (Mählmann et al., 2016).

Regarding the target population, most of studies (76%) addressed samples representative of the general population (Fomous et al., 2006; Henneman et al., 2006, 2013; Goddard et al., 2007, 2009; Ishiyama et al., 2008; Makeeva et al., 2009; Molster et al., 2009; Morin, 2009; Stewart-Knox et al., 2009; Hahn et al., 2010; Lemke et al., 2010; Sturgis et al., 2010; Mai et al., 2011; Smerecnik et al., 2011; Dijkstra et al., 2012; East et al., 2012; Kolor et al., 2012; 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; Abrams et al., 2015; Dodson et al., 2015; Etchegary et al., 2015; Graves et al., 2015; Miyamoto et al., 2016; Schmidlen et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Ahmed et al., 2017; Krakow et al., 2017; Fournier and Poulain, 2018; Metcalfe et al., 2018; Jones et al., 2019; Rebitschek et al., 2019; Middleton et al., 2020), while the remaining part involved samples selected based on demographic characteristics (detailed description in Table 1).

In most cases (59%) the initiatives described were promoted by 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).

Overall, 72% of included studies (n = 39) investigated citizens' knowledge (Table 2), 56% (n = 30) attitudes (Table 3), and 20% (n = 11) educational needs (Table 2) in the field of omics sciences, while 52% (n = 28) investigated attitudes and perceptions about genetic and/or omics tests (Table 4). To this end, tools such as questionnaires or surveys were used in 74% (n = 40) of studies (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). Instead, 26% (n =14) reported residential methods, such as meetings, workshop, or focus groups (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). Furthermore, in 4% of the studies (n = 2) a course was developed (Gleason et al., 2010; East et al., 2012), while in 4% of cases (n = 2) a movie or a short video was realized (Sturgis et al., 2010; Mählmann et al., 2016). Lastly, one study (2%) involved the online consultation of a web portal on genomics and its implications (Fomous et al., 2006), and in another one (2%), focused on nutrigenomics, a clinical trial was carried out (Nielsen and El-Sohemy, 2012).

TABLE 2
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Table 2. Citizens' knowledge and educational needs in the field of omics sciences (where investigated).

TABLE 3
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Table 3. Citizens' attitudes on omics sciences (where investigated).

TABLE 4
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Table 4. Citizens' perceptions and attitudes about genetic and/or omics tests (where investigated).

Finally, all the studies included in our systematic review deal with topics related to genomics and genetics or genetic tests, while we found none related to omics in general or to other specific branch of omics sciences such as metabolomics or proteomics.

Knowledge

Among studies investigating citizens' knowledge, 31% (n = 12) aimed to evaluate knowledge on basic concepts in genetics among the general population (Fomous et al., 2006; 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; Miyamoto et al., 2016; 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 (Henneman et al., 2006, 2013; Skirton et al., 2006; Goddard et al., 2007, 2009; Morren et al., 2007; Makeeva et al., 2009; Stewart-Knox et al., 2009; Mai et al., 2011; Kaphingst et al., 2012; Kolor et al., 2012; Haga et al., 2013; Nicholls et al., 2013; Almeling, 2014; Vermeulen et al., 2014; Abrams et al., 2015; Dodson et al., 2015; Graves et al., 2015; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Krakow et al., 2017; Metcalfe et al., 2018; Horrow et al., 2019) (Table 2).

Thirty-eight percent of the studies (n = 15) evaluated citizens' knowledge regarding the role of genetic factors in disease risk (including reproductive risk/fetal disease risk) (Morren et al., 2007; Makeeva et al., 2009; Molster et al., 2009; Hahn et al., 2010; Smerecnik et al., 2011; Nicholls et al., 2013; Borzekowski et al., 2014; Vermeulen et al., 2014; Waters et al., 2014, 2016, 2017; Abrams et al., 2015; Graves et al., 2015; Schmidlen et al., 2016; Simonstein and Mashiach-Eizenberg, 2016) (Table 2).

Furthermore, 15% of the studies (n = 6) addressed the ethical, social and legal implications related to genetic information (Fomous et al., 2006; Makeeva et al., 2009; Gleason et al., 2010; Lemke et al., 2010; Bombard et al., 2013; Almeling, 2014; McCormack et al., 2016). Ten percent (n = 4) of included articles focused on nutrigenomics and/or nutrigenetic tests (Goddard et al., 2007, 2009; Morin, 2009; Nielsen and El-Sohemy, 2012). Lastly, 10% of the studies (n = 4) dealt with the topic of genomics research (Ishiyama et al., 2008; Lemke et al., 2010; Dijkstra et al., 2012; Etchegary et al., 2015).

