What's not in the news headlines or titles of Alzheimer disease articles? #InMice.

There is increasing scrutiny around how science is communicated to the public. For instance, a Twitter account @justsaysinmice (with 70.4K followers in January 2021) was created to call attention to news headlines that omit that mice, not humans, are the ones for whom the study findings apply. This is the case of many headlines reporting on Alzheimer disease (AD) research. AD is characterized by a degeneration of the human brain, loss of cognition, and behavioral changes, for which no treatment is available. Around 200 rodent models have been developed to study AD, even though AD is an exclusively human condition that does not occur naturally in other species and appears impervious to reproduction in artificial animal models, an information not always disclosed. It is not known what prompts writers of news stories to either omit or acknowledge, in the story's headlines, that the study was done in mice and not in humans. Here, we raised the hypothesis that how science is reported by scientists plays a role on the news reporting. To test this hypothesis, we investigated whether an association exists between articles' titles and news' headlines regarding the omission, or not, of mice. To this end, we analyzed a sample of 623 open-access scientific papers indexed in PubMed in 2018 and 2019 that used mice either as models or as the biological source for experimental studies in AD research. We found a significant association (p < 0.01) between articles' titles and news stories' headlines, revealing that when authors omit the species in the paper's title, writers of news stories tend to follow suit. We also found that papers not mentioning mice in their titles are more newsworthy and significantly more tweeted than papers that do. Our study shows that science reporting may affect media reporting and asks for changes in the way we report about findings obtained with animal models used to study human diseases.

Introduction

Scientists have for some time voiced concern that media reporting of scientific findings, especially those related to health and diseases, are often misleading and that journalists frequently make inappropriate inferences regarding causality, using sensational language to describe scientific findings obtained in biomedical studies [1-3]. In March 2019, James Heathers, of Northwestern University, launched the Twitter account @justsaysinmice (with 70.4K followers in January 2021) to call attention to news stories with headlines omitting that the new medical findings they report on are based on research using mice, not humans. This situation, and the use of exaggerated language, is frequently seen in news reporting of health research, and Alzheimer disease (AD) is no exception [4].

AD is characterized by a degeneration of the brain, loss of cognition, and behavioral changes. The main histopathological cerebral hallmarks of AD are extracellular deposits of amyloid-β (Aβ) plaques and the presence of tau proteins in intracellular neurofibrillary tangles. However, questions abound as to how these 2 proteins orchestrate the onset and progression of AD in the human brain and whether there are other important unknown players involved in disease development and progression. It has been shown that while genetics do play a role in AD, lifestyle and other unknown factors seem to impact an individual’s chances of developing AD [5].

Currently, there are no drugs available that can either stop or slow the progress of AD, and the drugs approved by regulatory agencies to be used in AD patients (donepezil, rivastigmine, galantamine, memantine, and a combination of memantine plus donepezil) only treat some of the symptoms of this devastating disease in a limited number of patients [6]. Nevertheless, in 2019 alone, there were 132 agents in clinical trials for the treatment of AD [7]. This dearth of efficacious treatment options is the result of decades of failing clinical trials, in which approximately 99.6% of the drugs previously tested for safety and efficacy in animals were either ineffective or associated with severe side effects when given to AD patients [8]. The poor predictive value of animal models used to study AD, and other human diseases, has resulted in a loss of millions of dollars [9] and yet, drug development success rates are below 5% for most diseases [10].

The first transgenic mouse models of AD were reported in 1995 [11] with the PDAPP model, which was followed by the Tg2576 [12] and the APP23 mouse models [13]. According to ALZFORUM (www.alzforum.org), a comprehensive website that provides information on AD and includes an annotated database of rodent models of neurodegenerative diseases, there are currently 194 models between mouse and rat to study AD. A variety of different approaches have been applied in the attempt to create an animal model that mimics the many characteristics and the cognitive deficiencies seen in AD patients. These approaches include nongenetically modified models in which brain lesions are created in the animal counterpart area believed to be responsible for cognition or by giving injections of Aβ directly into the brain of the animal with the aim to produce some level of cognitive impairment. All these approaches create models with very different pathophysiological and clinical characteristics from the human disease. A number of “humanized” strains of transgenic mice carrying AD mutations have also been created [14]. Each of these models differ from one another, and none exhibits all the main features associated with AD in humans. Even though a number of animals may show some features found in AD patients, e.g., the buildup of amyloid plaques, none presents dementia as recognized in humans. Therefore, it seems correct to state that AD is an exclusively human condition that does not occur naturally in other species and appears impervious to reproduction in artificial animal models.

It is not known what prompts writers of news stories to either omit or acknowledge, in the story’s headlines reporting on AD research, that the study was done in mice. To better understand how writers chose their news headlines in this regard, we raised the hypothesis that they are influenced by article’s titles. To test this hypothesis, we investigated if research papers whose findings apply to mice, and not to humans, but which omit this caveat in their titles, generate significantly more news stories with headlines that likewise omit mice, if compared to research papers with titles that do mention mice. We also investigated if papers omitting mice in their titles generate more news or tweets. To this end, we analyzed a sample of 623 open-access papers indexed in PubMed in 2018 and 2019 that used mice (the most popular animal model to study AD) either as models or as a biological source for experimental research in AD—an exclusively human condition that has become an important public health issue affecting millions of people worldwide.

Our findings support our hypothesis that a strong association exists between news stories’ headlines and research papers’ titles regarding the omission, or not, of mice. News stories’ headlines that omit mice as the main study subject may mislead the public regarding the actual state of affairs in AD research, while they may raise false hopes for patients and their families.

Results

The sampling process

Our sample of 623 papers was composed of 2 groups that we named “declarative” and “nondeclarative.” The declarative group included papers that declared in their titles that mice were the main study’s species (N = 405), while the nondeclarative group included papers in which mice were omitted in the paper’s title (N = 218). Using Altmetric Explorer (a web-based platform that produces a report on digital attention data for research papers, including news stories, social media, and citations), we collected and analyzed the headlines of the digital news stories generated for each group of research papers in our sample and determined whether or not the news headline mentioned mice. Fig 1 shows all steps taken to obtain the groups of papers.

Fig 1

Sampling process.

