Changes in HIV incidence during the COVID-19 pandemic (2020–22) compared with the pre-pandemic period (2015–19) in Peru: An observational study

Max Carlos Ramírez-Soto; Hugo Arroyo-Hernández

doi:10.1371/journal.pone.0324784

Peer Review History

Original SubmissionFebruary 13, 2025
13 Feb 2025 Author Response https://doi.org/10.1371/journal.pone.0324784.r001
10 Apr 2025 Decision Letter - Oriana Rivera-Lozada de Bonilla, Editor PONE-D-25-07972Changes in HIV incidence during the COVID-19 pandemic compared with pre-pandemic Peru: an observational studyPLOS ONE Dear Dr. Ramírez-Soto, 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. I strongly suggest that the authors seek assistance with the revision of the English writing. While the overall content is clear, certain sections would beneBit from improved language Blow and grammar to ensure clarity and ease of reading fora broader audience. The background of the study could be expanded. It would be helpful to include more details about the condition being studied, how it is typically diagnosed, and how the COVID-19 pandemic may have affected diagnosis rates. Furthermore, discussing the implications of missed diagnoses during the pandemic would strengthen the background and provide more context for the study. The results section could be discussed in a more systematic and clearer manner. Currently, the presentation of the results feels somewhat fragmented. A more structured approach would enhance the readability and help the readers better understand the Bindings and their implications. Please submit your revised manuscript by May 25 2025 11:59PM. 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: https://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, Oriana Rivera-Lozada de Bonilla Academic Editor PLOS ONE Journal requirements: 1. When submitting your revision, we need you to address these additional requirements. 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 Reviewer comments: 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: Partly Reviewer #2: Partly Reviewer #3: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No Reviewer #2: No Reviewer #3: Yes ****** 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: No ****** 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: 1. Study Design The researchers used a cross-sectional study design but reported incidence rate ratios (IRRs). Recommendation: They should either revise this approach or provide a clear justification for using IRRs in cross-sectional data. 2.Use of Simple Averages and Pooled Incidence Rates as a Baseline The study averages HIV cases from 2015–2019 to establish a pre-pandemic reference and pools incidence rates over these years. This assumes that HIV incidence was stable, which may not be true. HIV cases could have been rising or falling before the pandemic due to policy changes, testing rates, or other factors. Simply averaging or pooling data ignores year-to-year variations. Recommendations: a. Instead of a simple average, the researchers may use time-series methods to estimate the expected trend had the pandemic not occurred. b. The researchers may calculate annual incidence rates (IRs) and test for a linear trend using regression models. This will show if HIV incidence was already changing before COVID-19. 3. Discussion and Future Research The researchers could expand the discussion on the implications of their findings and suggest future research directions. 4. The phrase “By 2022.” on page 2, line 33 needs clarification. Reviewer #2: Many thanks for the opportunity to review this article. I think it is a valuable piece of work as it is very important to well describe what the impact of the non-pharmaceutical interventions was on the health status of the populations in different countries and regions of the world during the Covid 19 pandemic. I feel the paper still needs some significant work before being published. I have provided many comments, questions and suggestions to help the authors improve the article. I hope these help. To me the main limitation, that should be addressed, is that the study is considering the average new infection numbers and IR for the years 2015 to 2019 . Some of the decreases described for 2020 may have started in 2018 or 2019 and could be explained by other factors. We cannot know this if we do not see the trends from 2015 to 2019. To draw strong conclusions, more robust approaches should be used, e.g. time series analyses. I am aware that these analyses are not always possible, and in some occasions a simpler approach can be enough to demonstrate a given hypothesis or to highlight a fact. In any case, I would at least present somewhere yearly trends for 2015 to 2019. And I would also work in all the other aspects that I commented about. Reviewer #3: Thank you for the opportunity to review your manuscript. I appreciate the effort and the valuable insights presented. However, I have a few points I would like to comment on. In addition to the detailed revisions, I would like to highlight three general observations. Please see attachment. ****** 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: Antonio Isidro Carrion Martin 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. Attachments Attachment Submitted filename: PONE-D-25-07972_reviewer_ic.pdf Attachment Submitted filename: Review.pdf https://doi.org/10.1371/journal.pone.0324784.r002
Revision 1