Study participants had, in most cases (64%, n = 25), a limited knowledge level regarding the abovementioned topics (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) (Table 2). Instead, few studies (26%, n = 10) showed a medium or moderate knowledge level (Henneman et al., 2006; Molster et al., 2009; Haga et al., 2013; Waters et al., 2014, 2016; Abrams et al., 2015; Dodson et al., 2015; Kaphingst et al., 2016; Miyamoto et al., 2016; Krakow et al., 2017). Eventually, just a small number of included studies (10%, n = 4) proved a medium-high or high knowledge level (Waters et al., 2014, 2016; 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) (Mai et al., 2011). 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) (Mai et al., 2011). 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 (Kaphingst et al., 2016). 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 (Kaphingst et al., 2012). 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 (Abrams et al., 2015).

Sources of Citizens' Information

Two studies (5%) investigated the main sources of citizens' information (Goddard et al., 2007; 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.

Attitudes

The topic of citizens' perceptions about benefits and risks related to the use of genomics or omics sciences in medicine was investigated by 56% (n = 30) of the studies included (Henneman et al., 2006, 2013; Skirton et al., 2006; Calsbeek et al., 2007; Morren et al., 2007; Ishiyama et al., 2008; 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; Haga et al., 2013; Nicholls et al., 2013; Almeling, 2014; Vermeulen et al., 2014; Etchegary et al., 2015; Kaphingst et al., 2015, 2016; Mavroidopoulou et al., 2015; Mählmann et al., 2016; McCormack et al., 2016; Miyamoto et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Fournier and Poulain, 2018; Metcalfe et al., 2018; Horrow et al., 2019; Jones et al., 2019; Middleton et al., 2020; Table 3). Most of them (59%, n = 16) showed that participants perceived benefits and usefulness from the use of genomics 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 (lifestyle modification) and treatment (personalization of 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).

The vast majority of study participants report concern on 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), and job discriminations (Henneman et al., 2006; Makeeva et al., 2009; Lemke et al., 2010; Almeling, 2014; Metcalfe et al., 2018) or 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). Three studies (Morren et al., 2007; Haga et al., 2013; Miyamoto et al., 2016) reported public's concern regarding potential consequences of genetic testing results, or in general personal genomics information, on working and professional life. Further issues and concern included costs (Hahn et al., 2010; Bombard et al., 2013; Nicholls et al., 2013; Metcalfe et al., 2018), access to tests and feasibility of the introduction of genetic tests in the health service (Bombard et al., 2013), and psychological distress, fears, and anxiety potentially caused by genetic test results (Skirton et al., 2006; Mählmann et al., 2016).

Regarding perceptions on genetic or omics tests (Table 4), investigated by 52% (n = 28) of the studies (Henneman et al., 2006, 2013; Skirton et al., 2006; Calsbeek et al., 2007; Morren et al., 2007; Makeeva et al., 2009; Morin, 2009; Stewart-Knox et al., 2009; Hahn et al., 2010; Mai et al., 2011; Nielsen and El-Sohemy, 2012; Bombard et al., 2013; Haga et al., 2013; Nicholls et al., 2013; Almeling, 2014; Vermeulen et al., 2014; Etchegary et al., 2015; Graves et al., 2015; Kaphingst et al., 2015; Mavroidopoulou et al., 2015; Mählmann et al., 2016; Miyamoto et al., 2016; Simonstein and Mashiach-Eizenberg, 2016; Fournier and Poulain, 2018; Metcalfe et al., 2018; Horrow et al., 2019; Pereira et al., 2019; Rebitschek et al., 2019), 39% of them highlighted overall positive attitudes among involved individuals (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). However, in 43% of the studies a clear position toward the use of these tests is missing, hence their use in clinical practice remains controversial (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). Moreover, in contrast with the spread of DTC-GTs, the importance of pre- and post-test genetic counseling was underlined (Morin, 2009; Mai et al., 2011; Almeling, 2014; Mavroidopoulou et al., 2015).

In several studies, participants reported that genetic tests would be appropriate only if used for the diagnosis of treatable or preventable diseases (Morren et al., 2007; 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).

Educational Needs

Twenty percent (n = 11) of the studies endorsed the issue of citizens' education (Table 2; 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). Most of them (82%, n = 9) highlighted a clear educational need 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), showing however a lack of proactivity in information seeking (Dijkstra et al., 2012). General population's education should focus, according to study participants, on the following main topics: genetic/genomics 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).

