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. 2021 Apr 9;16(4):e0249835. doi: 10.1371/journal.pone.0249835

Microbiome research in general and business newspapers: How many microbiome articles are published and which study designs make the news the most?

Andreu Prados-Bo 1,2,*, Gonzalo Casino 1,3,*
Editor: Federico Neresini4
PMCID: PMC8034714  PMID: 33836022

Abstract

The microbiome is a matter of interest for science, consumers and business. Our objective is to quantify that interest in academic journals and newspapers, both quantitatively and by study design. We calculated the number of articles on the microbiome from the total number of biomedicine articles featured in both PubMed and Spanish science news agency SINC, from 2008 to 2018. We used the Factiva database to identify news stories on microbiome papers in three general newspapers (The New York Times, The Times and El País) and three business newspapers (The Wall Street Journal, the Financial Times and Expansión), from 2007 to 2019. Then, we compared news stories with microbiome papers in PubMed, while also analyzing the frequencies of five study design types, both in the newspapers and in the papers themselves. Microbiome papers represented 0.8% of biomedicine papers in PubMed from 2008 to 2018 (increasing from 0.4% to 1.4%), while microbiome news published by SINC represented 1.6% of total biomedical news stories during the same period (increasing from 0.2% to 2.2%). The number of news stories on microbiome papers correlated with the number of microbiome papers (0.91, p < 0.001) featured in general newspapers, but not in business ones. News stories on microbiome papers represented 78.9% and 42.7% of all microbiome articles in general and business newspapers, respectively. Both media outlet types tended to over-report observational studies in humans while under-reporting environmental studies, while the representation of systematic reviews of randomized controlled trials, randomized controlled trials and animal/laboratory studies was similar when comparing newspapers and PubMed. The microbiome is receiving increasing attention in academic journals and newspapers. News stories on the microbiome in general and business newspapers are mostly based on research findings and are more interested in observational studies in humans and less in environmental studies compared to PubMed.

Introduction

On 19 December 2007, four years after the completion of the Human Genome Project, the Human Microbiome Project (HMP), conceived as a “second human genome project” [1], was launched. HMP focuses on microbial communities and their genomes on and in the human body, collectively known as the microbiome [2]. Research into the microbiome dates back to the early 20th century [3]. The 21st century, however, has witnessed a paradigm shift regarding the crucial role microbes play in the way ecosystems—from the ocean to the human body—function, rather than only being seen as infectious pathogens [4].

Relationships between microorganisms living in our bodies—especially in the gut—and health and risk of disease are currently a major focus of research, public interest and potential business for the pharmaceutical and health industries [4]. Much research in the field has focused on the link between the microbiome and physical and mental well-being, with current unknowns highlighting the need for advancement [5]. An altered human microbiome has been associated with the development of a wide range of diseases, including inflammatory bowel disease, metabolic syndrome, autoimmune disorders, and brain diseases, although causation has yet to be established [6]. Furthermore, microbiome research also has implications for food production [7] and for achieving an environmentally sustainable future [8].

As scholarship and investment in microbiome research develop, it is also important to address the impact of that research in general and business newspapers, which are relevant sources of information and can influence the decisions of the public, investors, health decision makers and healthcare practitioners [9,10]. Scientific articles mentioned in the lay press receive, on average, more citations in academic journals than comparable publications from the same journal that did not appear in the lay press [1116]. The factors associated with greater levels of newspaper coverage for scientific papers have also been studied. They include the prestige of the journal [17], the availability of press releases [1822], the domestic preference of newspapers for journals from their own country [23], and the newsworthiness of the topic [24].

Although nowadays many people do not obtain their information directly from newspapers, news from traditional media outlets continues to dominate the information repertoire of mobile internet users [25,26]. Social media, which has become an emerging source for keeping up with scientific issues [27], also relies heavily on newspapers to disseminate news among young people and adults [28,29].

Despite the current scientific interest in the microbiome, its social impact in newspapers has not been properly analyzed. One relevant way of studying the subject is by analyzing the number of newspaper articles in which authors, papers or journals are cited (called “press citations”) [18,23,30]. As such, our first objective was to analyze the extent to which the predictable increase in the number of microbiome papers in recent years has had a parallel impact in the press, in both general and business newspapers, given the potential for harnessing the human microbiome to prevent, diagnose or cure disease.

Previous studies showed that study designs based on weak methodology (i.e. observational and animal or laboratory studies) are more likely to be covered in newspapers than those of superior quality (i.e. randomized controlled trials) [18,31,32]. Microbiome research over the past two decades has mainly focused on characterizing microbiome composition across cohorts of clinical patients and matched controls, and on using animal models to understand the causal mechanisms [33]. We hypothesize that studies’ methodological rigor is not a major driver when selecting news stories on the microbiome for coverage by newspapers. Our second objective was to undertake a controlled comparison of the study designs of the microbiome papers featured in newspapers against those of the microbiome papers that appear in PubMed. Such an analysis allows us to build a picture of microbiome science’s current level of maturity, which shapes both society’s perception and the decisions individuals make in relation to their health.

Methods

Newspaper coverage of microbiome research

Based on previous studies of press coverage of biomedical research [3437], we used the Factiva database to search for news stories on the microbiome in three general newspapers (The New York Times, The Times and El País) and three business newspapers (The Wall Street Journal, the Financial Times and Expansión) from the United States, the United Kingdom and Spain, respectively. Those three countries were selected as they were representative of three previously identified national patterns (American, British and Western World) of biomedical reporting in the press [23]. Print and online editions of each newspaper were analyzed together, after ruling out duplicate news stories. The period analyzed begins in 2007—when the HMP was launched [38]—and ends in 2019.

