Genomics knowledge and attitudes among European public health professionals: Results of a cross-sectional survey.

BACKGROUND: The international public health (PH) community is debating the opportunity to incorporate genomic technologies into PH practice. A survey was conducted to assess attitudes of the European Public Health Association (EUPHA) members towards their role in the implementation of public health genomics (PHG), and their knowledge and attitudes towards genetic testing and the delivery of genetic services.
METHODS: EUPHA members were invited via monthly newsletter and e-mail to take part in an online survey from February 2017 to January 2018. A descriptive analysis of knowledge and attitudes was conducted, along with a univariate and multivariate analysis of their determinants.
RESULTS: Five hundred and two people completed the questionnaire, 17.9% were involved in PHG activities. Only 28.9% correctly identified all medical conditions for which there is (or not) evidence for implementing genetic testing; over 60% thought that investing in genomics may divert economic resources from social and environmental determinants of health. The majority agreed that PH professionals may play different roles in incorporating genomics into their activities. Better knowledge was associated with positive attitudes towards the use of genetic testing and the delivery of genetic services in PH (OR = 1.48; 95% CI 1.01-2.18).
CONCLUSIONS: Our study revealed quite positive attitudes, but also a need to increase awareness on genomics among European PH professionals. Those directly involved in PHG activities tend to have a more positive attitude and better knowledge; however, gaps are also evident in this group, suggesting the need to harmonize practice and encourage greater exchange of knowledge among professionals.

1. Introduction

The development of precision medicine (PM, also referred to as “personalized medicine”) has generated a debate within the international public health (PH) community on the opportunity to use genetic information and genomic applications in preventive medicine. However, the introduction of PM interventions into PH practice is still controversial. On one hand, the more skeptical have argued that investing in genomics may divert resources away from basic public health services and from addressing the structural causes of ill health [1-4]. On the other hand, public health professionals and associations worldwide have stressed that the potential of PM to identify high risk individuals and develop tailored preventive interventions cannot be ignored [5-8].

Over recent decades, several professionals have supported the incorporation of genome-based knowledge and technologies into PH, leading to the emergence of public health genomics (PHG) as a multidisciplinary field promoting the appropriate translation of genomics research into health benefits for individuals and populations [9,10]. PH professionals may play different roles in this translation, from evaluating the effectiveness and cost-effectiveness of genomic applications to modelling and assessing the implementation of evidence-based genomic applications into medical practice [9]. One of the priorities of the PHG movement is to achieve adequate knowledge and capacity among PH professionals to facilitate the integration of genomic information into PH activities [11-15]. What is the current level of competence of PH professionals in genomics? Several surveys have been performed to evaluate the knowledge, attitudes and professional behavior of physicians towards the integration of human genomic discoveries into clinical practice [16-21], but only one study targeted PH practitioners [22] and it focused solely on predictive genetic tests for chronic diseases. We conducted a survey on a sample of European PH professionals belonging to the network of the European Public Health Association (EUPHA), which represents European PH professionals, to assess their attitudes towards their role in the implementation of PHG, and their knowledge and attitudes regarding genetic testing and genetic services.

2. Material and methods

The study was conducted within the EU-funded project PRECeDI (Personalized PREvention of Chronic DIseases).

A specific questionnaire was developed for the survey, consisting of 33 items grouped into five sections (see S1 Text):

Professional details (four questions);

Professional activity (seven questions);

Knowledge of genetic testing and delivery of genetic services (four questions);

Attitudes towards genetic testing and delivery of genetic services (four questions);

Attitudes towards the role of PH professionals in PHG (six questions).

“The development of the questionnaire was informed by a literature review and by similar studies previously carried out by the same research group [18, 22]. It was also based on the inputs received by the members of EUPHA Section on PHG and by all partners of PRECeDI project, as described elsewhere [23]

“For the purpose of the survey, we defined genetic testing as “performing a type of medical test involving an analysis of human chromosomes, DNA, RNA, genes, and/or gene products (e.g., enzymes and other types of proteins), which is predominately used to detect heritable or somatic mutations, genotypes, or phenotypes related to disease and health”, following the definition proposed by Burke [24]. Further to discussion with other PRECEDI project partners, we have decided to adopt the classification of genetic testing used by the European Society of Human Genetics [25]. In particular, the survey was aimed at investigating knowledge and attitudes towards the implementation of susceptibility (also known as predisposition) tests, defined as “the detection of genetic variants that are associated with an increased risk of disease but cannot predict with certainty the development of disease, because of the incomplete penetrance of the genetic mutation”. Examples of this type of tests include BRCA testing, Lynch syndrome testing and familial hypercholesterolemia genetics tests. A “genetic service” was defined as “the provisions to diagnose, advise and treat individuals with risk factors for genetic disorders.” According to our interpretation, the delivery of a genetic service is therefore expected to provide not only genetic testing and counselling, but also treatment and follow up of individuals with genetic disorders, similarly to what was previously described by Battista et al.[26]. Statements included in section E were based on published literature dealing with the relationship between public health and human genomics and the possible role of public health professionals in putting PHG into practice [27] A filter question included in section B gave access to an extended version of the questionnaire, including four additional items in both sections C and D, for professionals who answered that they were involved in PHG activities. A pilot phase of the survey was conducted on 61 staff members of the Department of Public Health and Infectious Diseases of Sapienza University in Rome and 10 members of the Department of Genetics from the Vrije University in Amsterdam, to test clarity of language, practicability and interpretation of answers. Internal consistency was also assessed by obtaining Cronbach’s alpha coefficients. The questionnaire proved to be reliable in assessing attitudes towards the role of PH professionals in PHG, and it was slightly revised before distribution to the EUPHA network to improve the quality of some questions [23].