Sampling process leading to the groups of papers analyzed in this study. AD, Alzheimer disease; OA, open access.

Papers in both groups generate news stories

For the 405 and 218 papers (S1 and S2 Tables) in the declarative and nondeclarative groups, respectively, Altmetric Explorer tracked 382 (94.3%) papers in the declarative group and 212 (97.2%) papers in the nondeclarative group. Of the 382 tracked papers in the declarative group, 295 (77.2%) generated at least 1 news story (a total of 887 news stories or 3.0 stories per paper on average). From the 212 papers of the nondeclarative group tracked by Altmetric Explorer, 173 (81.6%) generated news stories (a total of 682 news stories or 3.9 stories per paper on average; Fig 1). Headlines that were not in English were translated using Google Translate. Because we were interested in detecting specific words in the title, namely mouse, mice, rodents, murine, or animal—see Materials and methods for details—we did not need precise translations. The first question we raised was “is there a significant difference in the number of papers that generated news stories between groups?” We found that that there is no significant difference between groups (p = 0.21; Fig 2).

Fig 2

Significant association between scientific papers’ titles and news stories’ headlines.

Number of declarative and nondeclarative papers refer to papers tracked by Altmetric Explorer. Number of news stories refer to stories with titles. No statistical difference was found for the number of papers that generated stories in each group (p = 0.21), while a significant difference for the number of stories generated by each group of papers was observed (p = 0.012). More important, a strong association was found between the type of title in the scientific article (whether or not declarative) and the type of headline in the corresponding news story (p < 0.01). Note the drawing of a little mouse in the title and headline of the images representing declarative groups.

Nondeclarative papers are more newsworthy

We next asked whether there was any difference between groups for the number of news stories that each group of papers generated. We found that nondeclarative papers generated significantly more news proportionally (3.9 versus 3.0 news per paper or 31.1% more news; Fig 1) than did the papers in the declarative group (p = 0.012; Fig 2).

Of the 887 news stories generated by declarative papers, 25 did not have a headline, resulting in a sample of 862 (97.2%) news stories. Of the 682 news stories reporting on papers in the nondeclarative group, 9 did not have any headline. The final number of news stories generated by nondeclarative papers that we worked with was 673 (98.7%; Fig 2). Of note is the fact that the number of papers originating news stories in either group remained the same.

News writers tend to follow articles’ authors on omitting, or not, mice

Next, we examined the headlines of the news stories generated from articles in each group. We found that of 862 news stories reporting on papers in the declarative group, 398 (46.2%) were declarative as well, meaning that 398 news stories have headlines that mention either mice or another qualifying word we considered (see Materials and methods for a list of qualifying words). However, of the 673 news stories reporting on papers in the nondeclarative group, only 70 (10.4%) were declarative, a difference that is highly significant (46.2% versus 10.4%; p < 0.01; Fig 2). This finding indicates that when authors mention mice in the paper’s title, writers tend to follow suit when crafting the headlines of their news stories.

Note in Fig 2 that only 10.4% (70) of the news stories reporting on papers in the nondeclarative group mention mice in their headlines, compared with 46.2% (398) for news stories that mention mice reporting on papers in the declarative group. Also, 70 declarative news stories were generated from 18 out of 173 papers (10.4%) that generated news stories in the group of nondeclarative papers, while in the group of declarative papers, 398 declarative news stories were generated from 284 papers out of 295 papers (96.3%) that generated news stories. Importantly, of the 1,535 news stories generated from research papers in both groups, only 468 (30.5%) were declarative, while 1,067 (69.5%) omitted mice from their headlines.

News stories posted online often reproduce the original title of the research paper [15]; thus, we examined whether the association we observed between the research paper’s title and the news story’s headline was a function of research papers’ titles being copied into news stories headlines. To answer this question, we first asked if there was a difference between the 2 groups of papers in the number of news stories in which the headline was a verbatim copy of the paper’s title. While in the group of news stories generated from nondeclarative papers 157 headlines were verbatim copies of the research paper’s title (157 out of 673 news stories, 23.3%), in the group of news stories generated from declarative papers, this number was 283 (283 out of 862 news stories, 32.8%), a difference that is highly significant (p < 0.01). This finding could suggest that titles of declarative papers tend to be more frequently copied into news stories’ headlines than titles of nondeclarative papers. However, a closer look at the outlets doing verbatim copies of research papers’ titles revealed that a section in the ALZFORUM website called Papers, in which papers in AD are featured and their full references, including their titles, are transcribed, was virtually the only vehicle doing verbatim copies of papers’ titles. Also, the apparent significant difference we obtained between the 2 groups is in reality a function of the number of papers that a single vehicle, ALZFORUM, posts on its website.

In any case, we excluded all news stories with headlines that were verbatim copies of their corresponding papers’ titles, resulting in 579 original headlines reporting on papers in the declarative group and 516 original headlines for papers in the nondeclarative group. We next tested whether a strong correlation between the type of paper’s title (whether or not declarative) and the news story’s headlines remained. We still found a highly significant difference between groups (p < 0.01; Fig 3).

Fig 3

Significant association between original headlines and papers’ titles.

Number of original news stories’ headlines and their association with research papers’ titles. Of the 579 original headlines generated from declarative papers, 115 (19.86%) acknowledged mice in their headlines, while only 70 original news stories’ headlines (13.57%) generated from nondeclarative papers did the same, a difference that is highly significant (p < 0.01). Note the drawing of a little mouse in the title and headline of the images representing declarative groups. Two news headlines were truncated and we did not find their full versions online. Because the truncated parts were similar to the articles' titles, they were considered verbatim copies.

In the attempt to explain the association between articles’ titles and news’ headlines, we raised the hypothesis that press releases in EurekAlert! (the main repository for science-related press releases) could influence writers on their news stories. However, we observed that a similar pattern for news stories is also found for EurekAlert! press releases, in which declarative papers generated more declarative releases (5 declarative releases out of 22 releases) if compared to nondeclarative papers (1 in 19). We next searched for press releases for any of the 70 articles in the nondeclarative group of papers that generated news stories that had mice in their headlines. We found that only 1 EurekAlert! press release was produced for a single paper among all the 70 nondeclarative research papers. Thus, press releases do not explain the association we found.

