Comparison of de-duplication methods used by WHO Global Antimicrobial Resistance Surveillance System (GLASS) and Japan Nosocomial Infections Surveillance (JANIS) in the surveillance of antimicrobial resistance

Toshiki Kajihara; Koji Yahara; John Stelling; Sergey Romualdovich Eremin; Barbara Tornimbene; Visanu Thamlikitkul; Aki Hirabayashi; Eiko Anzai; Satoyo Wakai; Nobuaki Matsunaga; Kayoko Hayakawa; Norio Ohmagari; Motoyuki Sugai; Keigo Shibayama

doi:10.1371/journal.pone.0228234

Peer Review History

Original SubmissionJanuary 8, 2020
25 May 2020 Decision Letter - Patrick Butaye, Editor PONE-D-20-00688 Comparison of de-duplication methods used by WHO Global Antimicrobial Resistance Surveillance System (GLASS) and Japan Nosocomial Infections Surveillance (JANIS) in the surveillance of antimicrobial resistance PLOS ONE Dear Dr. Kajihara, 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 reviewers were positive about the manuscript. There are some changes to be done to increase clarity. The manuscript should also be reduced in the introduction and discussion. That will increase its clearness and bring a clear message. Please submit your revised manuscript by Jul 09 2020 11:59PM. 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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. Please amend the manuscript submission data (via Edit Submission) to include author Satoyo Wakai. 3. Please amend your authorship list in your manuscript file to include author Tomoyo Wakai. [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. 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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: De-duplication of datasets used for surveillance of antimicrobial resistance is important and it has been shown that this strategy influences the final report. There are several strategies for de-duplication, the manuscript compares two of them, the Japanese JANIS and the WHO GLASS system. Depending on definition of the denominator for some antibiotics significant differences were found between the two methods. The methods and datasets appear comprehensive, presentation of results in general is adequate. I only have few comments: 1. pg. 3 "per multi-resistance phenotype" . In the whole paper there is no definition of multi-resistence phenotype. It only multi-resistant strains are included, the result is severly skewed. Explain or define "multi-resistance". 2. pg. 8 line 2: "using" 3. pg 10 "considering antimicrobial resistance": in which form is resistance considered? This remains unclear in the whole manuscript. 4. pg 10 last line, pg 11 first line: usage of ~, -, <=, >= is not consistent in the whole manuscript, please change 5 pg 11: "and data stratification": what kind of stratification(s)? Please elaborate. 6. pg 15: "specimen types involved in an infection": how was it assured that the isolate/specimen came from an infection rather than from colonization? 7. pg 18 last para. "in JANIS, the total number..." total number of what? (isolates, patients, specimens, or what?) 8. pg 18 last sentence: "decreased ... up to xx%" suggest to write "decreased resistance rates from ... to.. " 9. pg 21 2nd para last sentence: "specimen-type specific infection rates" again how was it determined that samples originated from infections rather colonizations? 10.pg 23 para 2 first sentence: hard to understand what is meant. In addition, the program code for the Java as well as for the Perl program should be made available. Reviewer #2: The manuscript provides important information about 2 large surveillance programs. De-duplication is a very important issue, and the study provide a broad analysis on how it can affect the results of these large surveillance programs. The data is interesting and deserves publication, but the manuscript is too long, especially discussion and introduction. These 2 sections can be extensively reduced. ****** 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.] 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.0228234.r001
Revision 1