Fig 1 shows how news stories on the microbiome were selected and categorized. First, we identified news stories in the Factiva database from the 6 newspapers that mentioned the microbiome and its hyponyms in any part of the text, no matter how many times. We excluded duplicates, infographics and other non-relevant news stories, as well as those in which the term microbiota referred to Microbiota decussata, commonly known as Siberian cypress, or plant flora. After filtering out opinion articles and editorials [19], we went on to study the newspapers’ interest in the microbiome (first objective), for which we identified news stories that devoted 50% or more of the text length (estimated by word count) to reporting on the microbiome (n = 518) [39]. Then, to analyze which study designs made the news compared to PubMed (second objective), we focused on microbiome news stories that cited at least one scientific paper (n = 361). For this objective, news stories with the following characteristics were excluded [19]: 1) the microbiome was reported but without reference to a specific study; 2) the microbiome was not a variable of the scientific paper cited in the news story; or 3) the news story was based on premature microbiome research not published in peer-review journals, such as studies presented at scientific or press meetings and ongoing clinical trials registered in the ClinicalTrials.gov database.

Fig 1. Process flow diagram of the categorization of news stories on microbiome papers.

Fig 1

Additionally, we studied news interest in the microbiome in the context of biomedicine by quantifying news stories citing the microbiome in the headline and published by SINC, which is a Spanish publicly-funded news agency specializing in science and technology. SINC agency (https://www.agenciasinc.es/) was chosen because it publishes under a Creative Commons 4.0 license and most Spanish newspapers and scientific online sources usually pick up SINC articles to inform the public.

The microbiome in the context of biomedicine

To estimate the relative interest in microbiome research in the context of biomedical research as a whole, we counted both papers on the microbiome and the total number of scientific publications in the PubMed database of biomedical literature from 2008 to 2018. News agency SINC, which classified news about biomedicine separately until 2018, was used to count the number of news stories on the microbiome against the whole of the biomedicine category. We used data from SINC because the number of news stories on biomedicine in newspapers cannot be calculated using Factiva. Thus, we had an estimate of the press interest in the microbiome from 2008 (when SINC was founded) to 2018 (when it finished categorizing news stories) to compare with the estimate in PubMed.

Study designs of microbiome papers in PubMed and research news

We adapted the criteria used by Bartlett et al. [18] and Lai and Lane [31] for categorizing the study design of medical research news to microbiome research. As such, we classified the microbiome paper study designs available in PubMed and reported in newspapers into 6 categories: 1) systematic reviews (SRs) with or without meta-analyses of randomized controlled trials (RCTs) in humans; 2) RCTs in humans; 3) human observational studies (defined as prospective and retrospective cohort studies, ecological studies, case-control studies, SRs not of RCTs, and case series); 4) environmental & plant studies (agricultural, aquatic, atmospheric, built environment and terrestrial ecosystems) [40]; 5) animal or laboratory studies; and 6) other designs (interventional studies without randomization and/or without a control group, case reports, narrative or nonsystematic reviews, consensus and reports of expert committees). We excluded commentaries, editorials, perspectives and letters, as such articles do not usually contain research evidence and are not always peer-reviewed [31]. Each scientific study cited in the press was identified on PubMed and downloaded for study design characterization. In PubMed, we set the MeSH and natural terms search to title, abstract and keywords, and applied filters for study designs. It should be acknowledged that PubMed counts articles published in online and print versions separately [41]. The searches were performed by one author (APB) between January and March 2020. Search phrases and filters used in Factiva and PubMed are listed in the supplementary S1 and S2 Files and the data acquired and used for analyses are included in S1 Dataset.

Statistical analyses

The primary outcome variable was the number of news stories on the microbiome collected by year from 2007 to 2019 that cited at least one scientific paper. That variable was presented as the mean and standard deviation for the overall sample and subinterest groups: individual newspapers, country (United States, United Kingdom and Spain) and newspaper type (general and business).

The relationship between two quantitative variables was evaluated using the Pearson correlation (linear adjustment): the number of news stories on microbiome papers per year in newspapers and published by SINC and the number of microbiome papers per year in PubMed. The average annual percentage change was evaluated for both the overall sample and the subinterest groups: individual newspapers, country and press type. Finally, the comparison between microbiome news/biomedicine news published by SINC vs microbiome papers/biomedicine papers in PubMed was carried out using a Chi Square test.

The level of significance was set at 0.05. Version 3.5.2 of software R (SPSS Inc., Chicago, IL, USA) and version 4.7.0.0 of the Joinpoint Regression Program were used for all analysis work.

Results

Newspaper coverage of microbiome research

Overall, 518 news stories with the microbiome as the main topic were published from 2007 to 2019, of which 361 cited at least one journal article (286 in general newspapers and 75 in business newspapers) (Fig 1). News stories on microbiome papers showed an irregular pattern of evolution compared to microbiome papers in PubMed (Fig 2A). Apart from a peak in 2008, the interest of general newspapers in microbiome research picked up steadily after 2012 with peaks in 2013, 2016 and 2018 (Fig 2B). News stories on microbiome papers represented 77.9% of overall news stories on the microbiome in The New York Times, 74.1% in The Times, and 78.6% in El País. The New York Times showed the most intense microbiome research coverage (10.3 news stories on microbiome papers annually), followed by The Times (6.8 news stories on microbiome papers annually) and, lastly, El País (5.1 news stories on microbiome papers annually) (Table 1).

Fig 2. News stories on microbiome papers compared to microbiome papers in PubMed.

Fig 2

(A) Individual newspapers; (B) General vs business newspapers; (C) Newspapers grouped by countries (the USA, the UK and Spain); (D) Microbiome news/biomedicine news published by SINC (2008–2018) vs microbiome papers/biomedicine papers in PubMed (2007–2019). Microbiome papers in PubMed are presented as a black curve on each graph.

Table 1. Number of news stories on microbiome papers, microbiome papers in PubMed, microbiome news published by SINC and correlations between them.