Furthermore, the importance of informed consent process as an educational moment (Kaphingst et al., 2012) 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 (Lemke et al., 2010).

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 (Lemke et al., 2010).

Lastly, 4 studies (8%) investigated methods to increase citizens' literacy, such as Science Cafés with genomics 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). 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 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 14), 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 omics-related 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 large-scale 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.

Funding

This work was supported by the National Center for Disease Prevention and Control (CCM), Italian Ministry of Health (CUP J54I18000300006), and by the ExACT project (Marie Skłodowska-Curie Research and Innovation Staff Exchange–RISE No. 823995).

Conflict of Interest

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.

Acknowledgments

The authors would like to thank Dr. Antonio Federici of the Italian Ministry of Health for his support in the activities of the National Center for Disease Prevention and Control (CCM) project Capacity building and citizens-omics: innovative actions for the literacy of health professionals and citizens in the era of omics sciences.

References

1000 Genomes Project Consortium Auton, A., Brooks, L. D., Durbin, R. M., Garrison, E. P., Kang, H. M., et al. (2015). A global reference for human genetic variation. Nature 526, 68–74. doi: 10.1038/nature15393

PubMed Abstract | CrossRef Full Text | Google Scholar

Abrams, L. R., McBride, C. M., Hooker, G. W., Cappella, J. N., and Koehly, L. M. (2015). The many facets of genetic literacy: assessing the scalability of multiple measures for broad use in Survey research. PLoS ONE 10:e0141532. doi: 10.1371/journal.pone.0141532

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahmed, S. M., DeFino, M., Connors, E., Visotcky, A., Kissack, A., and Franco, Z. (2017). Science Cafés: Transforming citizens to scientific citizens-What influences participants' perceived change in health and scientific literacy? J. Clin. Transl. Sci. 1, 129–134. doi: 10.1017/cts.2016.24

PubMed Abstract | CrossRef Full Text | Google Scholar

Almeling, R. G. S. (2014). Public opinion on policy issues in genetics and genomics. Genet Med. 16, 491–494. doi: 10.1038/gim.2013.175

PubMed Abstract | CrossRef Full Text | Google Scholar

American Society of Human Genetics (2020). Public Attitudes Toward Genetics & Genomics Research Literature and Polling Review Report. Available online at: https://www.ashg.org/wp-content/uploads/2020/01/2020-Public-Views-Genetics-Literature-Review.pdf

Google Scholar

An, J. Y. (2017). National human genome projects: an update and an agenda. Epidemiol Heal. 39:e2017045. doi: 10.4178/epih.e2017045

PubMed Abstract | CrossRef Full Text | Google Scholar

Boccia, S., Federici, A., Siliquini, R., Elisa Calabrò, G, Ricciardi, W., Amoroso, A., et al. (2017). Implementation of genomic policies in Italy: the new National Plan for innovation of the Health System based on omics sciences. Epidemiol Biostat Public Heal. 14, e12782-1–e12782-3. doi: 10.2427/12782

CrossRef Full Text | Google Scholar

Boccia, S., Pastorino, R., Ricciardi, W., Ádány, R., Barnhoorn, F., Boffetta, P., et al. (2019). How to integrate personalized medicine into prevention? recommendations from the Personalized Prevention of Chronic Diseases (PRECeDI) consortium. Public Health Genomics 22, 208–214. doi: 10.1159/000504652

PubMed Abstract | CrossRef Full Text | Google Scholar

Bombard, Y., Abelson, J., Simeonov, D., and Gauvin, F. P. (2013). Citizens' perspectives on personalized medicine: a qualitative public deliberation study. Eur. J. Hum. Genet. 21, 1197–1201. doi: 10.1038/ejhg.2012.300

PubMed Abstract | CrossRef Full Text | Google Scholar

Borry, P. (2010). Statement of the ESHG on direct-to-consumer genetic testing for health-related purposes. Eur. J. Hum. Genet. 18, 1271–1273. doi: 10.1038/ejhg.2010.129

PubMed Abstract | CrossRef Full Text | Google Scholar

Borzekowski, D. L., Guan, Y., Smith, K. C., Erby, L. H., and Roter, D. L. (2014). The Angelina effect: immediate reach, grasp, and impact of going public. Genet Med. 16, 516–521. doi: 10.1038/gim.2013.181

