The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017

Ian A. Critchley; Nicole Cotroneo; Michael J. Pucci; Rodrigo Mendes

doi:10.1371/journal.pone.0220265

Peer Review History

Original SubmissionJuly 8, 2019
13 Nov 2019 Decision Letter - Adriano Gianmaria Duse, Editor PONE-D-19-18189 The Burden of Antimicrobial Resistance among Urinary Tract Isolates of Escherichia coli in the United States in 2017 PLOS ONE Dear Dr Critchley , Thank you for submitting your manuscript to PLOS ONE. The paper is well-written and easy to follow. It provides useful information to clinicians in the USA and demonstrates the urgent need for additional oral antibiotics the treatment of urinary tract infections caused by multidrug-resistant Enterobacteriaceae. 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. Minor suggestions / recommendations: Page 5 Bacterial isolates: If this information is available, it would be useful to state what proportion of isolates were from community-acquired infections and what proportion were from hospital-acquired infections; also, from which anatomical sites were these organisms isolated? If this is not possible, state that these are from both settings and/or that sites are unknown, respectively. Reference 20 is not clear regarding this issue. Page 5 Susceptibility testing: Add the CLSI M100-S28 in the references Page 5 Resistance subsets: Consider stating which beta-lactamase genes in addition to blaCTX-M-15 were screened for. Furthermore, further characterisation of a common genotype, blaCTX-M15, could explain the persistence of these specific isolates in causing infections. Page 7 Susceptibility of all UTI isolates: Use the term "resistance/resistant" with the appropriate % consistently rather than interchanging it with "non-susceptible". Page 7 Prevalence of ESBL phenotypes Figure 2: Consider adding amikacin to figure 2. The high rate of amikacin susceptibility in the ESBL subset provides a carbapenem-sparing treatment option. Page 8 Figure 3: Showing ertapenem resistance rates would yield more useful information than meropenem does. It is clear that all isolates (ESBL and non-ESBL) are meropenem susceptible from Table 1. Ertapenem is a narrower spectrum carbapenem and where possible should be used preferentially. Page 8 Co-resistance among fluoroquinolone-resistant Table 2: Consider adding the amoxicillin-clavulanate data. Page 8 Susceptibility of blaCTX-M-15 genotypes: State what % the 151 represents of the total ESBL isolates. If any other predominating beta-lactamase type was found, add this information. If not, state this. Page 8 Susceptibility of blaCTX-M-15 genotypes Table 3: Correct year in title of Table 3 (2017 rather than 2016). Page 8 Susceptibility of blaCTX-M-15 genotypes Line 221: Should read "of the carbapenems" not "carbapenem". Page 9 Paragraph 2: Comment on the % blaCTX-M-15 found. Page 10: Nitrofurantoin and fosfomycin data are not presented-add this as a limitation of the study. Authors discuss the need for new oral antibiotics particularly from carbapenem class but perhaps testing of fosfomycin would have shown susceptibility among these pathogens. Fosfomycin is an old antibiotic, used as an oral treatment for uncomplicated urinary tract infections. Fosfomycin has been shown to have activity against some resistant uropathogens suggesting that this antibiotic may provide a useful option for the treatment of patients with difficult-to-treat-infections. We would appreciate receiving your revised manuscript by 30 November 2019. 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, Adriano Gianmaria Duse, MD Academic Editor PLOS ONE Journal requirements: 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 http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 1. We noticed you have some minor occurrence(s) of overlapping text with the following previous publication(s), which needs to be addressed: https://aac.asm.org/content/61/11/e01045-17 In your revision ensure you cite all your sources (including your own works), and quote or rephrase any duplicated text outside the Methods section. Further consideration is dependent on these concerns being addressed. 2. Thank you for including your competing interests statement; "Ian Critchley, Nicole Cotroneo and Michael J. Pucci are employees of Spero Therapeutics. Rodrigo Mendes is an employee of JMI Laboratories" We note that one or more of the authors are employed by a commercial company: name of commercial company. Please provide an amended Funding Statement declaring this commercial affiliation, as well as a statement regarding the Role of Funders in your study. If the funding organization did not play a role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript and only provided financial support in the form of authors' salaries and/or research materials, please review your statements relating to the author contributions, and ensure you have specifically and accurately indicated the role(s) that these authors had in your study. You can update author roles in the Author Contributions section of the online submission form. Please also include the following statement within your amended Funding Statement. “The funder provided support in the form of salaries for authors [insert relevant initials], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.” If your commercial affiliation did play a role in your study, please state and explain this role within your updated Funding Statement. 