Annual cites from 2007 to 2019 Cites in 2007 Cites in 2019 Average annual percentage change Correlations with microbiome papers in PubMed1 (p-value) Correlations with microbiome news published by SINC1,2 (p-value)
Microbiome papers in PubMed 9297,0 (6063.3) 2600 21292 19.6% - 0.62 (0.023)
Biomedicine papers in PubMed 1111673,6 (203280.1) 785933 1397557 4.9% - -
Microbiome/biomedicine in PubMed 0.8% 0.4% 1.4% 9.6% - -
Microbiome news in SINC2 8,1 (5.9) 0 9 24.8% 0.62 (0.023) -
Biomedicine news in SINC2 582.1 (81.1) 666 447 -3.7% - -
Microbiome/biomedicine in SINC2 1.6% 0.2% 2.2% 19.5% - -
Total newspapers 4.6 (4.9) 2.3 (2.2) 7.8 (7.5) 13.9% 0.88 (<0.001) 0.66 (0.014)
Individual newspapers
The New York Times 10.3 (6.4) 5 20 16.0% 0.83 (0.005) 0.48 (0.095)
The Times 6.8 (4.4) 5 13 14.3% 0.82 (0.005) 0.47 (0.102)
El País 5.1 (4.0) 1 8 22.7% 0.74 (0.004) 0.71 (0.006)
The Wall Street Journal 4.1 (1.8) 2 4 2.9% 0.14 (0.652) 0.35 (0.236)
Financial Times 1.5 (1.6) 1 2 11.8% 0.39 (0.177) 0.58 (0.038)
Expansión 0.2 (0.6) 0 0 4.3% 0.41 (0.166) 0.11 (0.713)
Country
USA 7.2 (5.6) 3.5 (2.1) 12.0 (11.3) 12.0% 0.85 (0.002) 0.57 (0.039)
UK 4.1 (4.2) 3.0 (2.8) 7.5 (7.8) 14.5% 0.81 (0.001) 0.57 (0.042)
Spain 2.7 (3.7) 0.5 (0.7) 4.0 (5.7) 23.1% 0.75 (0.003) 0.68 (0.010)
Newspaper type
General newspaper 7.4 (5.4) 3.7 (2.3) 13.7 (6.0) 15.7% 0.91 (<0.001) 0.61 (0.024)
Business newspaper 1.9 (2.1) 1.0 (1.0) 2.0 (2.0) 7.2% 0.39 (0.185) 0.56 (0.043)

Mean followed by the standard deviation in parentheses is indicated for microbiome/biomedicine papers in PubMed, microbiome/biomedicine news in SINC and news stories on microbiome papers in newspapers.

1The numbers showed the Pearson correlation coefficient.

2News stories published by SINC were available from 2008 to 2018.

Significant p-values are highlighted in bold.

In business newspapers, news stories on microbiome papers represented 56.4% of the overall number of microbiome news stories for The Wall Street Journal, 52.8% for the Financial Times, and 18.8% for Expansión. The Wall Street Journal was the business newspaper that featured microbiome research the most, followed by the Financial Times (4.1 and 1.5 news stories on microbiome papers annually, respectively). In contrast, news stories on microbiome papers in Expansión were almost null (Table 1).

The strong presence of research in news stories about the microbiome in the press was also supported by significant correlations between the number of news stories on microbiome papers in general newspapers and the number of microbiome papers in PubMed (r = 0.91, p < 0.001). The magnitude of that association was greater for the American and British general newspapers (r = 0.85, p = 0.002 and r = 0.81, p = 0.001, respectively) than for their Spanish counterpart (r = 0.75, p = 0.003) (Table 1). The strong interest in microbiome research shown by American newspapers compared to British and Spanish newspapers is also apparent in Fig 2C.

As shown in the PubMed curve (Fig 2A–2C), scientific interest in the microbiome gradually grew after 2007 and then picked up speed around 2011. The percentage of microbiome papers available in PubMed and microbiome news published by SINC against the total number of biomedicine publications increased significantly year on year, with a positive annual percentage change of 9.6% and 19.5%, respectively (Table 1). Of the total biomedical literature available in PubMed from 2008 to 2018, the number of microbiome papers increased from 0.4% to 1.4%. Of all the health and biomedical news stories published by SINC, articles citing the microbiome in the headline went from 0.2% to 2.2% from 2008 to 2018, thus doubling the trends shown by PubMed (Fig 2D and Table 1). The comparison between microbiome news/biomedicine news published by SINC vs microbiome papers/biomedicine papers in PubMed almost reached statistical significance (p = 0.052).

Papers covered in the news and number of press citations

In the 361 news stories on microbiome papers, 700 different papers published in scientific journals were cited. Each of those 700 papers was covered in at least one news story in one of the six newspapers. Some papers were covered several times in different news stories from different newspapers or from the same newspaper, resulting in a total of 825 press citations of the 700 papers.

The most cited papers (8 press citations) were “Artificial sweeteners induce glucose intolerance by altering the gut microbiota” (the only paper that was cited in all six newspapers) [42] and “Gut microbiota from twins discordant for obesity modulate metabolism in mice” [43]. Two papers had 7 press citations; 1 paper had 6 citations; 2 papers had 4 citations; 8 papers had 3 citations; 72 papers had 2 citations; and the remaining 613 papers had 1 press citation. The papers were cited in the newspapers generally within three months of publication (64.0% for general newspapers and 48.6% for business newspapers).

Study designs of microbiome papers in PubMed and research news

The study design of microbiome papers available in PubMed between 2007 and 2019 were as follows: 1.8% were SRs of RCTs in humans; 10.9% were RCTs in humans; 8.5% were human observational studies; 46.5% were environmental & plant studies; 30.4% were animal or laboratory studies; and 1.9% had other designs (see methods).

Fig 3 illustrates the over-representation (the percentage of microbiome study design in the press was higher than in PubMed) or under-representation (the percentage of microbiome study design in the press was lower than in PubMed) of microbiome study designs in newspapers vs PubMed. A common pattern was observed among the general and business newspapers that was characterized by an over-representation of observational studies in humans and an under-representation of environmental & plant studies. In contrast, SRs of RCTs in humans, RCTs in humans and animal or laboratory studies tended to be represented to the same degree in newspapers as in PubMed (Fig 3A and 3B).

Fig 3. Over-representation and under-representation of microbiome study designs in the press vs PubMed.

Fig 3

In terms of study design, no major differences were found between countries (Fig 3B). However, particular features were observed when analyzing newspapers at an individual level. The New York Times showed an over-representation (five-fold increase) of SRs of RCTs in humans, while The Times over-represented (seven-fold increase) RCTs compared to PubMed. In contrast, business newspapers covered a similar number of observational studies in humans and animal/laboratory studies (58/181 and 54/181), with the latter over-represented in The Wall Street Journal (Fig 3A).

Discussion

This is the first study to explore how high-circulation newspapers cover microbiome research in terms of the number of news stories and study design compared to PubMed. Our analysis shows some patterns across newspapers.

