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. 2020 Sep 18;15(9):e0238128. doi: 10.1371/journal.pone.0238128

Increased awareness and decreased acceptance of genome-editing technology: The impact of the Chinese twin babies

Daiki Watanabe 1, Yoko Saito 1,*, Mai Tsuda 2, Ryo Ohsawa 2
Editor: Simone Garzon3
PMCID: PMC7500613  PMID: 32946484

Abstract

Genome-editing technology has become increasingly known in recent years, and the 2018 news of genome-edited twins in China had a particularly significant impact on public awareness. In the present study we investigate the effect of Japanese media coverage on public opinions of this technology. To identify the effects we employ a questionnaire survey method on a pre-registered sample from online research company Macromill. Our repeated survey from 2016 through 2019 reveal a generally supportive attitude toward the medical application of genome-editing methods. To see this we employed a multinomial logit analysis examining the determinants of negative and positive impressions of the technology. Results show that although editing for medical purposes remained mostly acceptable, its use in fertilizing human eggs was increasingly rejected, especially in 2019, the most recent sample year. The suggestion is that while genome-editing applications in general medical fields are publicly accepted, its use in human functionality enhancement is heavily increasingly resisted. News of the twin babies in China did raise public awareness of the methods but also damaged their reputation. It therefore is important for genome researchers to hold such concerns in mind, keeping the public informed of changing technology fundamentals. As a related question we inquire into the public acceptability of genome editing for animal and plant breeding, such as in agriculture and fisheries, as well. We find the Japanese public views the medical and breeding applications of this technology to be unconnected with each other, despite that awareness of both has risen significantly in recent years.

Introduction

The emerging technology of genome editing, together with its applications, is attracting increased public attention, especially in its use with human genes. Many in the scientific community are calling for debate on the appropriate applications of this technology, one that will draw scientists, bioethicists, legal and regulatory bodies, and the public together [13]. Since these calls, the public’s perception and acceptance of human gene editing are starting to be investigated. Discussion focuses mainly on the technology’s medical applications, such as therapeutic or function enhancement purposes–and as an extension, the moral concerns of both the scientific and general community [49].

An earlier study [5] collected 12,000 respondents through social media, finding public acceptability of the technology for therapeutic uses differed starkly from that for reproductive uses. Another survey indicated more than 60% of respondents favored the technology’s application in medical treatments but disfavored its use in functionality enhancements, such as applications to human embryos [4]. And more knowledgeable respondents indicate the need for science community to consult with public. Another survey [6], based on respondents from eleven countries including the US and European nations, suggested medical applications’ functionality enhancement purposes are not more acceptable than therapeutic purposes are. In Australia, respondents were accepting of human gene editing for both research and human health purposes [7].

Surveys of the Japanese public have found similar results, and begun to go further in asking how one’s understanding or ‘literacy’ of genetic editing affect its acceptability. The more gene-literate respondents seem to show a more positive attitude toward its medical applications [10], though literacy has no significant effect on attitudes toward crop applications [11]. Survey [12] found gene-literate respondents to be even more cautious about gene manipulation than the less literate is. Disease-abatement applications are more acceptable than others, even when the respondent’s knowledge of the technology is small [13]. And the literature [14] suggests an ambiguity in the Japanese public toward genome editing methods in general. Media coverage of the birth of genetically edited twins in China included a great deal of ancillary information about the method’s applications in medical science. Media exposure doesn’t always alleviate resistance to biotechnology, it is found [15], and the impact of the twins’ birth in particular has not yet been examined.

In the present study, public acceptance of genome-editing technology was investigated by way of a sequence of surveys conducted in 2016, 2018, and 2019, with a focus on media impacts. Genome-editing methods have become widely known in Japan in recent years, and public attitudes are changing accordingly. Fig 1 shows that from 2015 to 2019 the search-volume frequency of the term “genome-editing technology” peaked in Japan during the week of November 26, 2018 when news of the twin babies was released in China [16]. News reports detailed the manner in which genome-editing technology was applied to a human embryo, and it was widely criticized in both academic and non-academic groups. The coinciding of the search-volume peak in late 2018 (Fig 1) seems to suggest that the controversy added substantially to public awareness of genome-editing methods. However, this has not been examined carefully until now, and it is especially important to do so during this early stage of the technology’s diffusion.

Fig 1. Search volume of term “genome-editing technology” in Japanese (Google).

Fig 1

The greatest number of searches recorded (100) was in the week of November 26, 2018.