We then asked if there was any particularity in these 70 research papers that could have driven writers to write headlines that mentioned mice. Notably, these research papers generated news stories omitting mice in their headlines as well as others acknowledging it, indicating that nothing particular in these papers could be driving writers to choose one way or the other. An initial analysis of the news outlets did not reveal a pattern that could indicate that omitting, or not, mice in the headline was an editorial decision of any kind.

Journal choice does not explain our findings

We next asked whether any of the journals in which these papers were published required that authors informed in the article’s title the main species used in the study. This requirement could explain why some authors acknowledged the use of mice in the paper’s title while others did not. To find this information, we referred to the guidelines of the journals. All 468 papers in both groups that generated news stories (295 + 173) were published in 157 different journals. Of this list, one journal (Cellular Physiology and Biochemistry) is no longer in business due to concerns about the integrity of papers published in the journal in 2017 and 2018. In our samples, we only had 2 papers published in this journal, 1 in each group. Of the 156 journals analyzed, only 8 (5.1%) require that the species used in the study is informed in the paper’s title (S3 Table).

Next, we checked whether there was any article in the nondeclarative group that was published in any of the 8 journals requiring the study’s species to be acknowledged in the title. Surprisingly, we found that 11 (6.4%) articles were published in such journals, indicating that even though these journals require that authors inform the study’s species in the paper’s title, they do not enforce authors to do it. As for articles in the declarative group, we found that only 7.8% papers (23 out of 295 papers) were published in journals that requested the title of the paper to inform the species used in the study. This finding indicates that for most papers in this group (272 papers or 92.2%), acknowledging the studies’ species in the paper’s title was most likely an authorial decision rather than one imposed by journals’ requirements.

Another constraint that may have played a role in authors mentioning mice, or not, in the paper’s title could be word or character number limitations set by the journal guidelines. To investigate this possibility, we again referred to the journals’ guidelines. We found that of the 156 journals we examined, only 39 (25.0%) limited the number of either characters or words allowed in the paper’s title (S3 Table).

We then found that 63 papers out of 173 (36.4%) in the nondeclarative group were published in journals that limit the number of either words or characters in the title, while in the declarative group of 295 papers, this number was 90 (30.5%), a difference that is not significant.

Articles’ titles omitting mice are more often tweeted

We then compared the number of tweets in each group of papers and found a significant difference for the mean number of tweets per paper in each group. While in the declarative group of research papers each paper generated 9.7 tweets (mean number), in the nondeclarative group, each paper generated 18.8 tweets (p < 0.01), indicating that articles’ titles that omit mice are more often tweeted than articles’ titles that openly acknowledge that the study findings apply to mice. Overall, papers in the nondeclarative group generated 2,632 tweets, while papers in the declarative group generated 1,902 tweets (Fig 4).

Fig 4

Significant association between research papers’ titles and tweet counts.

We found a significant association between the research paper’s title (whether or not declarative) and the number of tweets the research paper generates (p < 0.01). Papers’ titles that omit animals are more often tweeted than titles that openly acknowledge that the study was done in animals. Note the drawing of a little mouse in the title of the image representing the declarative group of papers.

Discussion

Here, we investigated the hypothesis that studies using mice as the main research subject, but which omit this information in their articles’ titles, generate significantly more news stories with headlines that likewise omit mice. Our data support our hypothesis that news writers are influenced by article’s titles regarding the omission, or not, of mice in their headlines.

Titles of scientific papers provide short and crucial information for paper retrieval and storage while aiming to raise the reader’s interest. Also, in biomedical research, most titles highlight some aspect of the study’s findings, as opposed to titles that limit to inform what was investigated but offer no information on the results obtained. The former is believed to better attract the reader interest, and, nowadays, is the preferred style adopted. Thus, most titles do carry information about the study results.

Previous studies have shown that the title can have a significant impact on how frequently the paper is cited by others [15]. Of note is the fact that in biomedical studies, the species used is assumed to have been humans, unless the authors inform otherwise. For this reason, most books and guidelines on how to write a title of a scientific paper advise authors that the species used in the study should be informed in the article’s title, when not humans [16-18]. As recommended by Ushma S. Neill in 2007 [19], then the executive editor of the high-impact Journal of Clinical Investigation, “try to get the species studied into the title; this is sometimes complicated if multiple species are used, but it allows readers to immediately put the work in its appropriate context.”

The main argument raised to justify the use of animals as models for human diseases is to advance knowledge about certain human conditions. As already mentioned in the introduction, AD is a condition that only humans develop, and which does not occur naturally, nor can it be experimentally induced in other species. As Dr. Susan Molchan, a geriatric psychiatry, and former NIH researcher and FDA reviewer has once said, “they’ve cured mouseheimer’s disease I don’t know how many times now,” when referring to scientists working with mice to understand AD [20]. Therefore, AD animal models should not be considered as full and valid representations of the human condition. This is a caveat that any study using animal models should inform up front, preferentially in its paper’s title. However, in our sample of 623 mice studies on AD, 34.9% of the papers (218 out of 623) omitted mice in their titles (Fig 1).

As articulated by Daniel Dor in a study entitled “On Newspaper Headlines as Relevance Optimizers” [21] “traditionally, newspaper headlines have been functionally characterized as short, telegram-like summaries of their news items. This is especially true with respect to news headlines.” Headlines play an important role in communication, and they may be the only piece of information that is actually read [2,21]. Indeed, according to a survey done by the Pew Research Center on Science News and Information in 2017 [22], only half of social media users click through science news stories. Of these, 10% do it often, 43% do it sometimes, and the remaining do it hardly, never, or simply do not see science news stories. Therefore, those who do not click through the story are left with the impression caused by the science news headlines only. Also, a study done on social clicks that used multiple data collection techniques to analyze Twitter conversations and clicks for URLs from 5 news sources show that most (59%) of the links on news stories shared in social media (Twitter) are never read [23]. Thus, it seems reasonable to conclude that for most online users, the only part of the news stories read by those who share them is the headline.