First, it should be noted that the proportion of papers on the microbiome in relation to all papers in PubMed has increased steadily from 2007 to 2019, with significant year-to-year growth. That proportion is difficult to estimate for newspapers as they do not classify biomedicine news separately from other news, but a similar increase is shown in publications by SINC, which categorized biomedical news separately until 2018.

Second, an increase in the number of microbiome papers from 2007 to 2019 has resulted in newspapers paying considerable attention to microbiome research, albeit not in a balanced proportion between newspapers. The first peak in press coverage of microbiome research in general newspapers, which took place in 2008, can be explained by the fact that that was the year when large human microbiome research initiatives were launched. They included the first phase of the HMP, the International Human Microbiome Consortium, the EU’s Metagenomics of the Human Intestinal Tract (METAHIT) project and the Canadian Microbiome Initiative, among others [40]. The subsequent publication of milestone papers in June 2012, reporting on five years of research, triggered an increase in the newspapers’ interest in the microbiome [44]. A news peak in 2013 was observed in The New York Times, with half of the stories covering research into microbes’ role in obesity and cardiovascular disease. That sudden increase also reflects the launch of the second wave of human microbiome projects, including the second phase of the HMP, the European Commission-funded My New Gut program and the French Government’s MetaGenoPolis program [40].

Third, business newspapers are not as sensitive to the two waves of microbiome research projects as general newspapers. That may have two explanations. On the one hand, microbiome-related patents have increased less markedly than scientific publications [45]. On the other hand, no microbiome therapeutics requiring US Food and Drug Administration and European Food Safety Authority or European Medicines Agency scrutiny have been approved for human use as yet [46].

Fourth, the American and British newspapers were the ones to mention microbiome papers the most. That is not surprising because the US-based National Institutes of Health (NIH) has provided nearly two-thirds of funding for microbiome research [45]. The findings also reflect American and British journalism’s longer scientific tradition and the countries’ dominant position in the scientific literature [23]. British and American newspapers also echo the top medical journals the most, with The New York Times standing out [23]. Similarly, The New York Times covered the Human Genome Project the most [1].

Fifth, the abundance of observational studies in humans in newspapers may be rooted in the over-representation of this kind of study design in press releases from journals and institutions [18,21], which can influence the content of subsequent microbiome news stories [22]. Our results are in agreement with those of Lai and Lane, who found that English-language general and business newspapers were more likely to cover observational studies and less likely to feature SRs of RCTs, RCTs and animal/laboratory studies [31]. Similar to our findings in general newspapers, the authors identified a similar percentage of systematic reviews of RCTs and animal/laboratory studies in the press (3% and 17%, respectively), but did not provide a comparison group of study designs available in PubMed [31]. Previous research showed that, when choosing observational studies, the press covers study designs of a lower quality (such as those with smaller sample sizes) compared to those published in high impact medical journals. That, in turn, might contribute to distorting the end image of medical advances [32]. The remarkable under-representation of environmental & plant studies in the newspapers under analysis might be rooted in the fact that these studies may be less newsworthy because they do not have a direct impact on human health. Indeed, surveys have shown that the topics of greatest interest to society are those of medicine and health, with scientific and technological discoveries and the environment and ecology generating far less interest [9,47]. Second, the level of knowledge required for journalists to understand and communicate the findings of these kinds of studies in layman’s terms can be higher than that required for observational study types, which could lead to their under-representation in the press. Third, environmental & plant studies are not usually published in top journals, which generally issue press releases, and that can have a negative effect on their impact in newspapers [1822].

It is also important to acknowledge that the over-representation of observational study designs can distort the public’s perceived image of the microbiome, as those study design types are often reported inaccurately in newspapers and usually do not mention any associated caveats and limitations [48]. For instance, while an altered microbiome has been reported in a wide variety of health conditions, such as irritable bowel syndrome, obesity and depression, often, it cannot be determined whether differences in the microbiome are causing the disease or, conversely, if the disease itself is causing the differences [49]. The fact that SRs of RCTs, RCTs and animal or laboratory studies tended to be represented to the same degree in newspapers compared to PubMed, with animal or laboratory studies being the second type of study design most cited in PubMed, reflects how microbiome research is still mainly based on basic science. It is worth highlighting that the reporting of SRs of RCTs and RCTs in The New York Times and The Times, respectively, may be seen as an indicator of good quality journalism. It should also be noted that the USA and the UK are the countries that produce the most Cochrane SRs [50] and that newspapers tend to report more on domestically produced science [23]. On the other hand, the over-representation of animal/laboratory studies in the business newspapers, which is mainly down to The Wall Street Journal, is expected as preclinical microbiome research (representing 30.4% of microbiome studies in PubMed) is the first step towards developing microbiome therapies, and that is where most companies’ initial efforts begin. Only a handful of microbiome-related products have entered the end phase of clinical trials [46] and that is reflected in reduced coverage of RCTs in the business press.

Beyond the study design of microbiome papers, the fact that we focused on influential newspapers in terms of readership and circulation might explain the intense coverage of scientific articles about the microbiome, as these newspapers usually have large science and medicine sections with specialist reporters [23]. Other factors might also explain why some microbiome papers are finally echoed by newspapers. They include the impact factor of the journal [16,17], the availability of press releases [1822], the domestic preference of newspapers for journals from their own country [23], and the newsworthiness of the topic [24]. The last factor is especially relevant in the case of the microbiome, due to the ever-increasing interest among both researchers and the lay public in targeting the microbiome to maintain health and quality of life [4]. An overall analysis considering all of these factors is needed to better elucidate how microbiome research is echoed in the media.

In the light of the ever-increasing amount of research about the link between the microbiome and human health and disease [4], one of the field’s urgent needs is precisely that of ensuring unbiased communication of microbiome research to the general public. In that regard, some journals published by the BMJ group indicate the evidence type and subjects studied to journalists when sending embargoed press releases, which may help inform reporting on microbiome findings [51,52]. Keeping up with the huge amount of research and publications on the microbiome and receiving training in science communication skills are also necessary for communicating microbiome research with caution and free from misinterpretation [4]. The European Society of Neurogastroenterology & Motility’s Gut Microbiota for Health platform (https://www.gutmicrobiotaforhealth.com/) is an example of a project that aims to translate the latest research on the rapidly-evolving field of the gut microbiome for both the scientific community and the lay public.

