Empathy and its associations with age and sociodemographic characteristics in a large UK population sample

Andrew Sommerlad; Jonathan Huntley; Gill Livingston; Katherine P. Rankin; Daisy Fancourt

doi:10.1371/journal.pone.0257557

Peer Review History

Original SubmissionMay 4, 2021
14 Jun 2021 Decision Letter - Marcel Pikhart, Editor PONE-D-21-14791 Empathy and its associations with age and sociodemographic characteristics in a large UK population sample PLOS ONE Dear Authors, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by 10 July 2021. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Marcel Pikhart Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For more information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially sensitive information, data are owned by a third-party organization, etc.) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: No ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: No ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: No ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: In my opinion, authors clearly stated the research questions, sufficiently explained the statistical methods used and relevant results. Reviewer #2: It seems to me an interesting and little explored topic, as the authors say, however I have some comments in relation to the manuscript: Introduction On line 61 it says: “Identifying the links between empathy and static characteristics such as gender and ethnicity or dynamic factors such as aging, education, employment or social behaviors, including marriage and social contact, has the potential to improve our understanding of what determines empathy and how it changes during the course of life ”. The claim is without a citation. Methodology In the methodology it was mentioned that the study is longitudinal, although a cross-sectional analysis was made for the paper. It is important to go into more detail about how the sample was selected and present it in the flow chart. Furthermore, it is worth saying why, if the data are longitudinal, a cross-sectional analysis was chosen. In methodology include: Variables are described using means (standard deviation [SD]) for continuous variables and frequencies and percentages for categorical variables, for example. Although the data is said to come from the COVID-19 Social Study and the link is presented for more information about it, it is necessary for the methodology to clarify the central objective of the general study. It seems appropriate to explain how people were surveyed. Is it representative of the entire population 18 years of age or older? (although something is said in the limitations, but not in the methodology). Are the scales used to measure EC and PT previously validated in the study population? Did they use cognitive impairment as an exclusion criterion? Can this be considered a bias of the study? Reviewer #3: The analysis is not advanced, and deals with a deep topic shallowly The researcher(s) should refer to modern theories about empathy Demographic factors are insufficient to describe a social psychology phenomenon ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: Yes:** Marcela Agudelo-Botero Reviewer #3: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0257557.r001
Revision 1
9 Aug 2021 Author Response Thank you for the comments of editors and reviewers. We have addressed these point by point below with our response in bold font and revised sections of the manuscript in italics. Editors comments 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf We have amended the manuscript to meet PLOS ONE’s style requirements and naming conventions. 2. We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For more information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions . In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially sensitive information, data are owned by a third-party organization, etc.) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. We have amended the data availability statement in the manuscript as below. Funding restrictions currently do not permit open publication of the data but they can be accessed via contact with the authors and will be made publicly available early next year. Our recent paper published in PLOS One had similar data restrictions (https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0248919). The data files supporting the findings of this study are available on request from the study data access committee through data sharing agreement via f.bu@ucl.ac.uk. The full data is not currently publicly available due to funding arrangements but will be made publicly available following completion of the COVID-19 Social Study at the start of 2022. We have explained the limitations on data availability in our cover letter. Reviewer #1 In my opinion, authors clearly stated the research questions, sufficiently explained the statistical methods used and relevant results. Thank you for your review of our paper and we are pleased that you thought that the study was clear and appropriately conducted. Reviewer #2 It seems to me an interesting and little explored topic, as the authors say, however I have some comments in relation to the manuscript: Thank you very much for your review and helpful comments which we think have improved our manuscript. Introduction On line 61 it says: “Identifying the links between empathy and static characteristics such as gender and ethnicity or dynamic factors such as aging, education, employment or social behaviors, including marriage and social contact, has the potential to improve our understanding of what determines empathy and how it changes during the course of life ”. The claim is without a citation. We have added citations to support this statement regarding empathy as a potentially learned social behaviour or determined by aging (p4, lines 62-65): Identifying the links between empathy and static characteristics such as gender and ethnicity or dynamic factors such as aging, education, employment, or social behaviours including marriage and social contact, has the potential to elucidate the determinants of empathy, such as learning through social interaction (1), and how empathy changes during the life-course (2). Methodology In the methodology it was mentioned that the study is longitudinal, although a cross-sectional analysis was made for the paper. It is important to go into more detail about how the sample was selected and present it in the flow chart. Furthermore, it is worth saying why, if the data are longitudinal, a cross-sectional analysis was chosen. Thank you for highlighting this. The COVID-19 Social study is a longitudinal study, with weekly surveys from March 2020.However, the IRI empathy questions on which we base our analysis were included at one time point of the study and so our presented analysis is cross-sectional. We have clarified this in the methods section (p7, lines 126-127): As the questions about empathy were included during only one of the weekly study questionnaires, our analysis was cross-sectional. We have also added a supplementary figure describing participant flow: S1 Figure. Flow of participants. Notes: Empathy questions were included in the study during week 13-20th June 2020 In methodology include: Variables are described using means (standard deviation [SD]) for continuous variables and frequencies and percentages for categorical variables, for example. We have added this to added this to the analysis section of the manuscript (p9, line 177-179): Variables are described using means and standard deviations (SD) for continuous variables and frequencies and percentages for categorical variables. Although the data is said to come from the COVID-19 Social Study and the link is presented for more information about it, it is necessary for the methodology to clarify the central objective of the general study. We have explained the overall aims of the main study (p6, lines 113-115): The COVID-19 Social Study started on 21st March 2020 to consider the psychological and social effects of the COVID-19 pandemic and the resulting restrictions on adults in the UK. It seems appropriate to explain how people were surveyed. Is it representative of the entire population 18 years of age or older? (although something is said in the limitations, but not in the methodology). Thank you, we have added detail about the approach to recruitment for this study (p6, lines 115-123): Although the sample was not random, its large sample, which is well-stratified to include differing groups and well-phenotyped, make it a suitable dataset for exploring broader psychological and social factors beyond the pandemic itself. The study was promoted through three primary routes to encourage participation from diverse and under-represented groups. Firstly, convenience sampling including promotion through existing mailing lists and networks including large databases of UK adults who had consented to contact about research; secondly we conducted targeted recruitment of individuals from low-income backgrounds, with no or few educational qualifications, or unemployed via partnership with recruitment firms; and thirdly we promoted the study to vulnerable groups including older people and those with mental illness through third sector organisations. Are the scales used to measure EC and PT previously validated in the study population? The scale has not been specifically validated in this study population – a novel contribution of our study is that this is the first large-scale use of the Interpersonal Reactivity Index in the UK. However, the IRI has well-established psychometric properties from population-based studies in several countries and we have summarised this information in the manuscript (p8, lines 147-152): The IRI has good psychometric properties and has been validated in several large population studies (3). The scales have high internal reliability and test-retest reliability (3). Internal consistency for these subscales, measured by Cronbach’s alpha, have been reported to be between 0.70 and 0.78 (4, 5). Cronbach’s alpha in our sample was 0.80 for the EC subscale and 0.81 for the PT scale. Construct validity is demonstrated by the correlation of the PT subscale with measures of cognitive empathy, and the EC scale with emotional empathy measures (6). Did they use cognitive impairment as an exclusion criterion? Can this be considered a bias of the study? We did not obtain data on the general cognition of study participants so were not able to use cognitive impairment as an exclusion criterion. Our approach recruitment and the online self-completion of questionnaires makes it unlikely that we had many participants with substantial cognitive impairment. However, we have added that there is the potential for measurement error through the inclusion of people with cognitive impairment (p24, lines 407-409): Finally, we did not have data on participants’ general cognition and, although our study procedures means it is unlikely that participants had substantial cognitive impairment, it is possible that cognitive impairment in some participants would cause measurement error. Reviewer #3 The analysis is not advanced, and deals with a deep topic shallowly. The researcher(s) should refer to modern theories about empathy We have added to our manuscript to place our study more clearly within modern theories about empathy. In the introduction, we have clarified the value of considering socio-demographic determinants of empathy (p4, lines 62-65) as markers of social learning: Identifying the links between empathy and static characteristics such as gender and ethnicity or dynamic factors such as aging, education, employment, or social behaviours including marriage and social contact, has the potential to elucidate the determinants of empathy, such as learning through social interaction (1), and how empathy changes during the life-course (2). We have added to our discussion in several places to place our research in the context of the extant literature. p20, lines 301-304: We expected that perspective taking would reduce with greater age, but that empathic concern may not. This hypothesis was due to the cognitive requirements of taking another person’s perspective, which is reflected in evolutionary models of empathy whereby perspective taking is a higher-level process than experiencing empathic concern, and thus more susceptible to loss through