5 Jun 2020 Author Response Point-by-point response to the editor’s and the reviewers’ comments: Editor’s comments: The reviewers were positive about the manuscript. There are some changes to be done to increase clarity. The manuscript should also be reduced in the introduction and discussion. That will increase its clearness and bring a clear message. Response: Thank you very much for your positive evaluation and constructive comments. We revised this article as below. Response to Reviewer’s Comments Reviewer #1: De-duplication of datasets used for surveillance of antimicrobial resistance is important and it has been shown that this strategy influences the final report. There are several strategies for de-duplication, the manuscript compares two of them, the Japanese JANIS and the WHO GLASS system. Depending on definition of the denominator for some antibiotics significant differences were found between the two methods. The methods and datasets appear comprehensive, presentation of results in general is adequate. I only have few comments: 1. pg. 3 "per multi-resistance phenotype". In the whole paper there is no definition of multi-resistence phenotype. It only multi-resistant strains are included, the result is severly skewed. Explain or define "multi-resistance". Response: Thank you very much for your comment. We removed the vague word “multi-resistance” throughout the text, and modified the sentences as follows: “removing repeated isolates of the same bacterial species isolated from a patient within 30 days, regardless of specimen type, but distinguishing isolates with change of antimicrobial resistance phenotype” (Abstract) and “Basically, JANIS uses a method that removes repeated isolates of the same species isolated from a patient within 30 days, regardless of specimen type, but still distinguishing isolates that showed change of antimicrobial resistance phenotype (e.g., from susceptible to resistant for any antibiotic, as detailed in Materials and Methods).” (Introduction) 2. pg. 8 line 2: "using" Response: We revised the word accordingly (page7 line18). 3. pg 10 "considering antimicrobial resistance": in which form is resistance considered? This remains unclear in the whole manuscript. Response: As explained above (No. 1), we modified it as “still distinguishing isolates that showed change of antimicrobial resistance phenotype (e.g., from susceptible to resistant for any antibiotic, as detailed in Materials and Methods)” (page 8 line 15-17). The detail in Materials and Method is as follows: “A subsequent isolate is selected and counted if it shows phenotypic change from susceptible to resistant (or vice versa) or a 4-fold or more comparison of MIC value for a specific antibiotic when compared to a previous isolate from the same patient within the 30-day period, as implemented in the in-house Java program. The server-side program of JANIS also selects the 1st isolate with intermediate susceptibility to a specific antibiotic isolated from the same patient within the 30-days period, although the intermediate susceptibility is not accounted for in this study because it focuses on and compares percentage of resistance.” (page12 line4-11). 4. pg 10 last line, pg 11 first line: usage of ~, -, <=, >= is not consistent in the whole manuscript, please change Response: We revised the word accordingly as (<15, 15-64, 64<) (page10 line9) and (<1, 1-4, 5-14, 15-24, 25-34, 35-44, 45-54, 55-64, 65-74, 75-84, 84<) (page10 line10-11). 5 pg 11: "and data stratification": what kind of stratification(s)? Please elaborate. Response: We elaborate it accordingly as “in each specimen type per age group, gender, and infection origin stratification” (page11 line6-7). 6. pg 15: "specimen types involved in an infection": how was it assured that the isolate/specimen came from an infection rather than from colonization? Response: Thank you very much for this important comment. As suggested, there is no way to distinguish infection from colonization here, so we removed “involved in an infection” and modified the sentence as “older patients tend to have multiple specimen types such as blood, urine, and sputum” (page15 line7-8). 7. pg 18 last para. "in JANIS, the total number..." total number of what? (isolates, patients, specimens, or what?) Response: We modified it as “total number of isolates subject to AST” accordingly (page18 line6). 8. pg 18 last sentence: "decreased ... up to xx%" suggest to write "decreased resistance rates from ... to.. " Response: We fixed it as “decreased the resistance rates for blood isolates from 16.4% to 13.6% and …” accordingly (page18 line16). 9. pg 21 2nd para last sentence: "specimen-type specific infection rates" again how was it determined that samples originated from infections rather colonizations? Response: We completely agree with your point as explained above (No. 6), and modified it as “infection or colonization” (page21 line10). 10.pg 23 para 2 first sentence: hard to understand what is meant. Response: We removed the paragraph according to the comment of Reviewer 2 and Editor. What we meant was “Regarding the de-duplication method from JANIS, the 30 day rule is used to count the patients after removing repeated isolates, and also count the isolates by selecting those with different antimicrobial resistance phenotype even within 30 days.”