PubMed Abstract | CrossRef Full Text | Google Scholar

Calsbeek, H., Morren, M., Bensing, J., and Rijken, M. (2007). Knowledge and attitudes toward genetic testing: a two year follow-up study in patients with asthma, diabetes mellitus and cardiovascular disease. J. Genet. Couns. 16, 493–504. doi: 10.1007/s10897-006-9085-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Coughlin, S. S. (2014). Toward a road map for global-omics: a primer on -omic technologies. Am. J. Epidemiol. 180, 1188–1195. doi: 10.1093/aje/kwu262

PubMed Abstract | CrossRef Full Text | Google Scholar

Covolo, L., Rubinelli, S., Ceretti, E., and Gelatti, U. (2015). Internet-based direct-to-consumer genetic testing: a systematic review. J. Med. Internet Res. 17:e279. doi: 10.2196/jmir.4378

PubMed Abstract | CrossRef Full Text | Google Scholar

Dijkstra, A. M., Gutteling, J. M., Swart, J. A., Wieringa, N. F., van Derwindt, H. J., and Seydel, E. R. (2012). Public participation in genomics research in the Netherlands: validating a measurement scale. Public Underst Sci. 21, 465–477. doi: 10.1177/0963662510381036

PubMed Abstract | CrossRef Full Text | Google Scholar

Dodson, D. S., Goldenberg, A. J., Davis, M. M., Singer, D. C., and Tarini, B. A. (2015). Parent and public interest in whole-genome sequencing. Public Health Genomics 18, 151–159. doi: 10.1159/000375115

PubMed Abstract | CrossRef Full Text | Google Scholar

East, K. M., Hott, A. M., Callanan, N. P., and Lamb, N. E. (2012). Biotech 101: an educational outreach program in genetics and biotechnology. J. Genet. Couns. 21, 704–712. doi: 10.1007/s10897-012-9491-0

PubMed Abstract | CrossRef Full Text | Google Scholar

ENCODE Project Consortium (2004). The ENCODE (ENCyclopedia of DNA Elements) Project. Science 306, 636–640. doi: 10.1126/science.1105136

CrossRef Full Text | Google Scholar

Etchegary, H., Green, J., Parfrey, P., and Street, C. P. D. (2015). Community engagement with genetics: public perceptions and expectations about genetics research. Heal Expect. 18, 1413–1425. doi: 10.1111/hex.12122

PubMed Abstract | CrossRef Full Text | Google Scholar

Fiske, A., Buyx, A., and Prainsack, B. (2019). Health information counselors. Acad. Med. 94, 37–41. doi: 10.1097/ACM.0000000000002395

PubMed Abstract | CrossRef Full Text | Google Scholar

Fomous, C., Mitchell, J. A., and McCray, A. (2006). “Genetics home reference”: helping patients understand the role of genetics in health and disease. Community Genet. 9, 274–278. doi: 10.1159/000094477

PubMed Abstract | CrossRef Full Text | Google Scholar

Fournier, T., and Poulain, J. P. (2018). Eating according to one's genes? Exploring the french public's understanding of and reactions to personalized nutrition. Qual Heal Res. 28, 2195–2207. doi: 10.1177/1049732318793417

PubMed Abstract | CrossRef Full Text | Google Scholar

Genomics England (2019a). The 100, 000 Genomes Project Protocol. Available online at: https://www.genomicsengland.co.uk/100000-genomes-project-protocol/ (accessed July 12, 2019).

Google Scholar

Genomics England (2019b). The UK has Sequenced 100,000 Whole Genomes in the NHS. Available online at: https://www.genomicsengland.co.uk/the-uk-has-sequenced-100000-whole-genomes-in-the-nhs/ (accessed July 12, 2019).

Google Scholar

Gleason, M. L., Melançon, M. E., and Kleine, K. L. (2010). Using critical literacy to explore genetics and its ethical, legal, and social issues with in-service secondary teachers. CBE Life Sci. Educ. 9, 422–430. doi: 10.1187/cbe.09-09-0065

PubMed Abstract | CrossRef Full Text | Google Scholar

Goddard, K. A., Duquette, D., Zlot, A., Johnson, J., Annis-Emeott, A., Lee, P. W., et al. (2009). Public awareness and use of direct-to-consumer genetic tests: results from 3 state population-based surveys, 2006. Am. J. Public Heal. 99, 442–445. doi: 10.2105/AJPH.2007.131631

PubMed Abstract | CrossRef Full Text | Google Scholar

Goddard, K. A., Moore, C., Ottman, D., Szegda, K. L., Bradley, L., and Khoury, M. J. (2007). Awareness and use of direct-to-consumer nutrigenomic tests, United States, 2006. Genet Med. 9, 510–517. doi: 10.1097/GIM.0b013e31812e6ac3