Media coverage can be an influencing factor in consumer preferences, as revealed for example in bovine spongiform encephalopathy (BSE), E. coli O157 cases [17], and kepone contamination [18]. These studies show media health data can discourage market demands for specific foods. Here we investigate whether it also affects the demand for genome editing technology. It is important to clarify that no consumer products from genome-editing technology have yet been marketed, so it was impossible for us to trace demand changes with market data. Survey questionnaires were thus used instead, as they are the most suitable alternatives to market information.

Biotechnology’s medical uses generally receive strong public support [19]. But even in these uses, acceptance likely will differ according to the technology’s purposes and to an individual’s knowledge or literacy of genetics. Given that both academics and the public received news of the Chinese twins with particular disfavor, we hypothesize that the acceptability of genome-editing technology itself was negatively affected by it. The goal of our study is to investigate the degree to which public acceptance would be affected by media coverage in general, and whether the degree of that influence would depend on the purposes of its use and on one’s knowledge of the methods. We thus separately specify a therapeutic use and a functionality-enhancement use of the technology to enable us to identify any differences in news-reader impressions that they might evoke.

We also analyzed the impact of news on genome editing applications in areas such as agriculture and fishery breeding. Although the main reason for the public’s response to the Chinese twins is that it was applied to a human embryo, it may also have affected sensitivities to applications in other areas as well. Genome editing, one of the new plant-breeding technologies (NBTs), can induce mutations more precisely than earlier methods could [20]. At the same time, they can be understood as a method similar to conventional cross-breeding. Rapid progress in molecular biology has facilitated progressively wider plant gene modifications [2122]. Yet even there, gene recombinant technology in particular has raised dietary worries [23]. Thus, although genome editing technology as a whole is considered scientifically promising, attitudes toward its various applications were perhaps entangled with one another when the term first became publicly known.

Survey and results

Survey description

Our survey of the public awareness/acceptance of genome-editing technology and related media coverage was conducted in Japan in March 2016, January 2018, and finally January 2019 (Table 1). For each survey, respondents were independently selected out of a pre-registered sample from the online survey company Macromill. The numbers of pre-registered respondents at hand to us at the times of our survey is shown in Table 1, and the associated summary statistics displayed in S1 Table. Original monitors in the pre-registered sample showed that 18.0% of respondents were under 19 years old and were excluded from our survey. According to Macromill, pre-registered samples are generated by voluntary registration.

Table 1. Survey parameters.

2016 2018 2019
Survey period March 2016 Jan-Feb 2018 Jan-Feb 2019
Questionnaire title Survey related to science and technology Food Questions Food Questions
Number of respondentsa 3,100 (682) 1,240 (422) 1,543b (677)
Number of respondents in the pre-registered sample (in thousands) 901.2 1,196.1 1,215.8
Note on surveyed sample Between 20–60 year age groups, equal numbers of males and females Between 20–60 year age groups, equal numbers of males and females An unequal number of males and femalesc

a Numbers in parentheses are those who replied “very knowledgeable,” “know some,” or “have heard” about genome-editing technology in Q3. Any who replied “Do not remember” in the following Q4 were also excluded. In each category, five alternatives were offered (S1 Text): “nothing at all,” “not much,” “have heard of it,” “have some information,” and “very knowledgeable.”

b Because seven respondents had been sampled in both the 2016 and 2019 surveys, they were excluded from the 2019 sample.

C The number of females and males in the 2019 survey were unequal because of the exclusion (see footnote b).

As our survey was conducted by the research firm Macromill, the sample had already been anonymized. We were allowed to access only to the respondents’ ID numbers, which are individually assigned upon their registration with Macromill’s pre-registered pool. Respondents hold the right to withdraw from or refuse to participate in the survey at any time during the online survey procedure. Given these provider rights and anonymity, written informed consent was not required. In addition to this however, the Research Ethics Committee of the Research Faculty of Agriculture, Hokkaido University, has formally confirmed our compliance.

Respondents to our survey were solicited on the basis of the questionnaire title sent from the survey company or posted on the company website, which remained open until the number of survey responses reached our requested sample size. We requested a sample with an equal number of male and female respondents aged between their 20s and 60s. The total number of respondents was 3,100 in 2016, 1,240 in 2018, and 1,550 in 2019. The pre-registered sample was 901,198 in 2016, 1,196,092 in 2018, and 1,215,789 in 2019. As we requested an equal number of respondents by sex and age group, the shares of these groups in our sample are largely the same across groups. We were not able to check for any statistically significant differences between the pre-registered samples and our surveyed ones, since standard deviations in the pre-registered sample are unavailable. But location and occupation shares are quite similar in the two samples.

