The drivers of West Nile virus human illness in the Chicago, Illinois, USA area: Fine scale dynamic effects of weather, mosquito infection, social, and biological conditions

Surendra Karki; William M. Brown; John Uelmen; Marilyn O’Hara Ruiz; Rebecca Lee Smith

doi:10.1371/journal.pone.0227160

Peer Review History

Original SubmissionDecember 10, 2019
17 Feb 2020 Decision Letter - Nikos T Papadopoulos, Editor PONE-D-19-34216 The drivers of West Nile virus human illness: fine scale dynamic effects of weather, mosquito infection, social, and biological conditions PLOS ONE Dear Dr. Smith, 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. Comments of both reviewers should be addressed. In addition, please elaborate more to render Figure captions self explained by including all respective information. Also, the references list should be checked carefully and editing mistakes should be corrected. For example all scientific names at species and genus level should be given in italics. Last table 5 could be included as supplementary materials. We would appreciate receiving your revised manuscript by Apr 02 2020 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols 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). This letter should be uploaded as separate file and labeled 'Response to Reviewers'. 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If your ethics statement is written in any section besides the Methods, please move it to the Methods section and delete it from any other section. Please also ensure that your ethics statement is included in your manuscript, as the ethics section of your online submission will not be published alongside your manuscript. [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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: I Don't Know ****** 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 ****** 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 ****** 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: Peer review report on PLOS ONE manuscript " The drivers of West Nile virus human illness: fine scale dynamic effects of weather, mosquito infection, social, and biological conditions", (Manuscript number PONE-D-19-34216). Recommendation: Minor Revision Comments to Authors: This manuscript analyzes the available long-term data of mosquito infection rates, West Nile virus human cases and weather variables from 2005 to 2016 combined with landscape and demographic characteristics of two Illinois counties of the Chicago region in order to evaluate relationships between the factors on fine temporal and spatial scale and identify the drivers that potentially affect the presence of human WNV illness and may act as early warning predictors. The paper is well written with a well-organized text, the data were analyzed using multi-level statistical modeling approaches and the findings are sufficiently documented and the results are valuable for a better understanding of the fine-scale drivers of spatiotemporal variability of WNV human case prevalence in an urban environment such as in the study area. Although numerous published studies that have shed light on factors that affect WNV transmission in an area, the knowledge regarding the influence of climatic variables in correlation with the data from the entomological surveillance and the number of WNV human cases, is still limited. For that reason, the paper makes a substantial contribution to the literature and is therefore recommended for publication in PLOS-ONE after minor revision taking into account the following general or specific comments. General comments The study uses and analyzes the 10-year data (2005 to 2014) from Cook and DuPage counties in the Chicago, Illinois region and the accuracy of the predictions of the developed model tested with the data of the same specific area. However, according to the literature, it is well known that models predicting the WNV transmission and human WNV infections do not always have the same accuracy when applied to other areas with different mosquito fauna, weather conditions and/or geomorphological and demographic characteristics. Therefore, we consider that the study area should also be mentioned in the title. Please comment and, if necessary, provide an adequate justification in the manuscript, for the reason that in this work were note included data from passive or active monitoring of WNV presence in birds and equids, which are considered by several authors as important prediction factors of the presence and spread of WNV virus in an area. Specific comments Line 170 of the manuscript: If available, please provide information on the species of Culex mosquitoes that have been tested for WNV presence as the vectorial competence of different species may vary significantly for WNV transmission to humans. Line 179 of the manuscript: Please add a bibliographical reference in the reference section for the MIR estimation tool by Biggerstaff, 2006. Line 188 of the manuscript: Please provide a definition and some additional information about the category of "probable cases of WNV" that were also included in the study along with the "confirmed cases" because the symptoms of infection by the West Nile vary in severity, with the mild forms can be easily confused with flu symptoms and usually go unreported. Lines 578-580 of the manuscript: Please, correct Reference no 39 by adding the name of the journal, volume number and pages numbers. Messina JP, Brown W, Amore G, Kitron UD, Ruiz MO. West Nile Virus in the Greater Chicago Area : A Geographic Examination of Human Illness and Risk from 2002 to 2006. URISA Journal 2011;23: 5-18. Reviewer #2: Dear authors, This is a well written paper that deals with the determination of factors affecting the spatiotemporal variability of WNV cases in humans through identification of the fine scale drivers of WNV transmission in an urban area with a repeated history of WNV outbreaks. The findings are very interesting since they include multi-level modeling of weekly data from over a decade and they extend our knowledge in the correlation of variables related to temperature, precipitation, mosquito infection, land cover, and demographic characteristics with the probability of an area having a WNV case or not. Further down please consider some comments of minor importance that may benefit the manuscript. It seems that the infection status of avian population, as primary reservoirs of WNV, and equids, as dead-end hosts, were not included among the tested variables for modeling structure. Please note that these are critical