Although scientific interest in microbiome research has driven an increase in news stories based on research findings, the patterns observed in study design coverage need to be tracked in order to inform on the evolution of the science behind the current microbial momentum being experienced by society. For microbiome scientists, the coverage of their research in newspapers and its dissemination in social media can improve their visibility and scientific citations. It is also important to acknowledge the potential role of media coverage in obtaining research funding, without forgetting that, although mentions of scholarly outputs on social media and news sites are becoming increasingly present in policy papers and research calls, it is too early to consider whether they contribute to the awarding of research funding [53].

One strength of our study is that we focused on both general and business newspapers ranked high in circulation from different countries over a long period of 12 years. Rather than gauging only news stories considered immediately newsworthy (that is, generated in response to a paper within 2 months of its publication), we analyzed all news stories on microbiome papers regardless of paper publication date. In addition, we analyzed the number of news stories on microbiome papers and study designs reported in newspapers vs patterns in PubMed.

Our study also has limitations. We did not focus on studying the impact of microbiome research in other mass media such as low-circulation newspapers, magazines, radio, television or the Internet. Moreover, our selection of international general and business newspapers is not representative of the general and business press around the world, even though our selection includes some of the most widely read and best quality international newspapers. Furthermore, our analysis only focuses on quantitative aspects. As a result, the study of all representations of the microbiome in the selected newspapers, regardless of whether they cite a scientific study, is limited in scope and deserves the application of a qualitative methodology that is outside the scope of our research objectives. Other authors have previously addressed newspaper coverage of the microbiome based on qualitative aspects, such as the tone of the discourse [54] and language employed to discuss advances in the microbiome [55], highlighting the need for microbiology literacy in society due to the role of microbes in the health of our planet [56]. Finally, analyzing the press citations of authors, papers or journals also has its limitations, given that their mentioning in newspaper articles does not provide any information about the context of the citation or the quality of the journalistic text.

Conclusions

Our results show that the microbiome is receiving increasing attention in both research and the press. News stories on the microbiome in both the general and business press during the period under study were mostly based on research findings. While the volume of microbiome-based scientific studies in the press mirrors the number of scientific papers in PubMed, the choice of studies covered by general and business newspapers over-represent observational studies and under-represent environmental & plant studies, while showing a similar degree of representation for SRs of RCTs, RCTs and animal or laboratory studies.

Supporting information

S1 File. Factiva search filters and phrases.

(DOC)

S2 File. PubMed search filters and phrases.

(DOC)

S1 Dataset. Data acquired and used for analyses.

(XLSX)

Acknowledgments

We wish to thank Mireia Bosch, Juan Carlos Martín and Queralt Miró for their support with data management and statistical analyses, and María García-Puente, Alicia Jarillo and Marta Diaz for their assistance with searches in PubMed. We also appreciate the critical insights received from Prof. Paul Enck while preparing the manuscript.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

The authors received no specific funding for this work.

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Decision Letter 0

Bright Nwaru

7 Sep 2020

PONE-D-20-23472

Microbiome research in general and business newspapers: which study designs make the news?

PLOS ONE

Dear Dr. Prados-Bo,

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APB is a paid consultant to companies commercially involved in the gut microbiota and probiotics. GC has declared no competing interests."

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Reviewer #1: In the manuscript entitled “Microbiome research in general and business newspapers: which study designs make the news?" the Authors provide a comprehensive statistical overview of a time span of a decade of microbiome related articles in three general newspapers, three business newspapers and from scientific articles featured in PubMed, as well as in the science news agency SINC. Besides showing the increased relative abundance of microbiome associated articles in these newspapers and in the scientific database PubMed, the authors characterized the design type of the primary literature articles allowing insight onto the impact on the press. It is an interesting analysis, but the scope and conclusions are rather limited. To assure a better quality of the submitted paper, there are several suggestions to be considered:

Major points

1. The exact and long-term aim of such analysis could be better explained. It is important for researchers to translate their results to the general public. What they can improve?

2. Are the news coverages coming from the article press-releases? This is important to address.

3. It would be interesting to analyze if the citations of the paper depend on press coverage.

4. The remarkable under-representation in the press of environmental & plant studies should be better explained in the discussion. A potential reason could be that environmental & plant studies are harder to apprehend in context of the microbiome to make reader-friendly stories in the press. (?)

5. The limitations of the study by not including the impact of microbiome research in other media have been mentioned in the discussion. A short explanation of the methodological limitations using other types of media could underline the reason for the restricted methods with “only” six newspapers analyzed.

Minor points

1. The visualization of filtering process in Fig.1 could be improved by highlighting the selected paths for analysis.

Reviewer #2: In the current manuscript the authors performed an analysis of microbiome study coverage in general and business newspaper from 2008-2018. The topic is potentially of interest for the scientific community to reach the best coverage of their finding in the news. However, there are several limitations due to the reported findings.

1) For this reviewer it is completely unclear how the authors evaluated the media coverage of certain articles. As far as I interpreted the reported data, the authors have classified articles available on PubMed regarding study evidence. I would prefer to have a comparison between top quality RCTs regarding media coverage. What was the reason for reports in the media? This would support scientists in getting their research recognized by lay audience via media coverage.

2) What was the difference between the three countries and did the authors evaluate reasons for the observed differences?

3) There should be a fact box included on game changers regarding media coverage of scientific data.

4) Was the media coverage accompanied by better funding of research groups? This would be essential information that could enhance the impact of the reported data.

5) Additionally the authors only report regarding newspapers, which is not targeting the younger population. What about social media, online publications,..?

6) In the current form, the data of the manuscript might be better reported in a letter to the editor.

Minor comment:

1) Fig.1. Please specify what Op-Ed is.