In this study, we found no significant difference in the number of papers that generated news stories between groups. However, when we compared the 2 groups of papers for the number of news stories each generated, we found that nondeclarative papers generated significantly more news stories than declarative papers. This finding indicates that nondeclarative papers are more “newsworthy,” if compared to declarative papers. Also, news stories that report on nondeclarative papers tend to omit in their headline that the study’s finding applies to mice and not to humans, revealing that the title of the research paper influences the news headline’s writer regarding omitting, or not, mice. The vast majority (69.5%; 1,067 stories out of 1,535; Fig 2) of the news stories generated from papers in both groups omit mice in their headlines. Often, these headlines overclaim the scientific finding and can lead to misperceptions by the general public. The use of misleading language in news reporting on AD research is not a rare event [4] and has been observed in other diseases such as cystic fibrosis [24] and multiple sclerosis [25].

It has been shown that information that sounds useful to others and which carry a positive and emotionally charged frame that evokes hope has higher chances to be replicated and shared by others [26]. For instance, news headlines such as (i) a common dietary supplement could be the answer to fighting AD; (ii) a diet high in salt causes dementia and other brain problems (translated from Spanish); or (iii) a long-standing antibiotic offers a new path against AD, among others, may leave the public with the impression that these findings are useful and offer hope to AD patients, when in reality they apply to mice, unless new scientific evidence is produced.

These headlines can be considered misleading, which, according to previous studies, can lead to misconceptions and misinformation. Even if readers read the full article, it may not be enough to deconstruct the impression left by a misleading headline [12]. Indeed, a survey done by Harvard School of Public Health and Alzheimer Europe that heard 2,678 individuals in 5 countries (France, Germany, Poland, Spain, and the United States) found that roughly half of the individuals believed that an effective treatment for AD was available at the time or would be available in the next 5 years. The survey was done in 2011 [27]. The dissatisfaction with health reporting has been recognized by journalists, outlet media, and by media-reporting organizations. This sentiment has prompted the creation of groups that oversight news coverage, such as HealthNewsReview.org, and the production of guidelines on how to report health news, by media outlets. One of the articles by HealthNewsReview.org entitled “Why you should be cautious of health claims based on animal and lab studies” aims at helping journalists understand the many caveats of animal studies and how better report on such studies [20].

Another example is the guidelines created for The Age, The Sydney Morning Herald, Brisbane Times, and WAtoday, in Australia, that among many topics explicitly describes that journalists “. . . will treat research based on animal studies with caution, preferring to focus on human trials, and making clear that the results may not translate to human trials” [28]. Similarly, Science Media Centre has produced a guideline that describes 10 best practices for reporting science and health stories that includes “headlines should not mislead the reader about a story’s contents and quotation marks should not be used to dress up overstatement” [29]. Nevertheless, the survey done by the Pew Research Center on Science News and Information [22] revealed that 43% of US adults say that the news media are “too quick to report research findings that may not hold up.” A smaller number of adults (30%) sees as a problem the fact that media oversimplifies scientific findings. Interestingly, 4 in 10 Americans (40%) believe that researchers also play a role on how science news are covered, an impression supported by our findings.

But what objective forces would be driving authors to omit, or not, mice in their research papers’ titles? We considered 2 main hypotheses: a requirement, as defined by the journal guidelines, for the study species to be acknowledged in the paper’s title and/or a constraint imposed by the journal on the number of words or characters allowed in the paper’s title. Neither hypothesis was supported by our data, and thus mentioning or not mice in the title seems to be an authorial decision, for which peer reviewers and journal editors may also play a role, and may reflect particular, and subjective, views.

In 2001, world-renowned evolutionary biologist Svante Pääbo had predicted that the sequencing of the human genome would reveal that our species shares a genetic scaffold with all species on Earth. For mice in particular, the number of genes and the general structure of the genome were expected to be similar to that of humans, highlighting our similarities [30]. Thus, it is possible that some researchers truly see animals, and mice in particular, as smaller and less complex creatures resembling humans, while overlooking the many differences between species at physiological, metabolic, and behavioral levels. Thus, mice may be considered by some as the unspoken norm, and its use in biomedical research is not seen as a caveat that requires further explanation.

Alternatively, a growing body of studies has called into question the scientific value of using animals in biomedical research, thus omitting animals in the study’s title may be a reaction (consciously or not) to this trend [31-35]. It is also possible that some studies’ authors perceive that omitting mice in the title would give them better chances of grabbing the journal’s editor attention or provide higher visibility, which could yield more citations [36]. Indeed, we found that research papers omitting mice in titles generate significantly more news and more tweets than papers that do mention mice (Figs 2 and 4). Thus, omitting mice in the paper’s title significantly improves the paper nonscientific impact (NSI), which has been defined as “the amount of attention given to scientific research by nonscientists in mainstream news outlets, online blogs, and/or social media” [37].

In a recent study that investigated whether an association exists between NSI and the number of citations a given study receives, authors found that research papers that receive more attention in nonscientific media are cited more by other peer-reviewed studies [37]. Thus, it is possible that papers receiving more media attention are and will be more cited. However, because here we considered papers published in 2018 and 2019, we would need more time for citations to accrue before this analysis can be done.

Spin is a concept more often associated with propaganda and journalism, used to influence public opinion, but which has also been found in research articles. Spin may be introduced by many means of p-hacking [38], manipulation of figures [39], or selective reporting of outcomes [40] and may have consequences on researchers’ interpretation of the study findings or clinical decision-making. Thus, omitting mice from the paper’s title may be considered a new class of spin [41] that we propose to classify as “misrepresentation” since the title of the paper is not a short and accurate representation of the full study but rather a misleading brief account that omits an important caveat: the fact that the study was done in mice. Due to the higher NSI of these papers and the fact that most online news stories and most tweets (which are often a mere copy of the work’s title [42]) are not read through, plus the fact that most titles in biomedical research summarize the study findings, this omission may lead to a misunderstanding of the actual implications of the study’s results for human health and its translatable potential to people suffering with AD, contributing to a wave of science misinformation.

Our study has limitations. The articles analyzed in either group constitutes a convenience sample that includes only research articles that are available as open access. This sample represents roughly half of all papers that used mice to study AD during 2 periods (2018 and 2019). We should also add that the results found here apply exclusively for the lists of articles on AD research we investigated and cannot be expanded to other areas without careful analysis. Also, we did not inspect each article thoroughly to check whether there is any characteristic inherent to the study that may explain the choice for mentioning mice, or not, in the title.