The questionnaire was administered online from March 2017 to February 2018. An invitation to participate in the survey was included in the EUPHA monthly newsletter of February 2017; furthermore, the Presidents of five EUPHA sections (Public Health Genomics, Public Health Epidemiology, Public Health Monitoring and Reporting, Public Health Practice and Policy, Chronic Diseases) sent an invitation to their members to respond to the survey. A final reminder was sent to all EUPHA members in September 2017. The first page of the survey included a description of its objective and of the different section of the questionnaire, and informed participants that all data collected were anonymous. Thus, no consent was requested to participate in the survey. The Ethical Committee of Sapienza University of Rome granted its approval to conduct the survey.

Survey responses were collected in an electronic spreadsheet (see S1 Dataset). A descriptive analysis was performed to define the distribution of socio-demographic characteristics of the sample and to assess rates of positive/negative attitudes towards and knowledge of PHG (frequencies, percentages, mean values and SD were calculated). An analysis of determinants of knowledge and attitudes on genetic testing and the delivery of genetic services, and on the roles of PH professionals in incorporating genomics into PH activities was conducted through the construction of multiple logistic regression models. The variables “knowledge on PHG”, “attitudes on PHG” and “attitudes on the role of PH professionals” originally consisting of multiple categories, were collapsed into two levels, adapting the methodology previously used in other surveys conducted by our research group [18, 22, 28]: a high level of knowledge of PHG was attributed to respondents providing correct responses to at least three of four questions included in section C of the questionnaire; positive attitudes towards PHG were defined as positive attitudes towards the three statements included in section D of questionnaire, except for question D1, which was excluded because it showed a totally different trend in the univariate analysis; for “attitudes on the role of PH professionals”, responders with positive attitudes were those who agreed with all six statements included in section E. Covariates included in the models were: group of professionals (involved in PHG activities vs not involved), gender, age, history of genetic conditions, exposure to information on genetic testing during undergraduate or post-graduate education, area of degree (with medicine as reference category), sector of work (with the academic sector chosen as reference), main area of work.

Multiple logistic regression models were built using the strategy suggested by Hosmer and Lemeshow [29]. Each variable was examined by univariate analysis using the appropriate statistical test (Student’s t-test or χ2 test) and was included in the model when the p-value was less than 0.25. Subsequently, multivariate logistic regression with backward elimination of any variable that did not contribute to the model on the grounds of the Likelihood Ratio test (cut-off, p  =  0.05) was performed. Adjusted odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. All statistical calculations were performed using Stata version 15.0 (Stata Corporation, College Station, TX, USA).

Approval to conduct the study was granted from the Ethics Committee of Sapienza University of Rome.

3. Results

Six hundred and twenty-two people accessed the survey and 502 completed all sections (80.7%). Respondents came from all EU28 Countries and some non–EU Countries, including Albania (n = 1), Andorra (n = 1), Bosnia and Herzegovina (n = 4), Norway (n = 15), Russia (n = 1), Serbia (n = 3), Switzerland (n = 25), Turkey (n = 7), and there were 27 people working in developing countries at the time the survey was conducted The response rate obtained was approximately 10%. Table 1 summarizes the main socio-demographic characteristics of the respondents. There were no significant differences in the socio-demographic characteristics between people who completed the whole survey and those who did not, except for the area of degree, with medical doctors being less likely to complete it (p = 0.026).

Table 1

Socio-demographic characteristics of respondents.

CHARACTERISTICS	N	(%)
Gender (n = 593)*
Female	287	48.4
Male	306	51.6
Age (n = 591)*
25–40	197	33.3
41–55	219	37.1
56–75	175	29.6
Type of health professional (n = 576)*
PH professional not involved in PHG	440	76.4
PH professional involved in PHG	57	9.9
Not PH professional and not involved in PHG	27	4.7
Not PH professional but involved in PHG	52	9.0
Area of degree (n = 574)*
Medicine	295	51.4
Health professions (e.g nursing)	50	8.7
Biology	30	5.2
Public health	73	12.7
Other (e.g. statistics, political sciences)	126	21.9
Sector of work (n = 573)*
Academic	337	58.8
Hospital	28	4.9
Government (national or local)	113	19.7
Public health service	33	5.8
Other (e.g. NGO, technical agency)	62	10.8
Information on genetic screening in undergraduate training (n = 573)*
Yes	242	57.8
No	331	42.2
Information on genetic screening in postgraduate training (n = 574)*
Yes	245	42.7
No	278	48.4
Not applicable	51	8.9

*Number of respondents to the question.

For knowledge of genetic testing, only 1.7% of respondents (9/526) correctly identified all applications of genetic testing that are based (or not based) on evidence of effectiveness, while 26.1% correctly identified at least eight out of 10 (141/526), which we set as the threshold for a correct response to this question (Table 2). Nearly 30% of respondents correctly identified all clinical conditions for which there is (or is not) strong evidence supporting the use of a genetic test (CDC tier-1) (Table 2). When asked about the professionals involved in the delivery of genetic testing, nearly 50% of respondents (49.4%, 256/518) correctly indicated that such professionals could equally be general practitioners or geneticists or oncologists (Table 2). Most respondents (91.0%, 472/519) knew that predictive/predisposition genetic tests must be associated with genetic counseling (Table 2).

Table 2

Knowledge of genetic testing and the delivery of genetic services, n (%).