2) Please provide more information about SINC (country, city) and why this agency was chosen.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2021 Apr 9;16(4):e0249835. doi: 10.1371/journal.pone.0249835.r002

Author response to Decision Letter 0


29 Oct 2020

Academic editor’s comments:

Journal requirements

01 Please ensure that your manuscript meets PLOS ONE’s style requirements, including those for file naming.

Both new files ‘Revised Manuscript with Track Changes’ and ‘Manuscript’ meet PLOS ONE’s style requirements regarding title, author, affiliations and main body. We have also updated file naming for figures and for supporting information, which have been resubmitted to meet PLOS requirements.

02 Thank you for stating the following in the Competing Interests section:

"I have read the journal's policy and the authors of this manuscript have the following competing interests:

APB is a paid consultant to companies commercially involved in the gut microbiota and probiotics. GC has declared no competing interests."

Please confirm that this does not alter your adherence to all PLOS ONE policies on sharing data and materials, by including the following statement: "This does not alter our adherence to PLOS ONE policies on sharing data and materials.” (as detailed online in our guide for authors http://journals.plos.org/plosone/s/competing-interests). If there are restrictions on sharing of data and/or materials, please state these. Please note that we cannot proceed with consideration of your article until this information has been declared.

Please include your updated Competing Interests statement in your cover letter; we will change the online submission form on your behalf.

We have included our updated Competing Interests statement in the cover letter so the online submission form may be changed on our behalf.

Reviewers’ comments: review comments to the author

Reviewer #1

Major points

01 The exact and long-term aim of such analysis could be better explained. It is important for researchers to translate their results to the general public. What they can improve?

Thank you for your consideration.

We have changed the way we state the aim and scope of our analysis in the introduction and discussion of the manuscript.

02 Are the news coverages coming from the article press-releases? This is important to address.

Thank you for acknowledging this point. Although this objective has not yet been studied in the context of the microbiome, it has been subject to considerable study for different scientific and biomedical topics (Entwistle, 1995; De Semir et al., 1998; Stryker, 2002; Schwartz et al., 2012). For instance, one of the manuscript’s authors has documented that journalistic articles in the Spanish press discussing current biomedical issues are intensely mediated by press releases (Casino, 2015).

The study of microbiome-related press releases does not seem to be a priority at the moment and such an exercise will require another methodology that is outside the scope of our manuscript.

We have clarified in the introduction of the manuscript that the influence of press releases on news coverage of scientific and biomedical topics has been widely studied.

03 It would be interesting to analyze if the citations of the paper depend on press coverage.

Thank you for your observation. Previous studies cited in the manuscript’s introduction have shown that scientific articles that receive press coverage have, on average, more citations in the scientific literature compared to those not mentioned in the press.

Exploring to what extent citations of microbiome papers depend on press coverage is outside the scope of this manuscript.

In the introduction of the first submitted version of the manuscript, we cited studies (references 11-16) supporting the influence of press coverage on subsequent scientific citations.

04 The remarkable under-representation in the press of environmental & plant studies should be better explained in the discussion. A potential reason could be that environmental & plant studies are harder to apprehend in context of the microbiome to make reader-friendly stories in the press. (?)

Thank you for encouraging us to reflect on an explanation for the under-representation in the press of environmental & plant studies.

We have explained in the discussion that the remarkable under-representation of environmental & plant studies in the newspapers under analysis might have its roots in the fact that the level of knowledge required to understand and communicate their findings in layman’s terms is higher than that required for observational study types. In addition, environmental & plant studies are usually published in less prestigious journals that probably do not issue press releases. Third, the studies may be less newsworthy because do not have a direct impact on human health. We have also acknowledged that the over-representation of observational study designs can distort the public’s perceived image of the microbiome, as those study design types are often inaccurately reported in newspapers and usually do not mention any associated caveats and limitations.

05 The limitations of the study by not including the impact of microbiome research in other media have been mentioned in the discussion. A short explanation of the methodological limitations using other types of media could underline the reason for the restricted methods with “only” six newspapers analyzed.

We are aware that we have not included any other mainstream media, social media or blogs in our analysis.

In response to your insightful comment, we have stated in the introduction that, although most people go online to search for information about scientific issues, newspaper content continues to dominate the online information repertoire over other media types.

Analyzing press citations has advantages over alternative metrics (known as altmetrics) for scientific publications in websites, blogs and social media. That is because the press is the main news producer and allows for reproducible tracking of newspaper articles on a specific topic within a defined period of time via the Factiva database, used in previous studies looking at the press coverage of biomedical research. That is not always possible for a content analysis of other types of media.

In addition, the selection of the sample of six newspapers responds to three patterns of reporting biomedical research in the press—USA, UK and Western World—described by the author Gonzalo Casino (Casino et al., 2017), which has also been acknowledged in the introduction. As such, our sample selection of newspapers might be seen as an indicator of how other newspapers from the same area of the world report microbiome research.

Minor points

01 The visualization of filtering process in Fig.1 could be improved by highlighting the selected paths for analysis.

We agree with your suggestion for improving the visualization of the methodology used in our manuscript.

We have changed figure 1 of the manuscript and increased the width of the lines to highlight the selected paths that have been used in our data analyses.

Reviewer #2

Major points

01 For this reviewer it is completely unclear how the authors evaluated the media coverage of certain articles. As far as I interpreted the reported data, the authors have classified articles available on PubMed regarding study evidence. I would prefer to have a comparison between top quality RCTs regarding media coverage. What was the reason for reports in the media? This would support scientists in getting their research recognized by lay audience via media coverage.

In an initial step, we downloaded all news stories on the microbiome (excluding opinion-editorial articles) and read all of them individually to identify the study mentioned, based on the author’s name, the name of the journal or by accessing the provided link to the scientific publication. Then, we proceeded with classifying the study design of the microbiome papers mentioned in the press and used study designs published in PubMed between 2007 and 2019 as a comparison group.

Analysis of the impact of study designs in the press is an active area of research that has been applied in the context of biomedical news, as stated in the methods section. We have adapted the criteria used by Bartlett et al. and Lai and Lane for categorizing the study design in newspapers in the context of microbiome research (i.e., we have created a new category for environmental & plant studies due to the special relevance of this research in the microbiome field, according to Stulberg et al.). As a result, in our analysis of newspapers and PubMed, we have considered the 6 study design categories defined in our manuscript as follows: SRs of RCTs, RCTs, observational study types, animal or laboratory studies, environmental & plant studies, and other designs.