Each year’s sample excluded those who had replied the previous year. To reduce opinion bias, we avoided using "genome-editing technology" in the questionnaire title when soliciting respondents from the pre-registration sample, and instead used more general terms like “survey on food” and “survey on science and technology.” Survey sheets in both the original language (Japanese) and the English translation are shown in the Questionnaire in S1 Text.

Content of media coverage

We asked respondents to indicate the degree of their awareness of genome-editing technology on a five-point Likert scale. We then, for some purposes, grouped those who replied “very knowledgeable,” “know some information,” or “have heard of it” as broadly ‘being aware’ of genome-editing methods (Fig 2 and S2 Table). Results show the proportion of those aware of the technology in this sense has been rising, from 28.8% in 2016 to 51.8% in 2019, implying the term "genome-editing technology" has become increasingly familiar in the past few years.

Fig 2. Proportion of those who “have heard”, “know some” or are “very knowledgeable” of the term “genome-editing technology,” shown by survey year, and further divided by (a) sex, and (b) age group.

Fig 2

Subsequent analysis was undertaken only with the respondents who were aware of genome technology according to that division, since those who aren’t would be unable to answer several of the important questions, such as whether they had encountered any media coverage on the subject. Summary statistics of both “not being aware” and “being aware” sub-samples are provided in S3 Table. Our results are consequently drawn from respondents who showed at least some interest in the technology. This may have an upward effect on the numbers of those who have a positive attitude. We could have provided in the online survey additional objective information, but respondents’ own views of a technology likely depend on the contexts in which the technology will be used, which inherently are not objective. Respondents saying they were unaware or ‘not much’ aware of gene editing were thus encouraged to skip these particular questions.

We further asked respondents who were aware of genome-editing technology which media content made the strongest impression (positive or negative) on them (Table 2). A number of possible media categories were suggested in this regard, including “an explanation of a technology,” “an application to fishery or agricultural breeding,” “an explanation of the risk of technology adoption,” “medical applications of the technology,” and “applications to fertilized human eggs.”

Table 2. Content making the strongest impression a.

Media Content 2016 2018 2019
Explanation of the technology itself 265 81 112
(c_tech) (38.9) (19.2) (16.5)
Application to fishery or agricultural breeding technology 210 101 137
(c_breed) (30.8) (23.9) (20.2)
Explanation of the risk of adopting the technology 76 31 54
(c_risk) (11.1) (7.4) (8.0)
Medical application of the technology 125 136 193
(c_medical) (18.3) (32.2) (28.5)
Application to fertilized human eggs - 67 172
(c_embryo) - (15.9) (25.4)
Other Media Categories 6 6 9
(c_others) (0.9) (1.4) (1.3)
Total 682 422 677

a A respondent could select only one media content. Tabled values indicate the number of respondents choosing that category. Parenthesized numbers are the corresponding percentage shares of the sampled respondents.

An “explanation of the technology itself” created the strongest impression (38.9%) in 2016, whereas “medical application” created the strongest in 2018 (32.2%) and 2019 (28.5%). Respondents on whom use in fertilized human eggs made the strongest impression rose from 15.9% in 2018 to 25.4% in 2019, suggesting the news of the twin babies in China had a substantial influence on the Japanese public.

The variety of types of impressions created by the media coverage of genome editing is shown in Table 3. The number of respondents saying they found it to be “interesting or impressive” was the highest response in 2016 and 2018, while the number saying they were “concerned about its side or unknown effects” was highest in 2019. As public awareness rose, safety issues, including uncertainties over the method’s side effects, began to receive the greater attention. Concerns about its ethical status were quite high in the 2018 and 2019 surveys, consistent with the increasing attention being paid to research ethics.

Table 3. Most closely matched impressions (or evaluation of each of the impressions).