29 Apr 2025 Author Response Response to reviewers Title of the article: Changes in HIV incidence during the COVID-19 pandemic compared with pre-pandemic Peru: an observational study Ms. Ref. No.: PONE-D-25-07972 Dear Editor, Thank you for your comments and those of the reviewers. We believe our manuscript has improved considerably. Reviewer #1 Comment 1. Study Design The researchers used a cross-sectional study design but reported incidence rate ratios (IRRs). Recommendation: They should either revise this approach or provide a clear justification for using IRRs in cross-sectional data. Response 1. Thank you for your comment. This is an observational study using surveillance data from the national health system. Therefore, we have corrected the design only as an observational study of health system surveillance. Comment 2. Use of Simple Averages and Pooled Incidence Rates as a Baseline The study averages HIV cases from 2015–2019 to establish a pre-pandemic reference and pools incidence rates over these years. This assumes that HIV incidence was stable, which may not be true. HIV cases could have been rising or falling before the pandemic due to policy changes, testing rates, or other factors. Simply averaging or pooling data ignores year-to-year variations. Recommendations: a. Instead of a simple average, the researchers may use time-series methods to estimate the expected trend had the pandemic not occurred. b. The researchers may calculate annual incidence rates (IRs) and test for a linear trend using regression models. This will show if HIV incidence was already changing before COVID-19. Response 2. Thank you for your comment. Thank you for your detailed comments, they help us to improve the study. A time series study would require a modeled analysis and other data, which we will consider in a future study. Following your recommendations, we have included trends in overall and regional incidence rates with 95% confidence intervals (see supplementary material, Table S2). These show slight changes in incidence rates that do not affect the study findings. Comment 3. Discussion and Future Research The researchers could expand the discussion on the implications of their findings and suggest future research directions. Response 3. Thank you for your comment. We have included an “Implications for Public Health” paragraph in the Discussion section. Comment 4. The phrase “By 2022.” on page 2, line 33 needs clarification. Response 4. Thank you for your comment. The error has been corrected. Reviewer #2 Many thanks for the opportunity to review this article. I think it is a valuable piece of work as it is very important to well describe what the impact of the non-pharmaceutical interventions was on the health status of the populations in different countries and regions of the world during the Covid 19 pandemic. I feel the paper still needs some significant work before being published. I have provided many comments, questions and suggestions to help the authors improve the article. I hope these help. To me the main limitation, that should be addressed, is that the study is considering the average new infection numbers and IR for the years 2015 to 2019. Some of the decreases described for 2020 may have started in 2018 or 2019 and could be explained by other factors. We cannot know this if we do not see the trends from 2015 to 2019. To draw strong conclusions, more robust approaches should be used, e.g. time series analyses. I am aware that these analyses are not always possible, and in some occasions a simpler approach can be enough to demonstrate a given hypothesis or to highlight a fact. In any case, I would at least present somewhere yearly trends for 2015 to 2019. And I would also work in all the other aspects that I commented about. Response 1. Thank you for your comment. Corregido. Hemos incluido las tendencias en las tasas de incidencia general y por regiones con intervalos de confianza del 95% (ver material suplementario, Table S2). Donde se muestras ligeros cambios en las tasas de incidencia que no afectan los hallazgos del estudio. Introduction Response 2. Thank you for your comment. We have corrected all spelling and grammatical errors in the new version of the manuscript. Methods We have corrected all spelling and grammatical errors in the new version of the manuscript. Comment 2. average number per year? or rather IR? Response 2. Thank you for your comment. The statistical analysis section also describes the calculation of the RI. This value is the number of cases estimated for the pre-pandemic period. The incidence rate is described in other paragraph in the Methods section. Comment 3. how were they calculated? Poisson regression? Response 3. Thank you for your comment. We have included some clarifications about the IRR. Results We have corrected all spelling and grammatical errors in the new version of the manuscript. Comment 1. I would only use one decimal digit (if needed at all), but whatever is chosen, I would be consistent, in the tables some figures have two decimals others only one Response 1. Thank you for your comment. The decimals in tables 2 and 3 have been corrected. We use two decimals. Discussion We have corrected all spelling and grammatical errors in the new version of the manuscript. Comment 1. I have no doubt that this is true, but there has not been any details or dates given for NPI in Peru, perhaps the authors should explain more? e.g. when lock down started, duration, when reduction in HIV clinics started, etc. Response 1. Thank you for your comment. We have included a brief explanation of confinement in Peru. Comment 2. To me the big question would be: was there a decrease in IR because of an actual reduction in transmission, i..e, people decrease sexual, recreational activities, etc (as a consequence of the NPIs) pr was the decrease rather a result on of the decrease in testing (i.e. infections continued to occur but were less likely to be diagnosed). I guess it was a bit of both? In any case I wonder if this IRs higher than the pre