Which of the following applications of genetic testing are based on evidence of effectiveness? (multiple answers are possible) (n = 526)*a	No	Yes
Diagnose disease	189 (35.9)	337 (64.1)
Determine the severity of a disease	420 (79.8)	106 (20.2)
Identify genetic mutations that are responsible for an already diagnosed disease	209 (39.7)	317 (60.3)
Identify genetic mutations that may increase the risk of developing a disease	139 (26.4)	387 (73.6)
Identify genetic mutations that could be passed on to children	163 (31.0)	363 (69.0)
Identify genetic mutations that influence the process of ageing	427 (81.2)	99 (18.8)
Guide doctors in deciding on the best treatment to use for certain individuals	276 (52.5)	250 (47.5)
Guide doctors in designing an optimal individualized weight loss diet	489 (93.0)	37 (7.0)
Ascertain the gender of a fetus	354 (67.3)	172 (32.7)
Screen newborn babies for certain treatable conditions	187 (35.6)	339 (64.4)
For which of the following clinical conditions is there currently a base of synthesized evidence supporting the implementation of genetic testing to predict disease risk? (multiple answers are possible) (n = 525)*b	No	Yes
Hereditary ovarian cancer	138 (26.3)	387 (73.7)
Lynch syndrome (hereditary nonpolyposis colorectal cancer)	231 (44.0)	294 (56.0)
Gastric cancer	461 (87.8)	65 (12.2)
Metastatic non-small-cell lung cancer	470 (89.5)	55 (10.5)
Prostate cancer	452 (86.1)	73 (13.9)
Alzheimer’s disease	370 (70.5)	155 (29.5)
Familial hypercholesterolemia	264 (50.3)	261 (49.7)
Type 2 diabetes	413 (78.7)	112 (21.3)
Acute myeloid leukemia	447 (85.1)	78 (14.9)
Depression	487 (92.8)	38 (7.2)
Which of the following professionals may be involved in the delivery of genetic testing?(n = 509)*
A. General practitioner		9 (1.7)
B. Geneticist		61 (11.8)
C. Oncologist		9 (1.7)
D. All of the above		256 (49.4)
E. B+C		183 (35.3)
Performing susceptibility (or predisposition) tests should necessarily be associated with genetic counseling that includes information, informed consent, and discussion of the results (n = 519)*
Agree		472 (91.0)
Uncertain		35 (6.7)
Disagree		12 (2.3)

*Number of respondents to the question.

aA correct response to the question was defined as having correctly identified at least 8/10 applications of genetic testing that are based (or not) on evidence of effectiveness.

bA correct response to the question was defined as having correctly identified all conditions for which there is (or is not) currently evidence supporting the implementation of genetic testing.

Percentages referring to correct answers are in bold.

In the subgroup analysis on PH professionals declaring an involvement in PHG activities, only 12.1% of them (4/33) correctly indicated the number of clinical conditions with available evidence supporting the implementation of a genetic test to predict disease risk, while 32.1% (15/53) correctly identified all components of a genetic service; in particular, less than half of respondents thought that treatment, follow-up and clinical surveillance can also be considered within the components of a genetic service (respectively 37.7%, 49.1%, and 47.2%) (see Tables 2_bis in S1).

Most respondents showed positive attitudes towards the implementation of genetic testing and the delivery of genetic services, except for the idea that it would be more important to invest resources in the social and environmental causes of ill health than in the implementation of genetic testing, with over 60% of the sample agreeing with this statement (Table 3).

Table 3

Attitudes towards genetic testing and the delivery of genetic services, and towards the role of PH professionals in PHG (% of answers).

Statement	Strongly agree	Agree	Neither agree nor disagree	Disagree	Strongly disagree
It is more important to invest resources in the social and environmental causes of ill health than in the implementation of genetic testing (n = 522)*	27.6%	32.8%	25.3%	13.2%	1.1%
Susceptibility (or predisposition) tests should be introduced in the clinical and public health practice even without health interventions with proven efficacy (n = 522)*	3.0%	12.8%	10.0%	41.6%	32.6%
Susceptibility (or predisposition) tests should be introduced in the clinical and public health practice only if economic evaluations show cost-effectiveness ratios favorable compared with alternative health interventions (n = 522)*	14.2%	44.5%	18.8%	18.8%	3.6%
Genetic tests for diseases that could have a fatal outcome (e.g. BRCA testing for breast and ovarian cancer) should be provided free at the point of delivery to people who could benefit from them (n = 522)*	28.3%	43.7%	11.5%	12.3%	4.2%
Public health thinking should consider that risk factors can affect subsets of the population differently based on genetic susceptibility. (n = 507)*	26.6%	61.7%	6.9%	3.8%	1.0%
Public health professionals should be involved in the continuous assessment of the utility and validity of emerging genomic applications (n = 507)*	37.6%	52.3%	8.1%	1.8%	0.2%
Public health programs should actively implement genomic applications that are evidence-based (e.g. BRCA testing for relatives of known mutation carriers). (n = 507)*	27.2%	51.5%	17.4%	3.7%	0.2%
Public health professionals should measure the utilization of genetic services in order to assess unmet needs and inequalities of access to services (n = 507)*	29.9%	50.7%	14.8%	2.8%	1.8%
Public health professionals should measure in practice outcomes, process indicators and value added of genomic applications (n = 507)*	34.4%	49.2%	13.8%	1.8%	0.8%
I think that in the future public health programmes (e.g. cancer screening, chronic diseases prevention programmes) will make a greater use of genetic information. (n = 507)*	29.8%	55.6%	12.6%	1.8%	0.2%

*Number of respondents to the question.

Percentages referring to positive attitudes towards genetic testing and delivery of genetic services, and towards the proposed roles of PH professionals are in bold.

Positive attitudes were also reported in the extended version addressed to professionals involved in PHG, ranging from 77.6% of respondents (38/49) indicating that the application of genetic testing in healthy family members of individuals with hereditary chronic diseases may increase prevention opportunities to 98.0% (48/49) agreeing (or strongly agreeing) that specific training initiatives are needed for PH professionals to develop their capacity to evaluate the quality of genetic services (see Tables 3_bis in S1).

There were high rates of agreement with the proposed roles that PH professionals may play in putting PHG into practice (Table 3). In particular, percentages of agreement ranged from 88.4% of respondents (448/507) who agreed (or strongly agreed) that public health thinking should consider that risk factors can affect subsets of the population differently based on genetic susceptibility to 78.7% of respondents (399/507) who agreed (or strongly agreed) that public health programs should actively implement genomic applications that are evidence-based (e.g. BRCA testing for relatives of known mutation carriers) (Table 3).

Table 4 summarizes the results of the multivariate analysis. A high level of knowledge was associated with indicating PHG as one of the main areas of work, having graduated in medicine, having received training on genetic testing during undergraduate education and working in a PH service. A high level of knowledge of genetic testing and genetic services was associated with positive attitudes towards PHG, while academics were less likely to be positive on the topic. People working directly in PHG were more likely to disagree with the importance of investing resources in social and environmental causes of health rather than in genomics. Finally, positive attitudes towards the role of PH professionals in implementing PHG were associated with working in PHG and with having received information on PHG during undergraduate training.