cognitive dysfunction (7). p21, lines 342-349: There are several potential explanations of woman having higher empathy than men. Firstly, there may be culturally-driven differences in socialisation behaviour by gender (8) through social learning (1). Secondly, differences may be explained through biological mechanisms, such as hormone-induced alterations in brain development through lower testosterone levels (9) or differential response to oxytocin (10), with genetic selection favouring more empathic women. Finally, social desirability bias may account for gender differences in self-reported empathy, supported by discrepancies in self-reported and task-based assessment of empathy where women over-reported their own empathy (11). P22, lines 367-369: Some previous research suggests that empathy improves during healthcare training (12), consistent with the Learned Matching hypothesis, whereby empathy emerges and strengthens during development through domain-general processes of associative learning (1). Demographic factors are insufficient to describe a social psychology phenomenon We agree that socio-demographic factors cannot fully explain complex social psychological phenomena and our study was not designed to perform a thorough investigation of how these demographic characteristics may interact with empathy. Instead, our aim was to perform an initial step of that investigation, by identifying large-scale epidemiological evidence of associations. Our study contributes to the understanding of how empathy may change during the life-course and how it differs according to socio-demographic characteristics, such as our novel finding of the gender difference in the associations of empathic concern and perspective taking by age. We therefore build upon previous research through the large UK based sample, our wide range of examined characteristics, and our consideration of potential confounders. Even though investigating detailed mechanisms of relationships between social factors and empathy was beyond the scope of this paper, this is an excellent suggestion for future lines of research and we have added that suggestion to the conclusion of our manuscript (p25, lines 434-442): Future research should seek to clarify the mechanisms for the associations we have identified in our epidemiological analysis through further detailed examination of relevant factors. In particular, it is important to understand whether the decline in perspective taking is general or specific to those who will go on to develop cognitive impairment, and which biological and psycho-social mechanisms drive gender differences in age-related empathy changes. Self-reported empathy is higher in people working in caring professions independent of personality and educational level and, considering the key importance of this domain in guiding social behaviour and protecting against adverse mental health outcomes, future studies should determine the extent to which this can be modified or is an inherent trait which should be sought for these roles. References 1. Heyes C. Empathy is not in our genes. Neuroscience & Biobehavioral Reviews. 2018;95:499-507. 2. Beadle JN, De la Vega CE. Impact of aging on empathy: Review of psychological and neural mechanisms. Frontiers in psychiatry. 2019;10:331. 3. Konrath S. A critical analysis of the Interpersonal Reactivity Index. MedEdPORTAL Directory and Repository of Educational Assessment Measures (DREAM). 2013. 4. Davis MH. A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology. 1980;10:85. 5. Hemmerdinger JM, Stoddart SD, Lilford RJ. A systematic review of tests of empathy in medicine. BMC medical education. 2007;7(1):24. 6. Davis MH. Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of personality and social psychology. 1983;44(1):113. 7. De Waal FB, Preston SD. Mammalian empathy: behavioural manifestations and neural basis. Nature Reviews Neuroscience. 2017;18(8):498-509. 8. Strayer J, Roberts W. Children's anger, emotional expressiveness, and empathy: Relations with parents’ empathy, emotional expressiveness, and parenting practices. Social development. 2004;13(2):229-54. 9. Van Honk J, Schutter DJ, Bos PA, Kruijt A-W, Lentjes EG, Baron-Cohen S. Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proceedings of the National Academy of Sciences. 2011;108(8):3448-52. 10. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves “mind-reading” in humans. Biological psychiatry. 2007;61(6):731-3. 11. Baez S, Flichtentrei D, Prats M, Mastandueno R, García AM, Cetkovich M, et al. Men, women… who cares? A population-based study on sex differences and gender roles in empathy and moral cognition. PloS one. 2017;12(6):e0179336. 12. Cunico L, Sartori R, Marognolli O, Meneghini AM. Developing empathy in nursing students: a cohort longitudinal study. Journal of clinical nursing. 2012;21(13-14):2016-25. Attachments Attachment Submitted filename: Sommerlad July 2021 - Response to reviewers.docx https://doi.org/10.1371/journal.pone.0257557.r002
6 Sep 2021 Decision Letter - Marcel Pikhart, Editor Empathy and its associations with age and sociodemographic characteristics in a large UK population sample PONE-D-21-14791R1 Dear Authors, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Marcel Pikhart Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0257557.r003
Formally Accepted
9 Sep 2021 Acceptance Letter - Marcel Pikhart, Editor PONE-D-21-14791R1 Empathy and its associations with age and sociodemographic characteristics in a large UK population sample Dear Dr. Sommerlad: 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. Marcel Pikhart Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0257557.r004

Open letter on the publication of peer review reports

PLOS recognizes the benefits of transparency in the peer review process. Therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. Reviewers remain anonymous, unless they choose to reveal their names.

We encourage other journals to join us in this initiative. We hope that our action inspires the community, including researchers, research funders, and research institutions, to recognize the benefits of published peer review reports for all parts of the research system.

Learn more at ASAPbio .