To our knowledge, this is the first study to present scientific evidence that the way science is reported by scientists plays a role on the way science news is reported by journalists. Whatever the underlying reasons for such omissions, it is expected that scientists communicate their findings accurately and at high standards. In fact, a much simpler argument is this: Why hiding in the article’s title the species used in the study?

The 2010 NC3Rs Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines, developed by the UK National Centre for the 3Rs to improve reporting of studies using animals, did not specifically recommend authors to inform the species, or strain, used in the study in the title of the research article, being this recommendation limited to the article’s abstract. The 2020 update to the ARRIVE guidelines [43] does not identify the title of a paper as an important element subjected to review. However, we believe the findings presented here provide grounds for further amendment of the ARRIVE guidelines, together with journal publication policy, to give special attention to the article’s title and require the titles of papers describing experimental studies to identify the species and/or tissue sources used in the research.

We expect that our recommendation for amendment to the ARRIVE guidelines will have an impact on the headlines of news stories and then we should start seeing more news stories that, as urged by James Heathers and his more than 70,000 Twitter followers, “just says in mice” in their headlines.

Materials and methods

Study design

We retrieved papers published in 2018 and 2019 and which were indexed in PubMed, which used mice to study AD. Papers published in 2018 were retrieved in June of 2020, and papers published in 2019 were retrieved in December of the same year. We were interested in retrieving 2 different groups of papers: The declarative group would include papers that mention mice in the title, while the nondeclarative group would be formed by papers that did not mention mice in the title. We selected research papers that were published in English in open-access journals and which were not comments or reviews.

We used the PubMed ID of each paper identified in our search to retrieve the matching research outputs using Altmetric Explorer. We used the Altmetric Explorer data to determine the number of news stories that each group of papers generated. We also analyzed the number of tweets that each group of paper generated and the mean number of tweets per paper in each group.

Data extraction from PubMed

Below are the 2 strings we built to extract the data:

String to retrieve papers published in 2018 in the declarative group:

(“mice”[All Fields] AND “alzheimer disease”[MeSH Terms] AND 2018:2018[PDAT] AND “English”[Language] AND “journal article”[Publication Type] AND “loattrfree full text”[Filter]) NOT (“review”[Publication Type] OR “systematic review”[Publication Type] OR “patient”[All Fields] OR “patients”[All Fields]) AND (“mice”[Title] OR “mouse”[Title] OR “rodent”[Title] OR “murine”[Title] OR “animal”[Title])

A similar string was used to retrieve papers published in 2019. Merging the results obtained with each query and removing overlaps (in some cases, PubMed retrieved the same paper twice in the 2018 and 2019 search results), we ended up with a sample of 405 papers. However, for our analysis, we only considered papers that were tracked by Altmetric Explorer. Thus, our final number of declarative papers was 382 (Fig 1). To be included in the declarative group, a paper had to have one of the following words in its title: mice, mouse, rodent, murine, or animal.

String to retrieve papers published in 2018 in the nondeclarative group:

(“mice”[All Fields] AND “alzheimer disease”[MeSH Terms] AND 2018:2018[PDAT] AND “English”[Language] AND “journal article”[Publication Type] AND “loattrfree full text”[Filter]) NOT (“review”[Publication Type] OR “systematic review”[Publication Type] OR “patient”[All Fields] OR “patients”[All Fields]) NOT (“mice”[Title] OR “mouse”[Title] OR “rodent”[Title] OR “murine”[Title] OR “animal”[Title])

A similar string was used to retrieve papers published in 2019. This query retrieved 201 papers published in 2018 and 194 in 2019. However, we wanted our group of nondeclarative papers to be limited to papers that used mice only. If a second species of rodent was used in the study, we kept the paper in the group (these were very few papers). Papers that used both mice and humans (ex vivo, patients’ samples, or human cells for culture) were removed. Studies done entirely in silico were also removed. Studies using genetically modified mice carrying human genes were kept. This screening was done by one of the authors only, MT. Our final sample of papers published in 2018 was 108, and, of papers published in 2019, was 117. After removing overlaps, we obtained a sample of 218 nondeclarative papers. Finally, the number of papers tracked by Altmetric Explorer was 212 (Fig 1).

A table with all tracked references in each group is available as Supporting information (S1 and S2 Tables).

Statistical analysis

We applied chi-squared test at a p < 0.01 to investigate whether the differences observed between groups could be considered significant.

List of declarative papers (N = 405).

(PDF)

Click here for additional data file.

List of nondeclarative papers (N = 218).

(PDF)

Click here for additional data file.

List of journals and their guidelines for papers’ titles (N = 156).

(PDF)

Click here for additional data file.

10 Sep 2020

Dear Dr Triunfol,

Thank you for submitting your manuscript entitled "What’s not in the Title? The Mice Used in the Study." for consideration as a Short Report by PLOS Biology.

Your manuscript has now been evaluated by the PLOS Biology editorial staff as well as by an academic editor with relevant expertise and I am writing to let you know that we would like to send your submission out for external peer review. However, we would like to consider your manuscript as a Meta-Research Article, rather than as a Short Report. We do think that given that the article is about reporting science, it would fit better as that type of article. Please select Meta-Research Article from the type of article menu when you are ready to complete your submission (see below).

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Kind regards,

Ines

--

Ines Alvarez-Garcia, PhD

Senior Editor

PLOS Biology

ialvarez-garcia@plos.org

31 Oct 2020

Dear Dr Triunfol,

Thank you very much for submitting your manuscript "What’s not in the Title? The Mice Used in the Study." for consideration as a Meta-Research Article at PLOS Biology. Thank you also for your patience as we completed our editorial process, and please accept my apologies for the delay in providing you with our decision. Your manuscript has been evaluated by the PLOS Biology editors, an Academic Editor with relevant expertise, and by two independent reviewers.