factors implicated in the WNV transmission in order to develop predictive models. As mentioned in the introduction, public health surveillance for WNV involves collection and testing of dead birds suspected to have died of WNV, testing of sentinel chickens or of wild birds captured for this purpose and reporting of cases of equine illness. Could you please justify this data gap in the model structuring? Is there any surveillance system for infected avian and equids population in the study area? In the “Introduction” you may add any relevant literature data where bird and/or equine infection rate were used for development of models predicting WNV transmission in humans. Also, in lines 440-459 of the manuscript, you could mention the fact that avian and equids infection status was not considered as a factor for prediction of WNV cases in humans in the study area. According to the best multivariable model that was used, the proportion of open water was negatively associated with the probability of WNV cases. Also, as mentioned in the discussion, a negative association of precipitation and WNV cases was observed and this indicates that dry and hot weather conditions would increase the probability of an area being positive for a WNV case. Instead, it is supposed that high rainfall and high percentage of water bodies in an area may favor mosquito population by increasing their breeding sites, and therefore may lead to increased WNV cases in humans. Hence, a positive correlation between precipitation and water bodies with WNV cases in humans is anticipated. Please comment. ****** 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: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0227160.r001
Revision 1
27 Feb 2020 Author Response Reviewer #1: Peer review report on PLOS ONE manuscript " The drivers of West Nile virus human illness: fine scale dynamic effects of weather, mosquito infection, social, and biological conditions", (Manuscript number PONE-D-19-34216). Recommendation: Minor Revision Comments to Authors: This manuscript analyzes the available long-term data of mosquito infection rates, West Nile virus human cases and weather variables from 2005 to 2016 combined with landscape and demographic characteristics of two Illinois counties of the Chicago region in order to evaluate relationships between the factors on fine temporal and spatial scale and identify the drivers that potentially affect the presence of human WNV illness and may act as early warning predictors. The paper is well written with a well-organized text, the data were analyzed using multi-level statistical modeling approaches and the findings are sufficiently documented and the results are valuable for a better understanding of the fine-scale drivers of spatiotemporal variability of WNV human case prevalence in an urban environment such as in the study area. Although numerous published studies that have shed light on factors that affect WNV transmission in an area, the knowledge regarding the influence of climatic variables in correlation with the data from the entomological surveillance and the number of WNV human cases, is still limited. For that reason, the paper makes a substantial contribution to the literature and is therefore recommended for publication in PLOS-ONE after minor revision taking into account the following general or specific comments. • Thank you for your comments and your feedback! General comments The study uses and analyzes the 10-year data (2005 to 2014) from Cook and DuPage counties in the Chicago, Illinois region and the accuracy of the predictions of the developed model tested with the data of the same specific area. However, according to the literature, it is well known that models predicting the WNV transmission and human WNV infections do not always have the same accuracy when applied to other areas with different mosquito fauna, weather conditions and/or geomorphological and demographic characteristics. Therefore, we consider that the study area should also be mentioned in the title. • Thank you for the suggestion, we have made that change Please comment and, if necessary, provide an adequate justification in the manuscript, for the reason that in this work were note included data from passive or active monitoring of WNV presence in birds and equids, which are considered by several authors as important prediction factors of the presence and spread of WNV virus in an area. • We have added a statement (145-147) that the avian and equid surveillance programs were not consistent across the time period, and added a discussion section (467-474) about the point. Specific comments Line 170 of the manuscript: If available, please provide information on the species of Culex mosquitoes that have been tested for WNV presence as the vectorial competence of different species may vary significantly for WNV transmission to humans. • We agree that is an important point; we have added some information as to common species in the region. Line 179 of the manuscript: Please add a bibliographical reference in the reference section for the MIR estimation tool by Biggerstaff, 2006. • Thank you, corrected Line 188 of the manuscript: Please provide a definition and some additional information about the category of "probable cases of WNV" that were also included in the study along with the "confirmed cases" because the symptoms of infection by the West Nile vary in severity, with the mild forms can be easily confused with flu symptoms and usually go unreported. • We have added the information. The difference between probable and confirmed cases is confirmatory testing by either IDPH or CDC; all cases had positive diagnostic results and clinical signs during the likely transmission season. Lines 578-580 of the manuscript: Please, correct Reference no 39 by adding the name of the journal, volume number and pages numbers. Messina JP, Brown W, Amore G, Kitron UD, Ruiz MO. West Nile Virus in the Greater Chicago Area : A Geographic Examination of Human Illness and Risk from 2002 to 2006. URISA Journal 2011;23: 5-18. • Corrected Reviewer #2: Dear authors, This is a well written paper that deals with the determination of factors affecting the spatiotemporal variability of WNV cases in humans through identification of the fine scale drivers of WNV transmission in an urban area with a repeated history of WNV outbreaks. The findings are very interesting since they include multi-level modeling of weekly data from over a decade and they extend our knowledge in the correlation of variables related to temperature, precipitation, mosquito