Table 4

Multivariate analysis of determinants of knowledge and attitudes (only significant results shown).

Variables	OR	95% CI	P value
Model 1: Higher level of knowledge of genetic testing and the delivery of genetic servicesa
PHG as main area of work (0 = no, 1 = yes)	6.35	2.62–15.33	0.000
Information on PHG during undergraduate training (0 = no, 1 = yes)	1.53	1.02–2.30	0.040
Area of degree (0 = other, 1 = medicine)	1.77	1.16–2.69	0.007
Sector of work (0 = other, 1 = public health service)	1.98	1.05–3.73	0.000
Model 2: Positive attitudes towards genetic testing and delivery of genetic servicesb
Sector of work (0 = other, 1 = Academic)	0.67	0.47–0.97	0.032
Knowledge (0 = score≤ 2, 1 = score 3, 4	1.48	1.01–2.18	0.048
Model 3: Positive attitudes towards the use of resources for genetic testingc
PHG as main area of work (0 = no, 1 = yes)	9.10	3.95–20.94	0.000
Model 4: Positive attitudes towards the role of PH professionals in PHGd
PHG main area of work (0 = no, 1 = yes)	4.04	1.48–11.02	0.006
Information on genetic testing during undergraduate training (0 = no, 1 = yes)	1.74	1.21–2.48	0.003

a Respondents were classified as those who answered correctly to three out of four questions addressing knowledge of genetic testing and the delivery of genetic services (Table 2) vs. all others.

b Respondents were classified as those who showed a positive attitude towards all the statements addressing attitudes towards genetic testing (Table 3) except the first one, which was analyzed separately.

c Respondents were divided into those who declared they disagreed or strongly disagreed with the statement “It is more important to invest resources in the social and environmental causes of ill health than in the implementation of genetic testing”(value = 1) vs all others (value = 0).

d Respondents were classified as those who showed a positive attitude towards all the statements addressing the possible role of PH professionals in implementing PHG vs all others.

4. Discussion

This survey revealed poor knowledge of genetic testing and the delivery of genetic services in a representative sample of European PH professionals. However, overall, attitudes towards both the use of genetic testing and delivery of genetic services, and the involvement of PH professionals in putting PHG into practice, were positive. The only negative sentiment was in response to the proposal that it was more important to invest resources in the social and environmental causes of ill health than in the implementation of genetic testing. Over 60% of respondents agreed in fact that public health resources should be targeted mainly at addressing the structural causes of ill health.

Nevertheless, over 70% of participants agreed that genetic tests for diseases that could have a fatal outcome (e.g. BRCA testing for breast and ovarian cancer) should be provided free at the point of delivery for those who could benefit from them. High rates of respondents also thought that, in the future, PH programmes (e.g. cancer screening, chronic disease prevention programmes) will make greater use of genetic information. Therefore, PH professionals seem to agree in principle with the importance of including genomic applications in PH practice, but at the same time they seem to fear that this could divert resources from addressing the “traditional” determinants of health. There is a long-standing debate in the PH community on the opportunity to focus on -omics and personalized medicine, and whether this may divert from the traditional population-based approach. However, the need to go beyond the dichotomous high-risk versus population approach was suggested, taking into account that also precision public health could contribute to improving population health and achieving social justice—equity, social inclusion, and empowerment [5].

Given the cost constraints currently faced by European healthcare systems, some prioritization criteria are needed to decide which genetic services should be funded from public budgets [30], and these should include consideration of medical benefit, health needs and costs. In this regard, a high proportion of respondents agreed with the idea that evidence on effectiveness and cost-effectiveness should guide the decision of whether to introduce genetic and genomic applications into clinical and PH practice. Such evidence is already robust for some genetic tests of chronic clinical conditions, such as hereditary breast and ovarian cancer, Lynch syndrome and familial hypercholesterolemia [31-34]. However, according to the responses recorded in our survey, many PH professionals are not fully aware of this: 26% for hereditary breast/ovarian cancer, 44% for Lynch Syndrome and 50% for familial hypercholesterolemia did not know that the evidence supported the implementation of the relative genetic testing to predict disease risk for these conditions. More widespread knowledge of those genetic and genomic applications with documented evidence of effectiveness and cost-effectiveness would therefore probably improve attitudes towards both the inclusion of PM in preventive interventions and the funding of such interventions through public budgets.

Another result that supports the thesis of improving knowledge to improve attitudes is the association between agreement with investing resources in genomics and involvement in work activities dealing with personalized medicine. This finding highlights the importance of increasing awareness of the opportunities that PM can offer, particularly among PH professionals not directly involved in genomics projects and/or activities. Communication and training needs have been also identified as key challenges in the implementation of PM by the European PerMed Consortium [35], while the PRECeDI consortiuum added among its recommendations the training of. of clinical and public health professionals should be promoted with the aim of reducing inappropriate use in healthcare [36].

Although professionals involved in PHG activities are better informed about genetic testing, gaps in knowledge were also identified in this group. This may be due to differences in recommendations for use of genetic testing, to a lack of standard procedures for the evaluation of genetic services, and to differences in how genetic services are delivered in different countries. It has in fact been reported that, internationally, different frameworks are adopted for the evaluation of genetic testing [37]. Furthermore, organizations that develop guidelines on the implementation of genomic medicine show wide variation in the use of external and systematic reviews, as well as in the updating of recommendations, when they are assessing the strength of relevant scientific evidence [38]. At the European level, it has been emphasised that guidelines and policies to support the integration of genomics policies into existing healthcare systems need to be harmonized across countries [26,39]. It has also been highlighted that current genetic services are usually delivered without an internationally standardized set of process and outcome measures, making the evaluation of healthcare services difficult [40]. Only a limited number of PHG professionals considered treatment, follow-up and clinical surveillance to be a component of a genetic service. This may be due to differences in the organizational models of genetic services across countries: research on this topic has in fact shown that the definition of a genetic service may vary largely across different settings [41-44].