PubMed Abstract | CrossRef Full Text | Google Scholar

Graves, K. D., Sinicrope, P. S., McCormick, J. B., Zhou, Y., Vadaparampil, S. T., and Lindor, N. M. (2015). Public perceptions of disease severity but not actionability correlate with interest in receiving genomic results: nonalignment with current trends in practice. Public Health Genomics 18, 173–183. doi: 10.1159/000375479

PubMed Abstract | CrossRef Full Text | Google Scholar

Haga, S. B., Barry, W. T., Mills, R., Ginsburg, G. S., Svetkey, L., and Sullivan, J. W. H. (2013). Public knowledge of and attitudes toward genetics and genetic testing. Genet. Test Mol. Biomarkers. 17, 327–335. doi: 10.1089/gtmb.2012.0350

PubMed Abstract | CrossRef Full Text | Google Scholar

Hahn, S., Letvak, S., Powell, K., Christianson, C., Wallace, D., Speer, M., et al. (2010). A community's awareness and perceptions of genomic medicine. Public Health Genomics 13, 63–71. doi: 10.1159/000218712

PubMed Abstract | CrossRef Full Text | Google Scholar

Henneman, L., Timmermans, D. R., and Van Der Wal, G. (2006). Public attitudes toward genetic testing: perceived benefits and objections. Genet Test. 10, 139–145. doi: 10.1089/gte.2006.10.139

PubMed Abstract | CrossRef Full Text | Google Scholar

Henneman, L., Vermeulen, E., van El, C. G., Claassen, L., Timmermans, D. R., and Cornel, M. C. (2013). Public attitudes towards genetic testing revisited: comparing opinions between 2002 and 2010. Eur. J. Hum. Genet. 21, 793–799. doi: 10.1038/ejhg.2012.271

PubMed Abstract | CrossRef Full Text | Google Scholar

Horrow, C., Pacyna, J. E., Sutton, E. J., Sperry, B. P., Breitkopf, C. R., and Sharp, R. R. (2019). Assessing optimism and pessimism about genomic medicine: Development of a genomic orientation scale. Clin. Genet. 95, 704–712. doi: 10.1111/cge.13535

PubMed Abstract | CrossRef Full Text | Google Scholar

Hoxhaj, I., Stojanovic, J., Sassano, M., Acampora, A., and Boccia, S. (2020). A review of the legislation of direct-to-consumer genetic testing in EU member states. Eur. J. Med. Genet. 2020:103841. doi: 10.1016/j.ejmg.2020.103841

PubMed Abstract | CrossRef Full Text | Google Scholar

Hoxhaj, I., Stojanovic, J., Tognetto, A., Sassano, M., Calabrò, G, and Boccia, S. (2019). Citizens' perspectives on genomic sciences and direct-to-consumer genetic tests: systematic reviews. Eur. J. Public Health. 29(Suppl. 4):ckz186.106. doi: 10.1093/eurpub/ckz186.106

CrossRef Full Text | Google Scholar

International Human Genome Sequencing Consortium (2004). Finishing the euchromatic sequence of the human genome. Nature 431, 931–945. doi: 10.1038/nature03001

CrossRef Full Text | Google Scholar

Ishiyama, I., Nagai, A., Muto, K., Tamakoshi, A., Kokado, M., Mimura, K., et al. (2008). Relationship between public attitudes toward genomic studies related to medicine and their level of genomic literacy in Japan. Am. J. Med. Genet. A 146A, 1696–1706. doi: 10.1002/ajmg.a.32322

PubMed Abstract | CrossRef Full Text | Google Scholar

Jones, K. H., Daniels, H., Squires, E., and Ford, D. V. (2019). Public views on models for accessing genomic and health data for research: mixed methods study. J. Med. Internet Res. 21:e14384. doi: 10.2196/14384

PubMed Abstract | CrossRef Full Text | Google Scholar

Kalokairinou, L., Howard, H. C., Slokenberga, S., Fisher, E., Flatscher-Thöni, M., Hartlev, M., et al. (2018). Legislation of direct-to-consumer genetic testing in Europe: a fragmented regulatory landscape. J. Community Genet. 9, 117–132. doi: 10.1007/s12687-017-0344-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Kaphingst, K. A., Blanchard, M., Milam, L., Pokharel, M., Elrick, A., and Goodman, M. S. (2016). Relationships between health literacy and genomics-related knowledge, self-efficacy, perceived importance, and communication in a medically underserved Population. J Heal Commun. 21(Suppl. 1):58–68. doi: 10.1080/10810730.2016.1144661