. In addition, the program code for the Java as well as for the Perl program should be made available. Response: We have made the programs at https://github.com/bioprojects/GLASS-JANIS-comparison as now written in Materials and Methods (page10 line12-13). Reviewer #2: The manuscript provides important information about 2 large surveillance programs. De-duplication is a very important issue, and the study provide a broad analysis on how it can affect the results of these large surveillance programs. The data is interesting and deserves publication, but the manuscript is too long, especially discussion and introduction. These 2 sections can be extensively reduced. Response: Thank you very much for your comment. We shortened the introduction and the discussion accordingly. Specifically, we removed the following sentence. Introduction-1: For P. aeruginosa, Acinetobacter baumanii and other species commonly found in healthcare-associated infections, there are frequently many repeated isolates in multiple specimen types over an extended period time, which makes the impact of the different methods larger. Introduction-2: (isolates collected on hospital day 3 or later are considered “hospital origin” while other hospital isolates and all outpatient isolates are considered “community origin”): “For each surveillance period (e.g. 12 months), only one result should be reported for each patient per surveyed specimen type and surveyed pathogen” (Guide to preparing aggregated antimicrobial resistance data files in GLASS) Introduction-3: As mentioned above, the data submitted to GLASS were tabulated using a method that has been used in JANIS because the JANIS team had not yet developed a tabulation program implementing stratified de-duplication. Discussion-1: Regarding the de-duplication method from JANIS, the 30 day rule is used to count the patients after removing repeated isolates, and also count the isolates by selecting those with different antimicrobial resistance phenotype even within 30 days. When the latter is used as a numerator, the percentage of resistance increases slightly. This is because of the count of subsequent isolates that show change from susceptible to resistant (or vice versa) or 4-fold or more comparison of MIC values for an antibiotic compared to the previous isolate from the same patient even within a 30 day period However, in the data from Japan in 2017 used in the WHO GLASS report, the count did not account for the change of antimicrobial resistance phenotype and thus the percentage of resistance was closer to the value calculated using the first-isolate rule from GLASS. Discussion-2 (moved to Supplementary Information): This is now downloadable from the home page of the antimicrobial resistance research center at the National Institute of Infectious Diseases (https://www.niid.go.jp/niid/ja/from-lab/2415-amrc/9213-janis-glass-excel-en.html). Users can interact with these data by simply clicking their mouse. This tool (its graphical user interface is shown in S1 Figure) can create antibiograms stratified by the bed size of hospitals (under 200, over 200 and under 500, over 500 beds), inpatient or outpatient, gender, specimen type, and age group as defined by GLASS. Based on this, users can create antibiograms after excluding UNKNOWN_NO_AST. As another variable regarding missing data, GLASS defines UNKNOWN_NO_BREAKPOINTS representing the number of isolates where AST was performed but no interpretation of the results is available for a specific antibiotic. In the Excel tool, we have renamed this as UNKNOWN_NO_SIR to imply that S-I-R interpretation was not possible. It can be included or excluded from the denominator for calculating resistance rates in the tool. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0228234.r002
15 Jun 2020 Decision Letter - Patrick Butaye, Editor Comparison of de-duplication methods used by WHO Global Antimicrobial Resistance Surveillance System (GLASS) and Japan Nosocomial Infections Surveillance (JANIS) in the surveillance of antimicrobial resistance PONE-D-20-00688R1 Dear Dr. Kajihara, 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, Patrick Butaye, DVM, PhD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0228234.r003
Formally Accepted
18 Jun 2020 Acceptance Letter - Patrick Butaye, Editor PONE-D-20-00688R1 Comparison of de-duplication methods used by WHO Global Antimicrobial Resistance Surveillance System (GLASS) and Japan Nosocomial Infections Surveillance (JANIS) in the surveillance of antimicrobial resistance Dear Dr. Kajihara: 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 Professor Patrick Butaye Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0228234.r004

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