As you will see, both reviewers find the conclusions of the study interesting and think it is worth pursuing the manuscript for publication, however they also raise several issues that need to be addressed. The main concern is that it is not clear what is actually measured in the study and that this is crucial to be able to draw solid conclusions. In addition, Reviewer 1 thinks you don’t test the quality of the reporting in the articles beyond the title or explore other factors that might influence it – like journal guidelines, for example. After discussing the reviews with the academic editor, we agree that all the comments should be addressed and that the clarifications about the methods are essential. We also think that conclusions need to be more focused on the actual findings and their limitations, and avoid speculation.

In light of the reviews (attached below), we will not be able to accept the current version of the manuscript, but we would welcome re-submission of a much-revised version that takes into account the reviewers' comments. We cannot make any decision about publication until we have seen the revised manuscript and your response to the reviewers' comments. Your revised manuscript is also likely to be sent for further evaluation by the reviewers.

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Thank you again for your submission to our journal. We hope that our editorial process has been constructive thus far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Ines

--

Ines Alvarez-Garcia, PhD,

Senior Editor,

ialvarez-garcia@plos.org,

PLOS Biology

------------------------------------------------------

Reviewers’ comments

Rev. 1: Kieron Rooney – this reviewer has waived anonymity

The general premise of this article is that the media reporting of studies is misleading / sensationalised on the basis of titles of either studies and/or subsequent news outlet reports not specifying animal species (mice specifically in this case report).

A combined PUBMED and altmetric search for articles specific to mouse models of Alzheimer Disease in one year (2018) was then utilised to test the influence of declaring species (or not) on title in a paper subsequently impacting the reporting in lay media outlets.

Upon finding some significant interactions between the study title influencing reporting in lay media and twitter reporting, the discussion focusses on building a platform for change in regulation of study titles - predominantly through revision of ARRIVE guidelines. The platform built infers (particularly on page 6, lines 65 - page 7, lines 85 AND page 5 lines 18 - page 6, lines 30) that there is some intention in omitting species from title by researchers.

My major concern with this manuscript, is that the discussion is a large over reach for the methods and data presented and arguably the authors could be accused of the same intention to sensationalise their outcomes that the AD community of 2018 are accused of.

At best, this is a thought provoking prod at the quality of titles used in a small subset of studies in a niche area of animal models. The data is no doubt interesting but is more hypothesis generating than testing. For example, the assumption is that the title is all that is important, and fair enough, the authors provide a reference to suggest the title is all that some people read. However, there was no attempt by the authors to further test the quality of media reporting by actually reading and providing an analysis of the content of the article. The bigger question to ask here, in testing the need for better regulation on titles in studies is whether or not the totality of reporting is omitting the use of animals. Many readers of lay articles could feasibly be hooked by the title, find very quickly that the article is reporting a study in animals and either read on or not. In the way that the current manuscript is presented I find the analysis having stopped solely at title a significant flaw in the novelty and significance of the manuscript. That is to say, I had not been convinced by the authors of this manuscript that the title, independent of a complete article is a significant issue to be concerned about.

Given the small number of studies identified, this manuscript could have been significantly enhanced by merely emailing the authors of the identified articles and asking them why they omitted or declared the animal species. Whether or not all replied is not an issue, but atleast some more considered primary data could have been used to support or refute the speculation provided in the current discussion.

There is also no consideration on the "why" a primary study gets reported in the media, and this is an important question to ask given the authors make inferences that animal species is omitted to gain more hits and attention. By raising this point, the authors identify a significant limitation - there is no consideration of why or how a specific primary study reaches lay media. Knowing this is important information given that certain institutions and authors are likely to predominate lay media on the basis of reputation and output, and as such a common culture could be influencing the study data here, beyond the limited considerations (such as spin) presented here.

Further, there was no consideration in the discussion provided to the contradictory result in which lay media declared animal species (n=38) despite originating from non-declared studies. Ignoring this outcome is akin to selective reporting. The authors need to be careful of accusing researchers of a malpractice if their approach itself can be questioned. For my read, the presence of this contradictory result (to the authors premise) is an important one to explore and provides evidence that there is more in the translation of a research paper title to the lay media title that needs to be explored. What is the role of the journalist here? Why did some include the animal species when the original study did not? I am not suggesting that the authors have to explore this point as a dataset to present, but there does need to be more adequate representation / discussion of this result in the discussion.

Finally, there is little if any recognition of what / who determines the title of their paper. That is disappointing given that is the cornerstone on which this work has been completed. We are given, as readers some speculation of spin and intentional deception by authors to gain more significance for their work, but for the most part, title content is determined at the journal level. Authors are provided a word or character limit, some journals will specify species identification is necessary. The authors of this manuscript could have value added to this work by reviewing the author guidelines of the journals included in their analysis to present an interesting discussion regarding whether or not, the title of published papers was adequately peer reviewed against journal requirements, or if journals themselves are the better target for regulation. Currently the authors conclude that an outcome of this work is revision of the ARRIVE guidelines to include a specification of species in title. However in the most recent ARRIVE 2.0 guideline, "title" is not identified as an item for review having been deleted from the original 2010 ARRIVE guidelines. A stronger argument could be built with a more considered investigation of the accuracy of reporting by the studies in this manuscript against the journal author guidelines.

Otherwise, the article was an interesting exploration that could inspire more investigation and as such could be an important contribution to the global debate on accurate reporting of animal use in research. The authors may want to consider some of the points raised above however, either in preparation for final acceptance or in the design of a follow-up study.

Editorial correction:

One typo (well done), Discussion, Page 5, line 97 "exits" I believe should be "exists"

Rev. 2: Quinn Grundy – this reviewer has waived anonymity

The authors conduct a meta-research study to examining reporting practices in research for Alzheimer's Disease conducted in mice models. Specifically, they examine whether the mouse model is specified in the title and whether this reporting is consistent between published papers and news reports on the study. The study relies on a convenience sample of open access papers published during 2018.

This is an interesting study and highlights important issues for science communication. I think the paper could be strengthened if these implications for science communication more generally were identified at the outset (ie the consequences of this specific type of 'spin'). The paper also needs some revisions in terms of reporting and particularly, the outcome reporting.