PubMed Abstract | CrossRef Full Text | Google Scholar

Kaphingst, K. A., Facio, F. M., Cheng, M. R., Brooks, S., Eidem, H., Linn, A., et al. (2012). Effects of informed consent for individual genome sequencing on relevant knowledge. Clin Genet. 82, 408–415. doi: 10.1111/j.1399-0004.2012.01909.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Kaphingst, K. A., Stafford, J. D., McGowan, L. D., Seo, J., and Lachance, C. R. (2015). Effects of racial and ethnic group and health literacy on responses to genomic risk information in a medically underserved population. Heal Psychol. 34, 101–110. doi: 10.1037/hea0000177

PubMed Abstract | CrossRef Full Text | Google Scholar

Kolor, K., Duquette, D., Zlot, A., Foland, J., Anderson, B., Giles, R., et al. (2012). Public awareness and use of direct-to-consumer personal genomic tests from four state population-based surveys, and implications for clinical and public health practice. Genet Med. 14, 860–867. doi: 10.1038/gim.2012.67

PubMed Abstract | CrossRef Full Text | Google Scholar

Krakow, M., Ratcliff, C. L., Hesse, B. W., and Greenberg-Worisek, A. J. (2017). Assessing genetic literacy awareness and knowledge gaps in the us population: results from the Health Information National Trends Survey. Public Health Genomics 20, 343–348. doi: 10.1159/000489117

PubMed Abstract | CrossRef Full Text | Google Scholar

Lea, D. H., Kaphingst, K. A., Bowen, D., Lipkus, I., and Hadley, D. W. (2011). Communicating genetic and genomic information: health literacy and numeracy considerations. Public Health Genomics 14, 279–289. doi: 10.1159/000294191

PubMed Abstract | CrossRef Full Text | Google Scholar

Lemke, A. A., Wolf, W. A., Hebert-Beirne, J., and Smith, M. E. (2010). Public and biobank participant attitudes toward genetic research participation and data sharing. Public Health Genomics.13, 368–377. doi: 10.1159/000276767

PubMed Abstract | CrossRef Full Text | Google Scholar

LePoire, E., Basu, B., Walker, L., and Bowen, D. J. (2019). What do people think about genetics? a systematic review. J. Community Genet. 10, 171–187. doi: 10.1007/s12687-018-0394-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Lin, J., and Qian, J. (2007). Systems biology approach to integrative comparative genomics. Exp. Rev. Proteomics 4, 107–119. doi: 10.1586/14789450.4.1.107

PubMed Abstract | CrossRef Full Text | Google Scholar

Mählmann, L., Röcke, C., Brand, A., Hafen, E., and Vayena, E. (2016). Attitudes towards personal genomics among older Swiss adults: an exploratory study. Appl. Transl. Genom. 8, 9–15. doi: 10.1016/j.atg.2016.01.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Mai, Y., Koromila, T., Sagia, A., Cooper, D. N., Vlachopoulos, G., Lagoumintzis, G., et al. (2011). A critical view of the general public's awareness and physicians' opinion of the trends and potential pitfalls of genetic testing in Greece. Per Med. 8, 551–561. doi: 10.2217/pme.11.48

PubMed Abstract | CrossRef Full Text | Google Scholar

Makeeva, O. A., Markova, V. V., and Puzyrev, V. P. (2009). Public interest and expectations concerning commercial genotyping and genetic risk assessment. Per Med. 6, 329–341. doi: 10.2217/pme.09.14

PubMed Abstract | CrossRef Full Text | Google Scholar

Martin, N. A., Friedman, S. J., Saxton, C., Yarden, R., Lindsey, S., Kuhn, E., et al. (2020). Using consistent terms in precision medicine to eliminate patient confusion. J. Clin. Oncol. 38(Suppl. 15):e24164. doi: 10.1200/JCO.2020.38.15_suppl.e24164

CrossRef Full Text | Google Scholar

Mavroidopoulou, V., Xera, E., and Mollaki, V. (2015). Awareness, attitudes and perspectives of direct-to-consumer genetic testing in Greece: a survey of potential consumers. J. Hum. Genet. 60, 515–523. doi: 10.1038/jhg.2015.58

PubMed Abstract | CrossRef Full Text | Google Scholar

McCormack, P., Kole, A., Gainotti, S., Mascalzoni, D., Molster, C., and Lochmüller, H. W. S. (2016). “You should at least ask”. The expectations, hopes and fears of rare disease patients on large-scale data and biomaterial sharing for genomics research. Eur J Hum Genet. 24, 1403–1408. doi: 10.1038/ejhg.2016.30