pandemic levels could back the hypothesis that IR decrease was a result of lack of testing, so a "surveillance artifact" , i.e. spread continued at similar levels and eventually even higher levels as a consequence of the increase of undiagnosed people.. In any case I feel this is not discussed enough.. Response 2. Thank you for your comment. We have included a brief explanation of the possible transmission of HIV. Comment 3. was there further decrease in testing? did testing start to increase gain in 2021? Response 3. Thank you for your comment. The sentence has been removed to avoid reader confusion. In addition. Paragraph 3 of this section mentions the decline in HIV testing. Comment 4. Not clear what this means, "able to care for several patients"? I guess you mean that your findings suggest a recovery of the health system ... which has also been documented in other studies? or something like that? Response 4. Thank you for your comment. We've corrected the sentence to explain the changes in healthcare in Peru. Comment 5. but proportional reduction was higher in females, right? I think that if you decide to focus on males because they represent a higher % of infections, you should somehow explain this. Response 5. Thank you for your comment. . It has been explained that both sexes were affected, including those at risk. Comment 6. The several factors would apply to overall changes, not only in men, right? To me those factors are the most important part of the discussion, and it is not clear why the focus only on men, i would use these factors to explain overall results and then maybe say something about males? Response 6. Thank you for your comment. It has been explained that both sexes were affected, including those at risk. Comment 7. Include the reference “Fourth, the economic and social disruptions of the pandemic could have altered behavior, including changes in migration patterns or access to healthcare, influencing HIV transmission dynamics”. Response 7. Thank you for your comment. The reference has been included “33. Winwood JJ, Fitzgerald L, Gardiner B, Hannan K, Howard C, Mutch A. Exploring the Social Impacts of the COVID-19 Pandemic on People Living with HIV (PLHIV): A Scoping Review. AIDS Behav. 2021;25(12):4125-4140. doi: 10.1007/s10461-021-03300-1”. Comment 8. “The observed decline in HIV incidence during this period should be interpreted with caution. It is likely that the reduced incidence reflects temporary changes due to the pandemic”. But this is for the overall figures, not only for men, right? Response 8. Thank you for your comment. It has been explained that men and women were affected. Comment 9. I feel there is a disconnection between this section and the precedent phrases, do you need to explain all the results from these papers, could you not just say that the problem of diagnosed infections may be more prounounced in those specific groups, and reference the papers. Response 9. Thank you for your comment. The sentence has been corrected according to your recommendations. Comment 10. “Prior to the pandemic, a study of men who have sex with men and 255 transgender women in the Lima region found that 31% were infected with HIV, of whom 35% had not been previously diagnosed [35]. Another study conducted in the Cajamarca region between 2015 and 2021 estimated that of 1,388 people living with HIV, approximately 393 cases (28.4%) were undiagnosed [36]”. I feel there is a disconnection between this section and the precedent phrases, do you need to explain all the results from these papers, could you not just say that the problem of diagnosed infections may be more prounounced in those specific groups, and reference the papers. Response 10. Thank you for your comment. The paragraph has been rewritten for better understanding of undiagnosed cases. Comment 11. “Another group considered vulnerable”. This feels like is not really related to the paper.. I would introduce this differently, and say that the most pronounced decrease occurred in regions with an important presence of indigenous populations... this could be explained by ... Response 11. Thank you for your comment. We have corrected the sentence according to your recommendations. Comment 12. Are these the same studies as 37 and 38? do they refer only to indigenous population? not clear.. if you are not talking about indigenous anymore, perhaps move into different paragraph? Response 12. Thank you for your comment. The information has been reorganized for better understanding by readers. Comment 13. the actions described were already put in place a while ago, before this paper. Any new public health recommendation from your own results? Response 13. Thank you for your comment. We have included a paragraph with the implications for public health. Comment 14. One of the big limitations of the study is that it considers average numbers and IR for the years 2015 to 2019, some of the decreases described for 2020 may have started in 2018 or 2019 and could be also explained by other factors. To draw strong conclusions more robust approaches should be used, e.g time series analyses. Although at times these analyses are not possible. In any case, I would at least present somewhere yearly trends for 1025 to 2019. Response 14. Thank you for your comment. We have included a brief description of the IR estimates that do not affect the estimates in the limitations section. Comment 15. Conclusiones. I guess you mean the overall reduction in diagnosis could have led... and then you say about deaths, but I do not think these are conclusions from your study? I would remove from conclusions. Response 15. Thank you for your comment. The sentence has been deleted. Reviewer #3 Thank you for the