Major comments:

In stating the research question, throughout the paper, including in the Abstract, Author Summary and Introduction, it is not completely clear what the authors actually measured. Although the authors state they measure an association, the outcome is unclear and seems to suggest they measured concordance/discordance. Simply stating the researchers investigated "whether a relationship exists" is vague; as the papers and news articles report on the same study, of course they are related. At the end of the introduction the authors state, "Our main interest was in determining whether the news headlines and the research papers' titles they refer to follow the same pattern regarding the omission, or not, of mice." This should be reflected throughout the paper and might better be described as consistency or concordance in reporting. Similarly, when reporting the findings, be consistent with your language and describe this as concordant reporting or consistent reporting rather than "media perception" (line 105), which is something entirely different.

I found the Results section difficult to follow. It was often difficult to understand what exactly was measured. Often I didn't understand the distinction between one group of results and the next as it was difficult to ascertain what was being compared. I think it would help to consistently report denominators and proportions alongside numerators and to re-organize the section so that results for the full sample are clearly reported, followed by sub-group analyses (I couldn't quite tell if this occurred), sensitivity analyses (excluding titles copied verbatim), and then secondary outcome (tweets). For example, I couldn't tell what the findings on line 150-151 referred to ("Of the 853 total news pieces generated from research papers in both groups, only 229 (26.8%) were declarative, while 624 (73.2%) omitted this fact from their headlines."

The Materials and Methods section could be strengthened. I would suggest the use of sub-headings including: Study design; Research questions and hypotheses; Data extraction; and Statistical Analysis. Key aspects that are missing are description of the outcome measures. This is a weakness throughout the paper and should be very clearly stated in the Methods, with corresponding analyses detailed. Further details re: who did the screening and whether it was done in duplicate would be useful. A Prisma-type flow diagram would be very useful to summarize the sampling and reasons for exclusion.

Specific comments:

Introduction, first sentence: Not just scientists are concerned and in fact, scientists sometimes the source of hype/spin

By line 90-91 on page 2, I came to understand your point about the appropriateness of mouse models for understanding Alzheimer's disease, however, this understanding would have been more helpful to have up around line 52-53. I would suggest stating this main point (ie Alzheimer's Disease is a human condition; scientists have created mouse models to attempt to study the disease; but, animal models have poor predictive value) following the research aim/question and then, walking the reader through the explanations. I am not a biologist, so the explanations were most helpful.

The sentences in the abstract, author summary and the introduction are sometimes quite long and could be broken up for readability (e.g. first sentence of the Introduction, lines 105-109).

On line 94, what is the significance of the clause "what the studies' authors consider to be AD" - could you explain?

Please avoid all non-standard acronyms including AD, non-GM - please spell out.

Your data availability statement suggests the data are proprietary/copyrighted, but the Methods on 98-100 suggest this platform is open access. Can you explain further how these data were accessed and if public, why the raw data cannot be made public? Further, if they are news headlines, are these data already in the public domain?

Could you avoid using NONDECLAPAPERS and DECLAPAPERS and simply describe the groups as you did in the Introduction? Or come up with more reader-friendly terminology?

You report "a declarative title does not impact media interest in the study." To avoid the suggestion of causality or directionality, please simply state that there was no difference between the groups.

This sentence strikes me as belonging in the Discussion "This finding indicates that when authors openly acknowledge the use of mice, or equivalent qualifying term, in the title of their research article, writers follow the same pattern when crafting the headlines for their news stories."

The Discussion feels a bit untethered from the study's findings at several points. I would suggest re-organizing to clearly summarize the study's key findings. Then, place each finding in the context of the wider literature in each paragraph. The discussion on the appropriateness of animal models for Alzheimer's research is interesting, however, doesn't really reflect the study's findings, so could perhaps be mentioned more succinctly. The literature on spin and the recommendations regarding reporting guidelines seem more relevant, but should be linked to specific findings.

A limitation is that this is a convenience sample, however, I wonder if open access articles are more likely to be picked up by journalists? Is there any evidence for this?

The Figures are engaging, but particularly in Figure 2, I can't understand what the final row of News articles refers to.

3 Feb 2021

Submitted filename: Point-by-pont.pdf

Click here for additional data file.

23 Mar 2021

Dear Dr Triunfol,

Thank you for submitting your revised Meta-Research Article entitled "What’s not in the Title? The Mice Used to Study Alzheimer's Disease" for publication in PLOS Biology. I have now obtained advice from the two original reviewers and have discussed their comments with the Academic Editor.

The reviews are attached below. You will see that both reviewers think that the manuscript is very much improved, but they also raise a few minor points that need to be addressed. Among them, they would like you to streamline the discussion and the text in general, to make it less redundant in some parts and to improve the flow. Please note that we don't include Authors Summaries in the articles anymore, so please remove it from the manuscript. In addition, we would like to make a suggestion for the title as following:

“#InMice: strong association between omission of animal model information in the title of Alzheimer Disease articles and it absence in the related news headlines”

Based on the reviews, we will probably accept this manuscript for publication, provided you satisfactorily address the remaining points raised by the reviewers. Please also make sure to address the following data and other policy-related requests.

As you address these items, please take this last chance to 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 cover letter that accompanies your revised manuscript.

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Please do not hesitate to contact me should you have any questions.

Sincerely,

Ines

--

Ines Alvarez-Garcia, PhD,

Senior Editor,

PLOS Biology

ialvarez-garcia@plos.org

----------------------------------------------

Reviewers’ comments

Rev. 1:

The authors have performed a great amount of work to address the comments raised by myself and the other reviewers. This is highly commendable. I do hope that in keeping with their platform for improved transparency that they adopt the PLOS option to publish the peer review history.

I do still have some minor issues, but I do not believe that these should prevent publication. I hope however that the authors consider in their own reflections that for my read, this paper has still not explained the why the outcome observed occurs. During the review process the authors have preferred not to interrogate further the question they raise themselves in the introduction "However, it is not known what prompts writers of news stories to either omit or knowledge (sic), in the story's headlines" This "why" this present paper raises is a more interesting question to me than the analysis presented, which I still think is more a prod than a comprehensive examination. To this end I would suggest that the authors reflect on the comment here that merely increasing the sample size as was identified in response to my query does not answer the "why does something happen", it simply increases the sample size for the "what happened". However I am content that the "why" is more a future question to ask from this work now and not a priority for the current manuscript as the major issues I had with the overreaching and speculation has been significantly dampened. In dampening the speculation, the need for a stronger mechanism / why something has happened has been reduced and this more comprehensive analysis of the outcome reported is more acceptable.