PubMed Abstract | CrossRef Full Text | Google Scholar

Metcalfe, S. A., Hickerton, C., Savard, J., Terrill, B., Turbitt, E., Gaff, C., et al. (2018). Australians' views on personal genomic testing: focus group findings from the Genioz study. Eur. J. Hum. Genet. 26, 1101–1112. doi: 10.1038/s41431-018-0151-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Middleton, A., Milne, R., Howard, H., Niemiec, E., Robarts, L., Critchley, C., et al. (2020). Members of the public in the USA, UK, Canada and Australia expressing genetic exceptionalism say they are more willing to donate genomic data. Eur. J. Hum. Genet. 28, 424–434. doi: 10.1038/s41431-019-0550-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Miyamoto, K., Iwakuma, M., and Nakayama, T. (2016). Experiences and attitudes of residents regarding a community-based genome cohort study in Japan: a population-based, cross-sectional study. BMC Med Genomics 9:14. doi: 10.1186/s12920-016-0175-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Moher, D., Liberati, A., Tetzlaff, J., and Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6:e1000097. doi: 10.1371/journal.pmed.1000097

CrossRef Full Text | Google Scholar

Molster, C., Charles, T., Samanek, A., and O'Leary, P. (2009). Australian study on public knowledge of human genetics and health. Public Health Genomics 12, 84–91. doi: 10.1159/000164684

PubMed Abstract | CrossRef Full Text | Google Scholar

Morin, K. (2009). Knowledge and attitudes of Canadian consumers and health care professionals regarding nutritional genomics. OMICS 13, 37–41. doi: 10.1089/omi.2008.0047

PubMed Abstract | CrossRef Full Text | Google Scholar

Morren, M., Rijken, M., Baanders, A. N., and Bensing, J. (2007). Perceived genetic knowledge, attitudes towards genetic testing, and the relationship between these among patients with a chronic disease. Patient Educ. Couns. 65, 197–204. doi: 10.1016/j.pec.2006.07.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Nicholls, S. G., Wilson, B. J., Craigie, S. M., Etchegary, H., Castle, D., Carroll, J. C., et al. (2013). Public attitudes towards genomic risk profiling as a component of routine population screening. Genome 56, 626–633. doi: 10.1139/gen-2013-0070

PubMed Abstract | CrossRef Full Text | Google Scholar

Nielsen, D. E., and El-Sohemy, A. (2012). A randomized trial of genetic information for personalized nutrition. Genes Nutr.7, 559–566. doi: 10.1007/s12263-012-0290-x

CrossRef Full Text | Google Scholar

Pereira, N. L., So, D., Bae, J. H., Chavez, I., Jeong, M. H., Kim, S. W., et al. (2019). International survey of patients undergoing percutaneous coronary intervention and their attitudes toward pharmacogenetic testing. Pharmacogenet. Genomics 29, 76–83. doi: 10.1097/FPC.0000000000000368

PubMed Abstract | CrossRef Full Text | Google Scholar

Rebitschek, F. G., Reisel, D., Lein, I., and Wegwarth, O. (2019). Epigenetic risk assessment of female cancers: women's information needs and attitudes. Public Health Genomics 22, 46–57. doi: 10.1159/000501975

PubMed Abstract | CrossRef Full Text | Google Scholar

Ricciardi, W., and Boccia, S. (2017). New challenges of public health: Bringing the future of personalised healthcare into focus. Eur J Public Health. Oxford University Press 27, 36–39. doi: 10.1093/eurpub/ckx164

PubMed Abstract | CrossRef Full Text | Google Scholar

Schmidlen, T. J., Scheinfeldt, L., Zhaoyang, R., Kasper, R., Sweet, K., Gordon, E. S., et al. (2016). Genetic knowledge among participants in the coriell personalized medicine collaborative. J Genet Couns. 25, 385–394. doi: 10.1007/s10897-015-9883-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Simonstein, F., and Mashiach-Eizenberg, M. (2016). Reprogenetics, genetic tools and reproductive risk: attitudes and understanding among ethnic groups in Israel. J Genet Couns. 25, 127–134. doi: 10.1007/s10897-015-9850-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Skirton, H., Frazier, L. Q., Calvin, A. O., and Cohen, M. Z. (2006). A legacy for the children–attitudes of older adults in the United Kingdom to genetic testing. J Clin Nurs. 15, 565–573. doi: 10.1111/j.1365-2702.2006.01372.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Smerecnik, C. M., Mesters, I., de Vries, N. K., and de Vries, H. (2011). Applying a theory-based framework to understand public knowledge of genetic risk factors: a case for the distinction between how-to knowledge and principles knowledge. Public Health Genomics. 14, 259–270. doi: 10.1159/000294149