In line with the criteria used by Bartlett et al. and Lai and Lane, and given that previous work suggests that large RCTs that report hard outcomes (i.e. high-quality RCTs) usually attract the same press interest as low-quality RCTs, we have not focused solely on the press coverage of high-quality RCTs. However, our classification does differentiate between randomized controlled trials (high-quality RCTs) and intervention studies without randomization and/or without a control group (low-quality RCTs). The latter has been included in the “other designs” category, as stated in the methods section.

Study quality is evaluated after publication and such an analysis would have required a specific methodology (such as the GRADE system), which is outside the scope of this study.

In the methods section, we have clarified the method used for classifying all of the different study design types mentioned in microbiome news stories.

02 What was the difference between the three countries and did the authors evaluate reasons for the observed differences?

Thank you for acknowledging this point.

First of all, we have clarified in the methods section that the three countries (USA, UK and Spain) were selected as they were representative of three previously identified national patterns of biomedical reporting in the press (American, British and Western World).

We have stated in the results section that American newspapers showed a greater interest in microbiome research, followed by British newspapers and, lastly, Spanish newspapers. When it comes to study design, no major differences were found between countries, as shown in figure 3B. However, at an individual level, The New York Times showed an over-representation of SRs of RCTs in humans, while The Times over-represented RCTs compared to PubMed.

We have also evaluated in detail in the discussion the reasons behind the observed differences. American and British newspapers’ considerable interest in microbiome research compared to the Spanish press might reflect the USA and the UK’s longer and more far-reaching scientific tradition and that tradition’s dominant position in the scientific literature. Second, British and American newspapers also echo the top medical journals the most. Third, the over-representation of SRs of RCTs and RCTs in The New York Times and The Times, respectively, may be because the USA and the UK are the countries that produce the most Cochrane SRs and newspapers tend to report more on domestically produced science.

03 There should be a fact box included on game changers regarding media coverage of scientific data.

We agree with the fact that it is important to dedicate special attention in our manuscript to changes in the landscape of coverage of scientific data with the emergence of social media and blogs as news sources.

In the introduction section, we have devoted several paragraphs to discussing online content and social media as new players involved in how scientific data is covered by the media. We also discuss social media’s impact on how the lay public engages with science, but also as a means by which scientists can improve their citations in academic journals. Although the lay public uses the internet as the main source for keeping up-to-date with scientific issues, newspaper content still dominates the online information repertoire and social media are used by newspapers as a way of amplifying their own content.

04 Was the media coverage accompanied by better funding of research groups? This would be essential information that could enhance the impact of the reported data.

Thank you for your comment on the relationship between the funding of research and media coverage of scientific articles.

There is little data in the literature regarding whether media coverage of scientific articles is used by funding entities to assign money for research and this objective is outside the scope of our manuscript.

Competitive research funding devotes part of the budget to communication and dissemination activities, which means more visibility in the media for the research group and thus greater probability of obtaining funding. However, media coverage is only one of the factors that can improve the funding of research projects.

As explained in the discussion, although mentions of scholarly outputs in social media and news sites are increasingly included in policy papers and research calls, it is too early to consider whether they contribute to the awarding of research funding.

05 Additionally the authors only report regarding newspapers, which is not targeting the younger population. What about social media, online publications,..?

We are aware that we have not included social media and other online publications in our analysis.

In the updated version of our manuscript, we have stated in the introduction that even though most people go online to search for information about scientific issues, newspaper content still dominates the online information repertoire over other types of media. In addition, the social media platforms used by the younger population tend to get their information from digital newspaper content. As we are aware of the changing landscape in which traditional media is moving from print to digital platforms, we included in our analysis the digital version of the newspapers under study when they were included in the Factiva database.

06 In the current form, the data of the manuscript might be better reported in a letter to the editor.

We appreciate the reviewer’s suggestion, but both authors consider that the results of this manuscript are original and novel and therefore are a better fit for the research article category. Furthermore, as far as we know, PLOS ONE does not include letters to the editor.

Minor comments

01 Fig. 1. Please specify what Op-Ed is.

Fig. 1 has been updated and includes the explanation of what Op-Ed is (i.e., opinion-editorial articles).

02 Please provide more information about SINC (country, city) and why this agency was chosen.

In the methods section (subsection “Newspaper coverage of microbiome research”), we have provided detailed information about SINC.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 1

Yann Benetreau

22 Feb 2021

PONE-D-20-23472R1

Microbiome research in general and business newspapers: how many microbiome articles are published and which study designs make the news the most?

PLOS ONE

Dear Dr. Prados-Bo,

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Reviewer #3: The second version of the paper addresses most of the comments made by the first round reviewers. Anyway, there are still some points that need to be considered before publication. They are the following:

a) applying the exclusion criteria proposed by the Authors, the news related to microbioma without an explicit reference to scientific papers remain out of the analysis. This is not a problem per se, but if the Authors claim to study the "social impact" of the microbioma's research the generic discourse about it in the newspapers is a relevant aspect. As a consequence, it cannot be completely ignored and if the Authors decide to leave this aspect outside the paper, it should be discussed, at least;

b) moreover, taking into account the above cited selection criteria, it is not surprising "the strong presence of research in the news stories about microbiome in the press". This result, indeed, mostly depends on precisely the application of such exclusion criteria;

c) it should be explained why the scientific papers most cited in the news have gained such a position. In other words, why these paper are more newsworthy than others?

d) the Authors listed three reasons for explaining “the remarkable under-representation of environmental & plant studies in the newspapers”. The last is that this kind of “studies may be less newsworthy because do not have a direct impact on human health”, but I wonder whether this can be actually the first and the most relevant.

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Reviewer #3: No

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PLoS One. 2021 Apr 9;16(4):e0249835. doi: 10.1371/journal.pone.0249835.r004

Author response to Decision Letter 1


11 Mar 2021

Academic editor’s comments

Journal requirements

Question 1: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Answer 1: The reference list of the manuscript has been reviewed in detail. It does not contain papers that have been retracted nor unavailable and unpublished work and personal communications.

All the references included in the manuscript as it stands now meet criteria specified in PLoS One submission guidelines (https://journals.plos.org/plosone/s/submission-guidelines#loc-references).