2016a 2018b 2019b
Number Saying “Most Impressionable” (%) Share of Those Agreeing with the Following: (Ave. score) Share of Those Agreeing with the Following: (Ave. score)
Interesting or impressive 269 (39.4) 83.4 (3.03) 78.7 (2.97)
Amazed by this technological advancement 191 (28.0) 79.9 (2.97) 81.4 (3.02)
*Looking forward to its adoption 49 (7.2) 70.1 (2.87) 64.8 (2.76)
*Worried about its adoption 84 (12.3) 64.0 (2.77) 74.3 (2.94)
Concerned about its side or unknown effects 62 (9.1) 72.0 (2.89) 82.1 (3.06)
Concerned about ethical issues (None) 71.8 (2.89) 79.6 (3.06)
Do not understand the reason for its adoption 4 (0.6) 24.4 (2.11) 37.8 (2.32)
Complicated explanation 22 (3.2) 34.6 (2.30) 42.7 (2.40)
Other 1 (0.2) 0.9 (--) 1.2 (--)

a In 2016 we asked respondents to rate the top three of these impression types. This table shows the number of those marking the indicated impression type as that which “most closely matches my own impression.” The number in parenthesis is that impression type’s percentage share of those rated as ‘top’.

b In 2018 and 2019 in contrast, we asked respondents to evaluate each impression on a four-point Likert scale: “Strongly agree (4),” “Somewhat agree (3),” “Disagree (2),” and “Strongly disagree (1).” The table indicates the number of respondents who marked that impression type as a (4) or a (3). The corresponding number in parenthesis is that impression type’s percentage share of those receiving a (4) or a (3).

Analytical framework

We selected a subset (see asterisked responses) of the impression responses in Table 3 most suitable for characterizing, respectively, an overall supportive and unsupportive attitude toward the technology. In particular we classified, as being “positive” about the technology, those who gave “look forward to its adoption” a higher Likert mark than to “a little worried.” Those who gave a lower mark to it were classified as being “negative.” Those giving the two an equal Likert score were “neutral,” that is, were considered to be indifferent or undecided toward this new technology. Results of these comparisons are shown in Fig 3 and S2 Table.

Fig 3. Impressions of genome-editing technology.

Fig 3

Definitions of impressions are calculated from Table 3, specifically comparing the rate between impressions “Looking forward to its adoption” and “Worried about its adoption”. Survey results are provided in Table B of S2. The present figure is drawn based on the share of each impression in S2 Table. Although the length of the bar is same, composition of impressions differ by year and sex. We set neutral to be center.

As shown in Fig 3, as “genome-editing technology” became more widely known, both male and female attitudes tended to shift from positive to either negative or neutral. Considering all these respondents, positive attitudes fell from 46.2% in 2016 to 27.6% in 2019 (S2 Table), and the share of those with a “neutral” or “negative” attitude rose.

Effect of media coverage on respondents’ impressions

Multinomial logit

We have investigated how public impressions of genome-editing technology appeared to change in the period between 2016 and 2019 as public awareness of the technology grew. We now look to the factors influencing these impressions, using the multinomial logit approach often employed in the analysis of consumer decision-making. Previous research [24] has used this approach to demonstrate the gap between consumer and producer perceptions of meat risk. Here we employ a similar approach to quantify the effect of media coverage and personal attributes on public support for gene editing.

Our model specification is the following. The respondent’s evaluation Yji of the technology, in which j is the evaluation category and i is the respondent, is determined by the media contents (X1i) he or she finds important, and by the respondent’s characteristics (X2i):

Yji=f(X1i,X2i) (1)

where a possible evaluation category is “positive,” “negative,” or “neutral.” That is, as detailed further in Fig 3:

j={1:neutral2:negative3:positive}

and

X1i: Vector of the media content types to which respondent i responds:

  • (c_tech, c_breed, c_risk, c_medical, c_embryo, c_others)

X2i: Vector of respondent i’s individual characteristics.

The following multinomial logit model was then estimated by maximum likelihood:

P(yi=j|xi)=exp(x'iβj)j=1exp(x'iβj) (2)
Yji=β0j+β1jX1i+β2jX2i+uij (3)

where P in Eq (2) is the occurrence probability; yi is the outcome respondent i chooses; vector β in Eq (3) is the set of parameters to be estimated and comprising the impact of the given explanatory variable on the respondent’s impression; and uij is the error term. Put differently, Yji indicates the impression j of respondent i as determined by media content (X1i) and respondent i’ s characteristics (X2i). A positive (negative) parameter indicates that the corresponding explanatory variable increases (decreases) the probability of the given impression.

Multinomial logit Eq (3) were estimated by maximum likelihood, using “neutral to the technology” as the base category (j = 1). The parameters thus are interpreted as changes in the probability of the corresponding variable relative to the ‘neutral’ base group. Estimates were derived separately for each of the three survey years. Media-content variables (X1i) are zero/one, in which "technical explanation (c_tech)" was used as the base. Details of media contents (X1i) and individual characteristics (X2i) are shown in S1 Text, and descriptive statistics and data are presented in S4 and S5 Tables. Estimation results are shown in Tables 46.