PubMed Abstract | CrossRef Full Text | Google Scholar

Stewart-Knox, B. J., Bunting, B. P., Gilpin, S., Parr, H. J., Pinhão, S., Strain, J. J., et al. (2009). Attitudes toward genetic testing and personalised nutrition in a representative sample of European consumers. Br J Nutr. 101, 982–989. doi: 10.1017/S0007114508055657

PubMed Abstract | CrossRef Full Text | Google Scholar

Sturgis, P., Brunton-Smith, I., and Fife-Schaw, C. (2010). Public attitudes to genomic science: an experiment in information provision. Public Underst Sci. 19, 166–180. doi: 10.1177/0963662508093371

PubMed Abstract | CrossRef Full Text | Google Scholar

Su, P. (2013). Direct-to-consumer genetic testing: a comprehensive view. Yale J. Biol. Med. 86, 359–365.

PubMed Abstract | Google Scholar

Tebani, A., Afonso, C., Marret, S., and Bekri, S. (2016). Omics-based strategies in precision medicine: toward a paradigm shift in inborn errors of metabolism investigations. Int. J. Mol. Sci. 17:1555. doi: 10.3390/ijms17091555

PubMed Abstract | CrossRef Full Text | Google Scholar

The International HapMap Consortium (2003). The International hapmap project. Nature 426, 789–796. doi: 10.1038/nature02168

CrossRef Full Text | Google Scholar

Turnbull, C., Scott, R. H., Thomas, E., Jones, L., Murugaesu, N., Pretty, F. B., et al. (2018). The 100, 000 genomes project: bringing whole genome sequencing to the NHS. BMJ 361:k1687. doi: 10.1136/bmj.k1687

PubMed Abstract | CrossRef Full Text | Google Scholar

van Dijk, E. L., Auger, H., Jaszczyszyn, Y., and Thermes, C. (2014). Ten years of next-generation sequencing technology. Trends Genet. 30, 418–426. doi: 10.1016/j.tig.2014.07.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Vermeulen, E., Henneman, L., van El, C. G., and Cormal, C. M. (2014). Public attitudes towards preventive genomics and personal interest in genetic testing to prevent disease: a survey study. Eur J Public Heal. 24, 768–775. doi: 10.1093/eurpub/ckt143

PubMed Abstract | CrossRef Full Text | Google Scholar

Waters, E. A., Ball, L., and Gehlert, S. (2017). “I don't believe it.” Acceptance and skepticism of genetic health information among African-American and White smokers. Soc Sci Med. 184, 153–160. doi: 10.1016/j.socscimed.2017.04.053

PubMed Abstract | CrossRef Full Text | Google Scholar

Waters, E. A., Muff, J., and Hamilton, J. G. (2014). Multifactorial beliefs about the role of genetics and behavior in common health conditions: prevalence and associations with participant characteristics and engagement in health behaviors. Genet Med. 16, 913–921. doi: 10.1038/gim.2014.49

PubMed Abstract | CrossRef Full Text | Google Scholar

Waters, E. A., Wheeler, C., and Hamilton, J. G. (2016). How are information seeking, scanning, and processing related to beliefs about the roles of genetics and behavior in cancer causation? J Heal Commun. 21(Suppl 2):6–15. doi: 10.1080/10810730.2016.1193917

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: citizens' literacy, omics sciences, genetic/omics knowledge, public attitudes, educational needs, systematic review, personalized medicine

Citation: Calabrò GE, Sassano M, Tognetto A and Boccia S (2020) Citizens' Attitudes, Knowledge, and Educational Needs in the Field of Omics Sciences: A Systematic Literature Review. Front. Genet. 11:570649. doi: 10.3389/fgene.2020.570649

Received: 08 June 2020; Accepted: 22 September 2020;
Published: 23 October 2020.

Edited by:

Daniel Strech, Charité – Universitätsmedizin Berlin, Germany

Reviewed by:

Thomas Reydon, Leibniz University Hannover, Germany
Gabriele Werner-Felmayer, Innsbruck Medical University, Austria

Copyright © 2020 Calabrò, Sassano, Tognetto and Boccia. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Giovanna Elisa Calabrò, alisacalabro@icloud.com

These authors have contributed equally to this work