There was strong agreement that PH professionals should foster the integration of genomics into PH practices, and over 80% of respondents agreed that in the future PH programs will make greater use of genetic information. Positive attitudes towards the involvement of PH professionals in genomics were associated with being trained in genetic testing during undergraduate education and with direct involvement in PHG activities.

It seems clear from these findings, therefore, that greater knowledge of genomics and personalized medicine among health professionals not directly involved in genetics would improve the capacity of health systems to incorporate new genomic technologies [11–14, 35]. Increasing PH capability in genomics could also help to avoid uncontrolled implementation of technologies without proven benefits, which can lead to inappropriate management of patients, detrimental effects on patient health, and waste of financial resources [36]. Our results are in line with the findings of two surveys on the genomics knowledge and attitudes of PH educators conducted respectively in Italy and the US [22,45], showing that knowledge is a significant predictor of positive attitudes towards the use of genetic testing and the delivery of genetic services in PH.

Our findings suggest that healthcare professional education could be the first step to increase knowledge and capacity of professionals on genomics. There are significant differences in the way in which professional education is delivered across the countries of Europe and also the study curricula of physicians and non physician PH specialists may differ substantially. A set of core competencies in genomics for health professionals (even though not specifically addressed at PH professionals) has been proposed by the European Society of Human Genetics, to provide an appropriate framework for establishing minimum standards of preparation and guide the development of study curricula for health-care professionals in all Countries (graduate or post- graduate) [45]. Based on this framework, a study conducted in Italy tried to identify a set of core competencies in genetics for non-geneticists, both physicians and non-physicians, developing a proposal of three different curricula according to the profession, including basic knowledge, but also attitudes and abilities needed to be able to effectively incorporate genomics into practice. [46]. Given the association observed between a direct involvement in PHG activities and both knowledge and attitudes, it may be useful to develop specific training initiatives for the PH workforce in framework of continuous medical education and/or on-job training,

This is the first survey conducted at the European level on knowledge and attitudes of PH professionals relating to genomics, and thus provides useful insights on the topic. However, despite using several measures to maximise it, the response rate was low and therefore the results only apply to approximately 10% of the whole EUPHA membership. The low response rate reflects one of the main challenges of web-based surveys and is coherent with other studies that also relied on this type of tool. Based on the results of different studies, Ban Mol reported in fact that a response rate below 10% is not uncommon for web surveys, which have been shown to generally get a 6 to 15% lower response rate compared to other survey modes [47]. The low response rate in our study was also influenced by our choice not to opt for an “aggressive” approach to reminders: no telephone calls were used, as in our previous surveys, and we chose to only sent a limited number of reminders (three emails were sent in total to EUPHA members), considering that repeated follow-ups have been shown to diminish returns and may have the counterproductive effect to irritate potential respondents, without noticeably increasing response rates [48].

A selection bias may therefore have occurred, with respondents differing systematically from non-respondents. The sample proved to be representative of the population of EUPHA members in terms of professional background: a recent survey conducted by the EUPHA secretariat indicated that 66% of responders identified themselves as researchers, 14% as policymakers and the remaining 20% as practitioners (data not published), showing a similar distribution than our sample. However, due to the anonymous nature of the survey, it was not possible to assess any other difference between responders and non responders. We can assume that people responding to the survey had, in general, a stronger interest in genomics than non-responders, and therefore showed more positive attitudes. Given the lower level of knowledge of genomics among people not involved in this area of work, we can also assume that genomics knowledge among the European PH community is even lower than reported in our study, reinforcing the apparent need to increase the genomics capability of professionals not directly dealing with this area. The fact that our findings are consistent with those of studies conducted in the PH community in Italy in 2010 and among US public health educators in 2008 [22, 49], and that responses were obtained from all EU countries, suggests that our conclusions are generally applicable across European and other nations. Another limitation of the study was the impossibility to compare knowledge and attitudes on genomics across different Countries: respondents came from a high number of Countries (over 35), not allowing to stratify responses according to the provenience. The lack of information on the organizational models of genetic services in all Countries did not allow to control for type of delivery model either [50].

In conclusion, our sample of PH professionals in Europe was positive about incorporating the increasing number of genomic applications into their working practice, and agreed they should play a role in this translation process, but their knowledge of PHG is rather weak. Specific efforts should be made to increase the capacity of PH professionals not directly involved in genomics, by implementing communication and/or training strategies at national and international levels. Our findings also highlight an urgent need to further develop and share common and standardized definitions and operational guidelines on PM within the PH community in Europe. In this respect, joint research and training initiatives on PM and genomics at the European level, such as the PRECeDI consortium, have proved to be useful in developing and sharing evidence in this field and should continue to be promoted.

Questionnaire.

(DOC)

Click here for additional data file.

Survey data.

(XLS)

Click here for additional data file.

Table 2_bis and Table 3_bis.

(DOCX)

Click here for additional data file.

2 Jan 2020

PONE-D-19-26230

Genomics knowledge and attitudes among European public health professionals: results of a cross-sectional survey.

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Reviewer #1: The paper provides a very interesting view on knowledge and attitudes of a sample of European public health professionals on genomics and personalized medicine. The topic is of major public health interest and the paper deserves publication. However, the very low response rate (only 10% of member of the European Public Health Association have answered the survey) represents an important limitation, as also acknowledge by the authors. In this regard, they have correctly indicated that “the low response rate reflects one of the main challenges of web-based surveys”. However, this point requires some further elaboration in order to support the quality of the results obtained, adding references to published literature (e.g. confirming that the response rate obtained is in line with the average rate of web base survey?). The authors could also discuss issues of representativeness of the sample (is the EUPHA members population different in composition than the study sample?). When describing the results, information on the provenience of the respondents could be added, again to provide an idea of the actual representativeness of the sample.

There are also some other suggestions related to the description of methods, results and discussion sections.