opportunity to review your manuscript. I appreciate the effort and the valuable insights presented. However, I have a few points I would like to comment on. In addition to the detailed revisions, I would like to highlight three general observations: • English Writing Support: I strongly suggest that the authors seek assistance with the revision of the English writing. While the overall content is clear, certain sections would beneBit from improved language Blow and grammar to ensure clarity and ease of reading for a broader audience. • Background of the Study: The background of the study could be expanded. It would be helpful to include more details about the condition being studied, how it is typically diagnosed, and how the COVID-19 pandemic may have affected diagnosis rates. Furthermore, discussing the implications of missed diagnoses during the pandemic would strengthen the background and provide more context for the study. • Clarity and Systematization of Results: The results section could be discussed in a more systematic and clearer manner. Currently, the presentation of the results feels somewhat fragmented. A more structured approach would enhance the readability and help the readers better understand the Bindings and their implications. ABSTRACT Comment 1. LINES 26-29. There are a couple of issues in this sentence that need correction. First, the phrase "from 25 geographically diverse from Peru" is unclear and likely missing a noun after "diverse". A suggested revision is "from 25 geographically diverse regions in Peru". Second, there is a subject-verb agreement error in "HIV incidence during the COVID-19 pandemic years (2020, 2021, and 2022) were compared". Since HIV incidence is singular, the verb should also be singular: "was compared". Please revise accordingly. Response 1. Thank you for your comment. We have corrected the sentence according to your recommendations. Comment 2. LINE 33. The words “By 2022” seem out of place. Response 2. Thank you for your comment. The error has been corrected. Comment 3. LINE 35. Consider removing the “and” before 4% for smoother phrasing. Response 3. Thank you for your comment. The error has been corrected. Comment 4. LINE 36. Age stratified should be age-stratified. Response 4. Thank you for your comment. The error has been corrected. Comment 5. LINE 42. “Was” should be “has” to reflect the appropriate tense. Response 5. Thank you for your comment. The error has been corrected. Comment 6. LINES 44-45 The sentence is grammatically incorrect. It should be: “By 2022, the incidence of HIV infection was higher than in the pre-pandemic period, especially in regions of the Peruvian Amazon." Response 6. Thank you for your comment. We have corrected the sentence according to your recommendations. INTRODUCTION Comment 1. LINE 51. The authors mention non-pharmaceutical interventions but never explain what they are. Although this is not the main focus of the work, I think providing a brief explanation would improve the Blow of the text. Response 1. Thank you for your comment. A description of non-pharmacological interventions has been included. Comment 2. LINE 73. The sentence “In China, a 59% reduction in testing across four regions” is incomplete and lacks a main verb. Consider revising it to something like, “In China, a 59% reduction in testing was observed across four regions.” Response 2. Thank you for your comment. We have corrected the sentence according to your recommendations. Comment 3. LINES 75-76 The phrase "a more than 50% drop" sounds slightly unnatural. A clearer construction would be "more than a 50% drop" or "a drop of more than 50%". Please consider revising for better readability. Response 3. Thank you for your comment. We have corrected the sentence according to your recommendations. Comment 4. LINES 77-78. The authors state that two studies assessed changes in HIV diagnoses in Peru but only present the results from one of them. Consider addressing why the second study's results are not presented or clarify the reasoning behind this. Response 4. Thank you for your comment. The results of another study were included. Comment 5. LINES 84-85. I’m not sure if “changes” is the appropriate term for conveying that undiagnosed HIV cases have implications for treatment initiation. Consider using "delays" or "barriers" instead, if that is the intended meaning. Response 5. Thank you for your comment. We have corrected Attachments Attachment Submitted filename: Response to Reviewer_R1.docx https://doi.org/10.1371/journal.pone.0324784.r003
2 May 2025 Decision Letter - Oriana Rivera-Lozada de Bonilla, Editor Changes in HIV incidence during the COVID-19 pandemic (2020–22) compared with the pre-pandemic period (2015–19) in Peru: an observational study PONE-D-25-07972R1 Dear Dr. Max Carlos Ramírez-Soto, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, 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, Oriana Rivera-Lozada de Bonilla Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0324784.r004
Formally Accepted
Acceptance Letter - Oriana Rivera-Lozada de Bonilla, Editor PONE-D-25-07972R1 PLOS ONE Dear Dr. Ramírez-Soto, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset You will receive further instructions from the production team, including instructions on how to review your proof when it is ready. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few days to review your paper and let you know the next and final steps. Lastly, 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 customercare@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. Oriana Rivera-Lozada de Bonilla Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0324784.r005

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 .