Table 4. Estimated parameters and marginal effects, 2016 a,b.
2016
Negative Positive
Parameter Marginal Effect Parameter Marginal Effect
c_breed -0.178 -0.026 -0.082 0.009
(0.278) (0.044) (0.260) (0.044)
c_risk 0.717* 0.273*** -0.716* -0.285***
(0.385) (0.058) (0.427) (0.070)
c_medical 0.009 0.029 -0.169 -0.041
(0.322) (0.051) (0.310) (0.052)
c_embryo - - - -
- - - -
c_others -0.330 0.182 -1.602 -0.328
(0.947) (0.213) (1.251) (0.264)
age 0.007 0.001 0.001 -0.001
(0.008) (0.001) (0.008) (0.001)
d_male 0.002 -0.056 0.351 0.083**
(0.235) (0.038) (0.228) (0.039)
d_univ 0.127 -0.002 0.190 0.025
(0.251) (0.040) (0.242) (0.042)
d_bio -0.282 -0.038 -0.156 0.008
(0.296) (0.045) (0.289) (0.048)
breed_k -0.004 -0.004 0.019 0.005
(0.053) (0.008) (0.051) (0.009)
social_aware - - - -
- - - -
tech_aware - - - -
- - - -
cons 0.562 - 0.745 -
(0.557) - (0.541) -
Log likelihood -679.96
Log likelihood (const) -699.71
Observation 682

a Standard errors are shown in parentheses.

b *,**, and *** indicate statistical significance at 10%, 5%, and 1%, respectively.

Table 6. Estimated Parameters and Marginal Effects, 2019a,b.
2019
Negative Positive
Parameter Marginal Effect Parameter Marginal Effect
c_breed 0.575* 0.065 0.623** 0.068
(0.327) (0.056) (0.314) (0.050)
c_risk 1.407*** 0.260*** 0.022 -0.092
(0.399) (0.066) (0.497) (0.078)
c_medical -0.140 -0.076 0.732** 0.135***
(0.320) (0.056) (0.291) (0.047)
c_embryo 1.513*** 0.290*** -0.122 -0.124**
(0.306) (0.049) (0.356) (0.055)
c_others -0.061 -0.128 1.711* 0.298**
(1.261) (0.213) (0.889) (0.135)
age 0.013* 0.003*** -0.012 -0.003**
(0.007) (0.001) (0.007) (0.001)
d_male -0.438** -0.108*** 0.385 0.096***
(0.210) (0.035) (0.237) (0.037)
d_univ -0.054 -0.026 0.235 0.044
(0.209) (0.036) (0.223) (0.035)
d_bio 0.316 0.032 0.387 0.045
(0.230) (0.040) (0.251) (0.040)
breed_k -0.076* -0.017*** 0.047 0.013*
(0.039) (0.007) (0.044) (0.007)
social_aware 0.279 0.067** -0.230 -0.058**
(0.183) (0.031) (0.186) (0.029)
tech_aware -0.361* -0.110*** 0.634*** 0.134***
(0.211) (0.036) (0.223) (0.034)
cons -0.546 - -2.763*** -
(0.829) - (0.883) -
Log likelihood -651.53
Log likelihood (const) -738.59
Observation 677

a Standard errors are shown in parentheses.

b *,**, and *** indicate statistical significance at 10%, 5%, and 1%, respectively.

Table 5. Estimated parameters and marginal effects, 2018 a,b.
2018
Negative Positive
Parameter Marginal Effect Parameter Marginal Effect
c_breed 0.312 -0.014 0.852** 0.144**
(0.387) (0.063) (0.380) (0.068)
c_risk 1.699*** 0.248*** 0.661 -0.007
(0.558) (0.080) (0.658) (0.111)
c_medical -0.201 -0.137** 1.236*** 0.262***
(0.393) (0.063) (0.358) (0.062)
c_embryo 0.872** 0.120* 0.432 0.015
(0.409) (0.065) (0.444) (0.079)
c_others 0.121 0.082 -0.744 -0.158
(0.982) (0.178) (1.243) (0.239)
age -0.004 0.001 -0.020** -0.004**
(0.009) (0.001) (0.009) (0.002)
d_male -0.417 -0.150*** 0.933*** 0.219***
(0.275) (0.042) (0.287) (0.048)
d_univ 0.153 0.027 0.007 -0.011
(0.289) (0.046) (0.271) (0.049)
d_bio -0.072 -0.00003 -0.158 -0.025
(0.340) (0.054) (0.310) (0.055)
breed_k 0.003 -0.004 0.060 0.012
(0.053) (0.009) (0.050) (0.009)
social_aware 0.292 0.088** -0.448** -0.113***
(0.244) (0.039) (0.227) (0.040)
tech_aware -0.438* -0.122*** 0.543** 0.143***
(0.255) (0.040) (0.249) (0.043)
cons 0.441 - -1.033 -
(0.991) - (0.969) -
Log likelihood -413.95
Log likelihood (const) -461.31
Observation 422