Methods

The paper refers to a previous study where the questionnaire was piloted. However, I would suggest providing clearer definitions of the terminology adopted and explaining how were the questions designed. E.g., in section E the authors write “The following statements are based on published literature dealing with the relationship between public health and human genomics and the possible role of public health professionals in putting PHG into practice.” What is the literature they are referring to? Did they use pre-existing questions coming from similar questionnaires (eg the study by Marzuillo et al, with some of the authors also belonging to this research group))?

Even if provided in the study questionnaire annexed to the manuscript, a clear definition of what is meant by “genetic testing” should be provided by the authors in the text: are they referring to predictive testing only? Similarly, I would suggest adding a definition of “genetic service”, which is widely used throughout the text.

Results/discussion:

As also stated before, it would be worth discussing how questions, particularly those belonging to section E of the questionnaire, were designed. I believe that there may be a social desirability bias in the responses provided, and I would suggest adding this point to the discussion.

Reviewer #2: The manuscript addresses an interesting question, which is to what extent do public health professionals have competence in genomics. The investigators obtained a sample of over 600 members of the European Public Health Association to identify both level of knowledge and attitudes regarding genetic testing and genetic services. The study is largely descriptive, with logistic regression analyses conducted to assess independent predictors of knowledge and attitudes.

The finding that only 29% of participants correctly identified all medical conditions for which there is (or not) evidence for implementing genetic testing and over 60% thought that investing in genomics may divert economic resources from social and environmental determinants of health are in themselves quite noteworthy and worthy of publication. However, the manuscript leaves three important questions unanswered. First, it provides no recommendations on how adequate knowledge and capacity among PH professionals can be achieved to facilitate the integration of genomic information into PH activities. Second, given the generally positive attitudes of most PH professionals towards genetic testing and genetic services, how much knowledge within the field is adequate? Third, the significance of the finding that 60% of the sample believed it was more important to invest resources in the social and economic causes of ill health than in the implementation of genetic testing does not mean that they believe genetic testing is unimportant. I believe a more nuanced interpretation of the finding must be provided in the discussion given the wording of the question and the implications of this finding for integrating genomics into public health. The authors need to explain why the belief that genomics are important but not as important as social and environmental determinants constitutes a barrier to their implementation in public health.

As the authors indicate, the response rate is very low, which raises questions regarding the generalizability of the findings and potential for response bias. The authors note on lines 143-145 that there were no significant socio-demographic differences between those who completed the entire survey and those who did not; however, that is not the same as comparing the socio-demographic differences between those who agreed to participate and those who did not. Given that one of the authors is from the European Public Health Association, surely there must be some demographic information of the membership of the association as a whole (19,000 according to the association website) that can be used to assess how representative of that membership.

It would also be helpful to provide information on the nationality of the study participants and a comparison of knowledge and attitudes by nationality. The authors note on lines 274-277 that organizational models of genetic services may differ in different countries. However, this was not included as a covariate in the regression analyses. However, a table of comparisons of knowledge and attitudes by nationality as well as other socio-demographic characteristics would be helpful.

In the multivariate analysis, knowledge is predictive of positive attitudes towards genetic testing and delivery of genetic services, but not of positive attitudes towards use of resources for genetic testing or positive attitudes toward the role of professionals in PHG. The significance of this finding should be addressed in the discussion, especially as it raises the question of what can be done to change attitudes without having to rely on increased education alone. The findings would seem to contradict the recommendation that greater awareness is needed.

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29 Feb 2020

Dear Editor and Reviewers,

Apologizing for the delay in providing our feedback, also due to work overload caused by the current SARS-COV2 outbreak in Italy, we would like to thank the reviewers for addressing several important points in the manuscript with their comments. We tried to include all their suggestions to improve the quality of the paper, expanding both the methods, results and discussion sections. We have also added ten additional references, including reference to the recommendations of PRECeDI project, which were released very recently. Finally, we added a sentence regarding the request for consent and the approval received by Sapienza University Ethics Committee to conduct the study in the methods section.

Please find below our responses to all comments of the two reviewers.

Reviewer #1

1. The Reviewer wrote “The very low response rate (only 10% of member of the European Public

Health Association have answered the survey) represents an important limitation, as also acknowledge by the authors. In this regard, they have correctly indicated that “the low response rate reflects one of the main challenges of web-based surveys”. However, this point requires some further elaboration in order to support the quality of the results obtained, adding references to published literature (e.g. confirming that the response rate obtained is in line with the average rate of web base survey?). The authors could also discuss issues of representativeness of the sample (is the EUPHA members population different in composition than the study sample?). When describing the results, information on the provenience of the respondents could be added, again to provide an idea of the actual representativeness of the sample.”

We agree with the Reviewer that the low response rate represents an important limitation in our study and that it should be better addressed in the Discussion section. We have added some references to published evidence on reported response rates, in order showing that “The response rate obtained in our study is coherent with that of other studies that also relied on web-based surveys. Based on the results of different studies, Ban Mol reported in fact that a response rate below 10% is not uncommon for web surveys (which have been shown to generally get a 6 to 15% lower response rate compared to other survey modes (Ban Mol C. Improving web survey efficiency: the impact of an extra reminder and reminder content on web survey response, International Journal of Social Research Methodology. 2017 20:4:317-327, DOI: 10.1080/13645579.2016.1185255),).” We have also specified that “we only sent a limited number of remainders (three emails were sent in total to EUPHA members), considering that repeated follow-ups have been shown to diminish returns and may have the counterproductive effect to irritate potential respondents, without noticeably increasing response rates (Deutskens, E. C., Ruyter, de, J. C., Wetzels, M. G. M., & Oosterveld, P.Response rate and response quality of internet-based surveys: an experimental study. Marketing Letters. 2004,15(1): 21-36. https://doi.org/10.1023/B%3AMARK.0000021968.86465.00).