infection, land cover, and demographic characteristics with the probability of an area having a WNV case or not. • Thank you Further down please consider some comments of minor importance that may benefit the manuscript. It seems that the infection status of avian population, as primary reservoirs of WNV, and equids, as dead-end hosts, were not included among the tested variables for modeling structure. Please note that these are critical factors implicated in the WNV transmission in order to develop predictive models. As mentioned in the introduction, public health surveillance for WNV involves collection and testing of dead birds suspected to have died of WNV, testing of sentinel chickens or of wild birds captured for this purpose and reporting of cases of equine illness. Could you please justify this data gap in the model structuring? Is there any surveillance system for infected avian and equids population in the study area? In the “Introduction” you may add any relevant literature data where bird and/or equine infection rate were used for development of models predicting WNV transmission in humans. Also, in lines 440-459 of the manuscript, you could mention the fact that avian and equids infection status was not considered as a factor for prediction of WNV cases in humans in the study area. • We have added a statement as to the inconsistent application of avian and equid surveillance in this region (145-147), and given more information about that surveillance in the discussion (467-474), including references to models using these data types. According to the best multivariable model that was used, the proportion of open water was negatively associated with the probability of WNV cases. Also, as mentioned in the discussion, a negative association of precipitation and WNV cases was observed and this indicates that dry and hot weather conditions would increase the probability of an area being positive for a WNV case. Instead, it is supposed that high rainfall and high percentage of water bodies in an area may favor mosquito population by increasing their breeding sites, and therefore may lead to increased WNV cases in humans. Hence, a positive correlation between precipitation and water bodies with WNV cases in humans is anticipated. Please comment. • Open water is classified as areas in which any aquatic vegetation is submerged, as opposed to woody or herbaceous wetlands. This is not likely to be stagnant water of the type used by Culex mosquitoes for breeding. Therefore, the negative association between proportion of open water and WNV cases is most likely due to the fact that open water, as defined, does not favor the mosquito population. We have noted this in the discussion (434-438). Attachments Attachment Submitted filename: revision.docx https://doi.org/10.1371/journal.pone.0227160.r002
27 Mar 2020 Decision Letter - Nikos T Papadopoulos, Editor PONE-D-19-34216R1 The drivers of West Nile virus human illness in the Chicago, Illinois, USA area : fine scale dynamic effects of weather, mosquito infection, social, and biological conditions PLOS ONE Dear Dr. Smith, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. The paper is much improved and there no need for additional review besides some important editorial elements that need to be addressed. Please my previous comments as far as improvements in figure legends and in references list are regarded. " .... In addition, please elaborate more to render Figure captions self explained by including all respective information. Also, the references list should be checked carefully and editing mistakes should be corrected. For example all scientific names at species and genus level should be given in italics. Last table 5 could be included as supplementary materials." Please consider the attached annotated pdf and also make some additional proofreading especially in reference. We would appreciate receiving your revised manuscript by May 11 2020 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols 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). This letter should be uploaded as separate file and labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out. We look forward to receiving your revised manuscript. Kind regards, Nikos T Papadopoulos Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. Attachments Attachment Submitted filename: PONE-D-19-34216_R1.pdf https://doi.org/10.1371/journal.pone.0227160.r003
Revision 2
3 Apr 2020 Author Response In addition, please elaborate more to render Figure captions self explained by including all respective information. Completed Also, the references list should be checked carefully and editing mistakes should be corrected. For example all scientific names at species and genus level should be given in italics. Corrected Last table 5 could be included as supplementary materials. Done Please consider the attached annotated pdf and also make some additional proofreading especially in reference. All corrections have been made Attachments Attachment Submitted filename: Response to Editor.docx https://doi.org/10.1371/journal.pone.0227160.r004
10 Apr 2020 Decision Letter - Nikos T Papadopoulos, Editor The drivers of West Nile virus human illness in the Chicago, Illinois, USA area : fine scale dynamic effects of weather, mosquito infection, social, and biological conditions PONE-D-19-34216R2 Dear Dr. Smith, We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements. Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication. Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. 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 enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and 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. With kind regards, Nikos T Papadopoulos Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0227160.r005
Formally Accepted
15 Apr 2020 Acceptance Letter - Nikos T Papadopoulos, Editor PONE-D-19-34216R2 The drivers of West Nile virus human illness in the Chicago, Illinois, USA area : fine scale dynamic effects of weather, mosquito infection, social, and biological conditions Dear Dr. Smith: I am 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 notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, 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. For any other questions or concerns, please email plosone@plos.org. Thank you for submitting your work to PLOS ONE. With kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Nikos T Papadopoulos Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0227160.r006

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