a Standard errors are shown in parentheses.

b *,**, and *** indicate statistical significance at 10%, 5%, and 1%, respectively.

Discussion of marginal effects

Consider now the multinomial logit results in Tables 46. Respondents exposed to media coverage of the technology’s medical applications (c_medical) showed significantly favorable impressions to it in both 2018 and 2019, indicating a supportive attitude toward the medical use of genome-editing methods. However, the marginal effect of medical content on this favorable impression fell from 26.2% in 2018 to 13.5% in 2019. At the same time, the November 2018 revelation about fertilized human eggs (c_embryo) displayed a strong negative response, especially of course in 2019, right after the China news was received. The corresponding marginal effect on that unfavorability was 12.0% in 2018, rising to 29.0% in 2019. Moreover, the China news brought the greatest change, relative to other types of media content, in the probability of having a negative attitude toward gene editing.

Together these findings are indicative of the substantial effect in Japan of the Chinese twins news on the public acceptability of gene editing, a finding similar to a study of the US reaction [4]. While publics appear to support the medical uses of genome editing in general, its use in functionality enhancement, as in fertilized human eggs, impairs that acceptability. Given that ethical concerns in our 2019 sample had become slightly stronger than they were the previous year (Table 3), compliance with ethical principles will be an important factor in public support. Crucially, the risks of genome editing, apart from any hopes or expectations of its effects, weigh heavily on public opinion.

Our model parameter pointing to the media coverage of the technology’s risks, (c_risk), especially in its negative impression, was highly significant, with one of the highest marginal effects on public unacceptability of any we modeled. In contrast, media coverage of genomics’ uses in agriculture and fish breeding (c_breed) appear conducive to positive impressions of it in 2018 and 2019, although in 2019 its parameter was significantly negative as well as positive. News of the Chinese twins did not affect the positive views toward genomic breeding. The public’s views of medical versus farm and fish gene editing don’t seem, that is, to have been confused with one another, although each raised awareness of the technology in general.

On the side of the respondents’ own characteristics (X2i), knowledge of breeding technology (breed_k) significantly reduced the likelihood of an unfavorable view of gene-editing methods, and interest in technology in general (tech_aware) raised the probability of a favorable one. Interest in social issues (social_aware) raised the likelihood of being unfavorable. Male (d_male) respondents generally had a more positive attitude toward genomics than females did, and older (age) participants were more likely to be negative. Note these outcomes are drawn from the Japanese public, and generalizations outside Japan may require further analysis.

Conclusions

The purpose of this study has been to investigate the public acceptability of genome editing during this time of increased awareness, particularly in light of the sensational announcement of the Chinese twins. Because the twin-baby news was released in late 2018 and received widespread attention in public as well as academic circles, our 2016–2019 survey horizon offered a valuable opportunity to see how public opinion was affected by the media coverage.

Our respondents who had earlier been exposed to the technology’s medical applications tended to have approving-views of genome editing, even in 2018 and 2019. On the other hand, insofar as they were exposed to news of its use with human fertilized eggs, they were especially inclined to oppose it. Revelations about the Chinese twins raised public awareness of genome editing technology in general, along with ethical criticism of it when used for the human performance-enhancement purposes.

Our multinomial logit model doesn’t ask how any particular types of ethical concerns affect media responses (Tables 2, 4 and 6). And we are unable here to examine specific ethical concerns in more detail, such as, for example, risks of life or compliance of the medical research. We have seen, however, ethical concern itself moved higher in 2018 and 2019, in the midst of the twins event (Table 3). Further study of the public’s ethical concerns will be required, although the science community must do its own part to keep the public informed about critical technologies’ purposes and applications.