We have also added a sentence discussing representativeness of the sample, writing “Despite the low response rate obtained, the sample proves to be representative of the population of EUPHA members in terms of professional background (a recent survey conducted by the EUPHA secretariat indicated that 66% of respon s identified themselves as researchers, 14% as Policymakers and the remaining 20% as Practitioners (data not published), showing a similar distribution than our sample)”.

We thank for the suggestion to also include information on the nationality of respondents in the Results section. We have added the following paragraph “Respondents came from all EU28 Countries and some non –EU Countries, including Albania (n=1), Andorra (n=1), Bosnia and Herzegovina (n=4), Norway (n=15), Russia (n=1), Serbia (n=3), Switzerland (n=25), Turkey (n=7), and there were 27 people working in developing countries at the time the survey was conducted”

2. The Reviewer wrote “The paper refers to a previous study where the questionnaire was piloted. However, I would suggest providing clearer definitions of the terminology adopted and explaining how were the questions designed. E.g., in section E the authors write “The following statements are based on published literature dealing with the relationship between public health and human genomics and the possible role of public health professionals in putting PHG into practice”. What is the literature they are referring to? Did they use pre-existing questions coming from similar questionnaires (eg the study by Marzuillo et al, with some of the authors also belonging to this research group))?”

We agree with the Reviewer that we did not clarify enough how the questionnaire was developed. Our manuscript included a reference on the paper presenting the results of the pilot phase of the survey, where more information on the questionnaire are provided. However, we have also added a sentence clarifying that “The development of the questionnaire was informed by a literature review and by similar studies previously carried out by the same research group (18,22). It was also based on the inputs received by the members of EUPHA Section on PHG and by all partners of PRECeDI project, as described elsewhere (23).”

3. The Reviewer wrote “Even if provided in the study questionnaire annexed to the manuscript, a clear definition of what is meant by “genetic testing” should be provided by the authors in the text: are they referring to predictive testing only? Similarly, I would suggest adding a definition of “genetic service”, which is widely used throughout the text.”

We agree with the Reviewer that a definition of the terms “genetic testing” and “genetic service” should have been provided also in the manuscript. We have added the following paragraph in the methods section:

“For the purpose of the survey, we defined genetic testing as “performing a type of medical test involving an analysis of human chromosomes, DNA, RNA, genes, and/or gene products (e.g., enzymes and other types of proteins), which is predominately used to detect heritable or somatic mutations, genotypes, or phenotypes related to disease and health”, following the definition proposed by Burke (24). Further to discussion with other PRECEDI project partners, we have decided to adopt the classification of genetic testing used by the European Society of Human Genetics (25). In particular, the survey was aimed at investigating knowledge and attitudes towards the implementation of susceptibility (also known as predisposition) tests, defined as “the detection of genetic variants that are associated with an increased risk of disease but cannot predict with certainty the development of disease, because of the incomplete penetrance of the genetic mutation”. Examples of this type of tests include BRCA testing, Lynch syndrome testing and familial hypercholesterolemia genetics tests. A “genetic service” was defined as “the provisions to diagnose, advise and treat individuals with risk factors for genetic disorders.” According to our interpretation, the delivery of a genetic service is therefore expected to provide not only genetic testing and counselling, but also treatment and follow up of individuals with genetic disorders, similarly to what was previously described by Battista et al.”( 26)

4. The Reviewer wrote “As also stated before, it would be worth discussing how questions, particularly those belonging to section E of the questionnaire, were designed. I believe that there may be a social desirability bias in the responses provided, and I would suggest adding this point to the discussion.”

We thank the reviewer for this comment. We had described the questionnaire development in the paper presenting the results of the pilot phase of the survey, but we agree that it would be useful to provide more information on the process also in this paper. We have included a sentence clarifying that “Statements included in section E were based on published literature dealing with the relationship between public health and human genomics and the possible role of public health professionals in putting PHG into practice (27)”.

Reviewer #2

1. The Reviewer wrote “The finding that only 29% of participants correctly identified all medical conditions for which there is (or not) evidence for implementing genetic testing and over 60% thought that investing in genomics may divert economic resources from social and environmental determinants of health are in themselves quite noteworthy and worthy of publication. However, the manuscript leaves three important questions unanswered. First, it provides no recommendations on how adequate knowledge and capacity among PH professionals can be achieved to facilitate the integration of genomic information into PH activities. Second, given the generally positive attitudes of most PH professionals towards genetic testing and genetic services, how much knowledge within the field is adequate? Third, the significance of the finding that 60% of the sample believed it was more important to invest resources in the social and economic causes of ill health than in the implementation of genetic testing does not mean that they believe genetic testing is unimportant. I believe a more nuanced interpretation of the finding must be provided in the discussion given the wording of the question and the implications of this finding for integrating genomics into public health. The authors need to explain why the belief that genomics are important but not as important as social and environmental determinants constitutes a barrier to their implementation in public health.”

We thank the reviewer for this comprehensive comment, which allowed us to address interesting issues in the Discussion section of the manuscript.

With regards to the way in which knowledge and capacity among PH professionals can be achieved to facilitate the integration of genomic information into PH activities, we have elaborated more in the discussion section on the need to increase the genomic competences of PH professionals in Europe. “Healthcare professional education should be the first step to increase knowledge and capacity of professionals on genomics. There are significant differences in the way in which professional education is delivered across the countries of Europe, and also the study curricula of physicians and non physician PH specialists may differ substantially. A set of core competencies in genomics for health professionals (even though not specifically addressed at PH professionals) has been proposed by the European Society of Human Genetics, to provide an appropriate framework for establishing minimum standards of preparation and guide the development of study curricula for health-care professionals in all Countries (graduate or post- graduate) (45). Based on this framework, a study conducted in Italy tried to identify a set of core competencies in genetics for non-geneticists, both physicians and non-physicians, developing a proposal of three different curricula according to the profession, including basic knowledge, but also attitudes and abilities needed to be able to effectively incorporate genomics into practice (46).