Reviewers’ comments: review comments to the author

Question 1 from reviewer 3: Applying the exclusion criteria proposed by the Authors, the news related to microbioma without an explicit reference to scientific papers remain out of the analysis. This is not a problem per se, but if the Authors claim to study the "social impact" of the microbioma's research the generic discourse about it in the newspapers is a relevant aspect. As a consequence, it cannot be completely ignored and if the Authors decide to leave this aspect outside the paper, it should be discussed, at least.

Answer question 1 from reviewer 3:

Thank you for acknowledging this point as this question needs to be discussed in depth.

For our first objective of quantifying the six newspapers’ interest in the microbiome, we focused both on news stories on the microbiome that cite at least one scientific paper (361/518=69.7%) and news stories on the microbiome that do not reference a scientific paper (157/518=30.3%), in relation to the total number of news stories that had the microbiome as the main topic. For the second objective of quantifying which microbiome study design made the news the most, we only focused on news stories that explicitly mentioned a scientific publication on the microbiome because we wanted to quantitatively compare that to PubMed publications.

News stories on the microbiome that did not reference a scientific paper can be addressed according to a qualitative methodology that explores several variables, including the topics addressed and the language used to discuss the latest scientific advances in microbiome research. However, this research objective is outside the scope of our manuscript. It should also be acknowledged that other authors have focused on studying news stories on the microbiome from the perspective of language and by using a qualitative methodology (Chuong KH et al. 2015; Nerlich & Hellsten, 2009; Nerlich, 2017).

We have re-written the first part on newspaper coverage of microbiome research in the methods section to better clarify our workflow and analysis. We are aware that excluding news stories that had the microbiome as the central topic but which did not reference a scientific paper is a limitation of our manuscript and have acknowledged this point in the discussion.

Question 2 from reviewer 3: Moreover, taking into account the above cited selection criteria, it is not surprising "the strong presence of research in the news stories about microbiome in the press". This result, indeed, mostly depends on precisely the application of such exclusion criteria.

Answer question 2 from reviewer 3:

Thank you for your comment.

The microbiome is a current hot topic for newspaper coverage and, in an initial step, we applied strict selection criteria to ensure that the news stories under analysis covered the microbiome as the central topic, in an in-depth and objective way.

If a news story mentioned the microbiome or any of its synonyms in a quote, for contextualizing a recipe or in the title of a book, we did not consider them to be relevant enough in terms of informing on the microbiome. Therefore, articles that mentioned the microbiome at some point but where the microbiome was not the focus—i.e. it was discussed in less than 50% of the text—were excluded from our analysis. This sampling process is known to eliminate news stories that contain tangential microbiome-related content (i.e., false positives) (Guasch et al., 2019).

In our first objective of quantifying the newspapers’ interest in the microbiome, we found that news stories on the microbiome that do not mention a scientific article represented a minority (30.3%), in relation to the total number of news stories that had the microbiome as the main topic. As we were interested in doing a controlled comparison between the scientific literature and newspapers, in our second objective, we ruled out news stories on the microbiome that did not mention a scientific paper in order to compare the same variable (mention of a scientific paper) in the six newspapers and in articles collected via PubMed.

We have acknowledged in the discussion the limitation of not considering all representations of the microbiome, regardless of whether they cite a scientific study, in the newspapers we analyzed.

Question 3 from reviewer 3: It should be explained why the scientific papers most cited in the news have gained such a position. In other words, why these paper are more newsworthy than others?

Answer question 3 from reviewer 3:

Thank you for your observation.

There is no one factor alone that can explain why some microbiome scientific articles are more newsworthy than others. In our analysis we have shown that study design could influence journalists’ selection of the scientific papers that will be echoed in newspapers. Beyond study design, our decision to focus on influential newspapers in terms of readership and circulation might explain the intense coverage of scientific findings in the press, as these newspapers have large science and medicine sections with specialist reporters. Other factors that might also be important include the impact factor of the journal, the availability of press releases, the domestic preference of newspapers for journals from their own country, and the newsworthiness of the topic.

We have clarified in the discussion which factors, beyond study design, may explain why some microbiome scientific papers are more newsworthy than others (lines 351-362). To date, different partial analyses have been done studying which factors shape how scientific and medical findings are echoed in newspapers, while in future an overall analysis could clarify which factors have the strongest weight in determining which microbiome scientific papers are finally echoed in the media.

Question 4 from reviewer 3: The Authors listed three reasons for explaining “the remarkable under-representation of environmental & plant studies in the newspapers”. The last is that this kind of “studies may be less newsworthy because do not have a direct impact on human health”, but I wonder whether this can be actually the first and the most relevant.

Answer question 4 from reviewer 4:

Thank you for encouraging us to reflect on this explanation for the under-representation of environmental & plant studies in the newspapers under analysis.

We agree on your point of view. Therefore, we have stated in the discussion that the fact that environmental & plant studies do not have a direct impact on human health might be the most relevant underlying factor in our findings and have placed it in first position on the list. Moreover, we have also cited the findings of two large population surveys that have shown that the topics of greatest interest to society are those of medicine and health, with scientific and technological discoveries and the environment and ecology generating far less interest (National Science Board, 2018; Fundación Española para la Ciencia y la Tecnología (FECYT), 2018).

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 2

Federico Neresini

26 Mar 2021

Microbiome research in general and business newspapers: how many microbiome articles are published and which study designs make the news the most?

PONE-D-20-23472R2

Dear Dr. Prados-Bo,

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.

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Kind regards,

Federico Neresini

Guest Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Federico Neresini

30 Mar 2021

PONE-D-20-23472R2

Microbiome research in general and business newspapers: how many microbiome articles are published and which study designs make the news the most?

Dear Dr. Prados-Bo:

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. Federico Neresini

Guest Editor

PLOS ONE

Associated Data

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

    Supplementary Materials

    S1 File. Factiva search filters and phrases.

    (DOC)

    S2 File. PubMed search filters and phrases.

    (DOC)

    S1 Dataset. Data acquired and used for analyses.

    (XLSX)

    Attachment

    Submitted filename: Response to Reviewers.docx

    Attachment

    Submitted filename: Response to Reviewers.docx

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.


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