There are a few minor editorial / typographical errors that stood out and I have listed some below, but in general the new discussion, while more circumspect would benefit from another editorial read over, as there are some very long sentences, separated by commas, that make it somewhat difficult to read, in places.

Line 23: Should "knowledge" be "acknowledge"

Line 106: As for Line 23

Line 294: Should "though" be "through"

Line 304: SHould "that" be "than" (this does occur elsewhere in a few places and the authors should confirm / check throughout)

Line 364: Should "constrain" be "Constraint"

Lines 437 - 441: (principally line 438) it is not just that the ARRIVE 2.0 "still does not identify the title of a paper as an important place to acknowledge the species, or strain, used in the study" The ARRIVE 2.0 don't even stipulate the title as an element to review!

Rev. 2:

Thank you for the opportunity to re-review this manuscript. The additional analyses are interesting and I think address some of the questions about the validity of the associations measured. The paper is improved, however, I still had difficulties with the reporting clarity and think that in many places, less may be more, and suggest some cutting (particularly in the Discussion).

Abstract - I would suggest reordering the first sentences so that the @justinmice sentence comes first as a 'hook' and introduces the paper's main focus - accurate science reporting; then to introduce the content on Alzheimer's disease as essentially the case study you are using to study this (akin to the way you have ordered the Author Summary).

In the Author Summary, perhaps delete "solid" from "solid data" (let the reader judge this) and reword to avoid suggesting causality/directionality (ie state, "science reporting is associated with media reporting").

In the Introduction, I actually liked the ordering the authors had in the earlier version - a paragraph introducing the main focus (scrutiny of science reporting) and I love the 'hook' with @justinmice. Perhaps you can keep the original first paragraph, then introduce the material on Alzheimer's disease and explain explicitly, why this provides such a good case study for studying the phenomenon of omission of the animal model in titles.

It seems the paragraphs beginning line 116 ("This sample) belongs at the beginning of the Results (or could be omitted) and then the section "Our findings" (line 124) in the Discussion or omitted. I would suggest ending the Introduction on line 115.

Results:

The results needs a first paragraph that explains how you arrived at this sample and the two comparison groups. Again, in meta-research papers, a flow digram is often the most expedient way to communicate this, especially to clearly show how many scientific papers in each group resulted in news pieces (with accompanying 'n's). Could you revise Figure 1 to include all aspects of the sampling process including the sampling frame, how many papers were excluded and reasons why.

I had previously raised this, but particularly for descriptive data, including proportions (%) would be meaningful; every proportion should be accompanied by the numerator and denominator so it is really clear to which group or sub-sample you are referring to. It is otherwise very hard to follow. And when providing comparisons, please provide the proportion for each group, e.g "We did find that nondeclarative papers generated significantly more news proportionally (31%) than the papers in the declarative group (X%) (p = 0.012)."

In Figure 1, what is the significant of the last row of "News" - what are the two groups?

For each aspect of the analysis, it would be helpful to have a sub-heading to guide the reader. e.g. to introduce the section beginning "News stories posted online often reproduce the original title of the research paper [15]. . "

Line 239, "constraint" typo; and "mentioning mice or not" and line 240 "limitations"

Discussion:

The Discussion is quite repetitive - I would try to cut it substantially so that the key study findings are highlighted and then briefly placed in the context of the literature. I think with some serious editing, it could be cut by a 1/3 or more and not lose anything.

The first sentence of the discussion 249 is very hard to read; please reword, or just delete. The second sentence makes sense and nicely sums up the main finding.

This sentence seems contradictory: "Interestingly, the The PLoS guidelines on How to Write a Great Title suggests authors to include the organism used in the research, even though none of the PLoS journals asks authors to add the study's organism to the article's title [18]."

Line 311- reword, I am not sure that "overclaims" is a word - perhaps "over-interprets"?

You mention "One example is the guidelines created for The Age, The Sydney Morning Herald, Brisbane Times and WAtoday, in Australia." What do these guidelines actually entail?

The material on 340 reporting post-hoc sub-group analysis should be in the Results and the Discussion of these results separated out.

The material beginning on line 370 is quite speculative and does not really add much. I would suggest deleting this paragraph.

The paragraphs beginning line 397 and 406 should be combined.

13 Apr 2021

Submitted filename: Point-to-point.pdf

Click here for additional data file.

5 May 2021

Dear Dr Triunfol,

On behalf of my colleagues and the Academic Editor, Lisa Bero, I am pleased to say that we can in principle offer to publish your Meta-Research Article entitled "What's not in the news headlines or titles of Alzheimer’s disease articles? #InMice" in PLOS Biology, provided you address any remaining formatting and reporting issues. These will be detailed in an email that will follow this letter and that you will usually receive within 2-3 business days, during which time no action is required from you. Please note that we will not be able to formally accept your manuscript and schedule it for publication until you have made the required changes.

Please take a minute to log into Editorial Manager at http://www.editorialmanager.com/pbiology/, click the "Update My Information" link at the top of the page, and update your user information to ensure an efficient production process.

PRESS

We frequently collaborate with press offices. If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximise its impact. If the press office is planning to promote your findings, we would be grateful if they could coordinate with biologypress@plos.org. If you have not yet opted out of the early version process, we ask that you notify us immediately of any press plans so that we may do so on your behalf.

We also ask that you take this opportunity to read our Embargo Policy regarding the discussion, promotion and media coverage of work that is yet to be published by PLOS. As your manuscript is not yet published, it is bound by the conditions of our Embargo Policy. Please be aware that this policy is in place both to ensure that any press coverage of your article is fully substantiated and to provide a direct link between such coverage and the published work. For full details of our Embargo Policy, please visit http://www.plos.org/about/media-inquiries/embargo-policy/.

Thank you again for supporting Open Access publishing. We look forward to publishing your paper in PLOS Biology.

Sincerely,

Ines

--

Ines Alvarez-Garcia, PhD

Senior Editor

PLOS Biology