We believe that our previous response could also answer to the Reviewer’s question on how much knowledge within the genetic field is adequate. Overall, there is scarce evidence on PH practitioners’ capacity in this area, ours was one of the few studies conducted on this specific topic, and no study so far has ever tried to estimate a miminum level of knowledge required to properly include genomic applications into PH practice. However, as already stated, core competencies needed to properly incorporate genetics into practices have been proposed by different scientific societies both at the European and national level.

Finally, with regards to the third point raised by the reviewer, we agree that those answering that “investing resources in the social and economic causes of ill health is more important than investing them in the implementation of genetic testing” do not necessary believe that genetic testing is unimportant. However, in a time where public health budgets are suffering, they may fear that investing in public health genomics and precision medicine could divert resources from addressing the “traditional” determinants of health, as already stated in the discussion. We have added the following sentence in the Discussion “In this regard, there is a long-standing debate in the PH community on the opportunity to focus on -omics and personalized medicine, and whether this may divert from the traditional population-based approach. The need to go beyond the dichotomous high-risk versus population approach was suggested, taking into account that precision public health could contribute to improving population health and achieving social justice—equity, social inclusion, and empowerment, through the use of individual data.”

2. The Reviewer wrote “As the authors indicate, the response rate is very low, which raises questions regarding the generalizability of the findings and potential for response bias. The authors note on lines 143-145 that there were no significant socio-demographic differences between those who completed the entire survey and those who did not; however, that is not the same as comparing the socio-demographic differences between those who agreed to participate and those who did not. Given that one of the authors is from the European Public Health Association, surely there must be some demographic information of the membership of the association as a whole (19,000 according to the association website) that can be used to assess how representative of that membership.”

We agree with the Reviewer that some more information on the generalizability of the results would be needed. Unfortunately, the EUPHA secretariat does not have detailed information on the socio-demographic characteristics of its of the Association members. In this regard, we would like to clarify that the reference population for your survey was that of EUPHA members, which account to approximately 5,000 people, much smaller than the 19,000 reported in the website, which refer to the subscribers to the EUPHA Newsletter (the so called “EUPHA Network”). EUPHA is an umbrella organization for public health associations and institutes in Europe, therefore its members are all individual members of national public health associations, who, when subscribing to their national association, have indicated to be interested in European public health affairs and policies and paid an additional fee, which entitles them to a subscription to the European Journal of Public Health and reduced fees for the EPH Conference. The only information provided by national public health associations to EUPHA secretariat is their members’ e-mail address. Early 2019, the Secretariat did a very short web survey on the professional background of EUPHA Newsletter subscribers. Results, based on 170 responses only, indicated that 66% of responders identified themselves as researchers, 14% as Policymakers and the remaining 20% as Practitioners. These results are similar to those reported in our survey, with 58.8% of respondents defined as Academics (researchers), 19.7% working at the Governmental level, and the remaining working in different types of practices (Hospital, Local Health Units, NGOs, etc.). This information was included in the manuscript.

3. The Reviewer wrote “It would also be helpful to provide information on the nationality of the study participants and a comparison of knowledge and attitudes by nationality. The authors note on lines 274-277 that organizational models of genetic services may differ in different countries. However, this was not included as a covariate in the regression analyses. However, a table of comparisons of knowledge and attitudes by nationality as well as other socio-demographic characteristics would be helpful.”

We thank the Reviewer for this comment. We agree that it would have been interesting to compare differences in attitudes and knowledge by nationality, however, responses came from a too high number of Countries, not allowing to include it as a covariate in the analysis (the number of observation for each category would have been to small). We could have combined countries according to the type of organization of genetic services, but unfortunately, information on the organization of delivery models in European countries is not available: within PRECeDI project, we attempted to conduct an expert survey in Europe to assess the delivery of genetic services and adherence to international guidelines for genetic testing for BRCA, Lynch Syndrome, Familial Hypercholesterolemia and Hereditary Trombophilia, but we were able to collect responses only from a limited number of Countries (six to twelve Countries, according to the type of hereditary condition assessed) (Rosso A, et al. European Journal of Public Health, Volume 28, Issue suppl_4, November 2018, cky213.371,) We have added the following sentence in the Discussion section of the paper, when addressing the limitations of the study “Another limitation of the study was the impossibility to compare knowledge and attitudes on genomics across different Countries: respondents came from a high number of different counties (over 35), not allowing to stratify responses according to the provenience. The lack of information on the organizational models of genetic services in all Countries did not allow to control for type of delivery model either (50).” However, as previously reported in response to Reviewer #1, we have included information on the nationality of study participants.

4. In the multivariate analysis, knowledge is predictive of positive attitudes towards genetic testing and delivery of genetic services, but not of positive attitudes towards use of resources for genetic testing or positive attitudes toward the role of professionals in PHG. The significance of this finding should be addressed in the discussion, especially as it raises the question of what can be done to change attitudes without having to rely on increased education alone. The findings would seem to contradict the recommendation that greater awareness is needed.

We thank the reviewer for this comment, which suggested us that some information should also be provided on the results of the univariate analysis. Actually, both the association between knowledge and positive attitudes towards the use of resources for genetic testing and with positive attitudes toward the role of professionals in PHG were statistically significant at the univariate analysis P=0.016 annd P=0.021). However, when controlling for other covariates, knowledge appeared to be less relevant than other factors, mainly the fact of having PHG as one of the main areas of work (which, in turn, is one of the strongest predictors of knowledge). We have added a paragraph explaining the association between knowledge and attituded in the Discussion, and we also added a sentence saying that “Given the association observed between a direct involvement in PHG activities and both knowledge and attitudes, it may be useful to develop specific training initiatives for the PH workforce in framework of continuous medical education and/or on-job training”.

We hope that the manuscript can now be considered suitable for publication.

Sincerely,

Annalisa Rosso and all co-authors

Submitted filename: Response to reviewers.docx

Click here for additional data file.

9 Mar 2020

Genomics knowledge and attitudes among European public health professionals: results of a cross-sectional survey.

PONE-D-19-26230R1

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18 Mar 2020

PONE-D-19-26230R1

Genomics knowledge and attitudes among European public health professionals: results of a cross-sectional survey.

Dear Dr. Rosso:

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