Finally, our results do indicate that Japanese have avoided confusing or even associating genomics’ medical applications with its farm breeding ones. In fact, familiarity with farm breeding brings a more favorable impression of gene editing overall.

Supporting information

S1 Text. Questionnaire.

(DOCX)

S1 Table. Summary statistics of pre-registered and survey sample.

(XLSX)

S2 Table. Awarenesses and their corresponding impressions.

(DOCX)

S3 Table. Summary statistics of survey sample: ‘Not being aware’ and ‘Being aware’.

(XLSX)

S4 Table. Summary statistics of respondents included in multinomial logit analysis.

(XLSX)

S5 Table. Data and definition.

(XLSX)

Data Availability

All relevant data are available within the paper and supporting information files.

Funding Statement

This research was supported (in part) by Cooperative Research Grant # 2043 of the Plant Transgenic Design Initiative (PTraD) by Gene Research Center, Tsukuba-Plant Innovation Research Center, University of Tsukuba, and a grant from the Cross-ministerial Strategic Innovation Promotion Program (SIP), Technologies for creating next-generation agriculture, forestry and fisheries by the Bio-oriented Technology Research Advancement Institution, NARO.

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Decision Letter 0

Simone Garzon

12 May 2020

PONE-D-20-07652

Increased Awareness and Decreased Acceptance of Genome-Editing Technology: The Impact of Chinese Twin Babies

PLOS ONE

Dear Dr. Saito,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The manuscript and the reviewers’ comments were carefully evaluated. The manuscript was appreciated by the Reviewers. Nevertheless, as suggested, the manuscript requires some improvements before to be considered for publication, particularly about the methods description. Further suggested revisions are in detail reported in the Reviewers’ comments.

We would appreciate receiving your revised manuscript by Jun 26 2020 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Simone Garzon

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: I Don't Know

Reviewer #3: No

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for this manuscript. The article presents the survey clearly and thoroughly. I found it very interesting to read. I would like to see a few more details on where the study was conducted, particularly about the location of the survey respondents. Was the survey distributed globally? What languages were used? Some comments in the article suggest that the survey was conducted in Japan only (e.g. p. 11, line 143). It would also be important to discuss the implications of this. If the survey was conducted in one country only, this needs to be stated and an acknowledgement made that this may limit the generalizability of its findings.

One small formatting issue is that reference numbers were regularly used as subjects in sentences, e..g. “[3] found that their results …” This approach is unfamiliar to me and should be checked against the journal's style guidelines.

Otherwise, this is a very good manuscript.

Reviewer #2: I think this manuscript provides important findings about the impacts of the Chinese human embryo editing controversy on public opinion about gene editing in Japan. As such, I support its publication. However, I have a few suggestions for the authors to consider:

1. I found it confusing that the article starts with the discussion of gene editing of plants and animals ("breeding" applications), even though the primary focus is on human gene editing. I think it would therefore be better to start the paper with a discussion of human gene editing and the Chinese incident. At the end of the current intro, it comes back to use of gene editing for animals and plants, which is appropriate there because one of the interesting secondary findings of the paper is that controversy over Chinese human embryo editing dis not seem to appreciably affect public opinion on breeding applications of gene editing. But it confusing to focus on animal and plant applications in the first paragraph of the paper given that the primary focus and finding is on impact on opinion about medical and embryo use of gene editing.

2. On lines 104-05, the manuscript states that the subjects were randomly selected from a "pre-registration sample." It would be useful to say more about how this pre-registraton sample was created. Was it created from a particular geographical region? How were people solicited for the pre-registration sample?-These details are important for understanding the representativeness of the sample.

3. My understanding is that the subjects were all from Japan. That should be explicitly stated. Also, it would be useful to have a little bit of information about the overall perspective of the Japanese public. For example, Japan is a world leader in stem cells, does this make the public more supportive of embryo science generally, or is it similar to European and the Americas?

4. Table 1 states that there was unequal number of males and females in 2019 (even though text says same numbers each year. How unequal was the 2019 sample, did it favor males or females, and was this likely to have had any effect on the results?

5. In table 3, I did not understand the headings “Most Impressionable” (for 2016) vs “Describes Me” (for 2018 and 2019). The meaning of these terms should be explained better.

6. In the conclusion, the authors state that public requires requires researchers to strictly follow ethical guidelines. This might be a reasonable speculation - but was not directly tested by the study. It may be that people are disturbed by embryo manipulations even if it does follow ethical guidelines. Therefore the role of ethical guidelines should be presentrd as a reasonable hypothesis, or excluded altogether since it was not evaluated in this study.

– what does this mean ?and more males or females?

Reviewer #3: I read with great interest the Manuscript titled “Increased Awareness and Decreased Acceptance of Genome-Editing Technology: The Impact of Chinese Twin Babies” (PONE-D-20-07652).

I was particularly pleased to review this paper. In my honest opinion, the topic is interesting enough to attract the readers’ attention. Methodology seems appropriate and conclusions are supported by the data analysis. Nevertheless, authors should clarify different points of methods and improve the discussion discussing limitations of the study that are not evidenced in the discussion.

In general, the Manuscript may benefit from several major revisions, as suggested below:

- All the text needs a language revision in order to improve some typos and grammatical errors.

- Please, check in all the text the use of references as subject. This is not correct, use the form Surname et al. [reference] verb …

- I would suggest checking the use of abbreviation in the abstract and in the main text, they need to be reported in the extended form at the first use.

- I would suggest checking the authors guidelines for the manuscript format.

- I would suggest providing more information about the target population included in the Macromill database, the geographic area, and how the list of the company has been built. Is it actually representative of the entire population? All these details are required to understand the possible biases and limitations of the survey which need to be better discussed.

- I would suggest providing data about non responders and discuss the possible role of this proportion of subjects on the study results. This can be a source of bias and limitations. Are more characteristics of the investigated population available, such age, education, or other? The same about who did not respond.

- I would suggest providing more detail about “how” the survey was conducted. The modality, if interviewers were adopted, which language, if the survey was validated and the process of validation. In general, more details about the methods are required to understand the actual value of provided results and specifically the inference from these results.

- I would suggest adding a methods section with deep detailed description of survey development with validation, survey distribution, target population (geographic area, language, details about list). The Authors should add this section with the aim to allow the repetition of the study by other investigators, key information and steps used to product the results need to be reported.

**********

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Reviewer #1: Yes: Dónal O’Mathúna

Reviewer #2: No

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

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PLoS One. 2020 Sep 18;15(9):e0238128. doi: 10.1371/journal.pone.0238128.r002

Author response to Decision Letter 0


26 Jun 2020

Dear Reviewers.

Your comments are insightful, greatly useful for our revision, and are much appreciated. As you recommend, we have now shifted our focus to the medical application of genome editing technology and generally away from the agricultural and fish breeding aspects. This shift allows us to contribute more widely to the literature on the technological use of genome editing, in both the scientific and general community.

Please refer to the "Reply to the reviewers' comment" for the further details of our reply.

Thank you again for your invitation to revise.

Attachment

Submitted filename: 3-R3. Reply to reviewer comments.docx

Decision Letter 1

Simone Garzon

11 Aug 2020

Increased Awareness and Decreased Acceptance of Genome-Editing Technology: The Impact of the Chinese Twin Babies

PONE-D-20-07652R1

Dear Dr. Saito,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Simone Garzon

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #3: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you for responding to my earlier comments, particularly making it very clear that this survey was conducted with the Japanese public. While the article is generally written well, it could benefit from one more careful proofreading by someone with excellent English-writing skills. There are places where the English currently is awkward. e.g. p. 2, line 32 "ask" should be "inquire"; p. 3, line 45, the concluding phrase is incomplete grammatically; p. 14, line 187, "the" should be inserted between "was" and "highest".

Otherwise, the article is very good.

Reviewer #3: I carefully evaluated the revised version of this manuscript.

Authors have performed the required changes, improving significantly the quality of the paper.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Dónal O'Mathúna

Reviewer #3: No

Acceptance letter

Simone Garzon

8 Sep 2020

PONE-D-20-07652R1

Increased Awareness and Decreased Acceptance of Genome-Editing Technology: The Impact of the Chinese Twin Babies

Dear Dr. Saito:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Simone Garzon

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Text. Questionnaire.

    (DOCX)

    S1 Table. Summary statistics of pre-registered and survey sample.

    (XLSX)

    S2 Table. Awarenesses and their corresponding impressions.

    (DOCX)

    S3 Table. Summary statistics of survey sample: ‘Not being aware’ and ‘Being aware’.

    (XLSX)

    S4 Table. Summary statistics of respondents included in multinomial logit analysis.

    (XLSX)

    S5 Table. Data and definition.

    (XLSX)

    Attachment

    Submitted filename: 3-R3. Reply to reviewer comments.docx

    Data Availability Statement

    All relevant data are available within the paper and supporting information files.


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