2. Please also provide an updated Competing Interests Statement declaring this commercial affiliation along with any other relevant declarations relating to employment, consultancy, patents, products in development, or marketed products, etc. Within your Competing Interests Statement, please confirm that this commercial affiliation does not alter your adherence to all PLOS ONE policies on sharing data and materials by including the following statement: "This does not alter our adherence to PLOS ONE policies on sharing data and materials.” (as detailed online in our guide for authors http://journals.plos.org/plosone/s/competing-interests) . If this adherence statement is not accurate and there are restrictions on sharing of data and/or materials, please state these. Please note that we cannot proceed with consideration of your article until this information has been declared. Please include both an updated Funding Statement and Competing Interests Statement in your cover letter. We will change the online submission form on your behalf. Please know it is PLOS ONE policy for corresponding authors to declare, on behalf of all authors, all potential competing interests for the purposes of transparency. PLOS defines a competing interest as anything that interferes with, or could reasonably be perceived as interfering with, the full and objective presentation, peer review, editorial decision-making, or publication of research or non-research articles submitted to one of the journals. Competing interests can be financial or non-financial, professional, or personal. Competing interests can arise in relationship to an organization or another person. Please follow this link to our website for more details on competing interests: http://journals.plos.org/plosone/s/competing-interests https://doi.org/10.1371/journal.pone.0220265.r001
Revision 1
22 Nov 2019 Author Response Response to reviewer comments: Page 5 Bacterial isolates: If this information is available, it would be useful to state what proportion of isolates were from community-acquired infections and what proportion were from hospital-acquired infections; also, from which anatomical sites were these organisms isolated? If this is not possible, state that these are from both settings and/or that sites are unknown, respectively. Reference 20 is not clear regarding this issue. Authors’ response: The isolates that were tested represent both nosocomial and community-acquired infections from both uncomplicated and complicated UTIs. Unfortunately, we do not have access to enough demographic data to be able to separate isolates from community versus hospital-acquired infections. We have added information on anatomical sites with the majority of the organisms being isolated from a urine culture and 132 isolates being isolates from patients with the Foley catheter. Page 5 Susceptibility testing: Add the CLSI M100-S28 in the references Authors’ response: This has been added to the reference list Page 5 Resistance subsets: Consider stating which beta-lactamase genes in addition to blaCTX-M-15 were screened for. Furthermore, further characterisation of a common genotype, blaCTX-M15, could explain the persistence of these specific isolates in causing infections. Authors’ response: The isolates were screened in silico for narrow and extended spectrum β-lactamases, including carbapenemases. We have also added a comment stating that the usual β -lactamase profiles observed in these studies have been previously published (references added). [Mendes et al., 2019 doi: 10.1093/ofid/ofz004, Castenheira et al., 2019 doi: 10.1128/AAC.00160-19 and Mendes et al., 2019 doi: 10.1089/mdr.2019.0198]. Page 7 Susceptibility of all UTI isolates: Use the term "resistance/resistant" with the appropriate % consistently rather than interchanging it with "non-susceptible". Authors’ response: Changes made to substitute the non-susceptible rates with resistance rates Page 7 Prevalence of ESBL phenotypes Figure 2: Consider adding amikacin to figure 2. The high rate of amikacin susceptibility in the ESBL subset provides a carbapenem-sparing treatment option. Authors’ response: Figure 2 has been amended to include amikacin. Page 8 Figure 3: Showing ertapenem resistance rates would yield more useful information than meropenem does. It is clear that all isolates (ESBL and non-ESBL) are meropenem susceptible from Table 1. Ertapenem is a narrower spectrum carbapenem and where possible should be used preferentially. Authors’ response: Yes, we agree but unfortunately not all the 287 ESBL phenotypes of E. coli were tested against ertapenem (only 141 isolates had available susceptibility results for ertapenem) so we selected meropenem as a representative carbapenem since data was available for all 287 ESBL phenotypes for these three drugs. Page 8 Co-resistance among fluoroquinolone-resistant Table 2: Consider adding the amoxicillin-clavulanate data. Authors’ response: Although only 8.6% of the levofloxacin-resistant isolates were resistant to amoxicillin-clavulanate, 34.3% of the isolates displayed were in the intermediate category that would not be reflected in the current presentation of the table and was a factor in our reason not to include. Page 8 Susceptibility of blaCTX-M-15 genotypes: State what % the 151 represents of the total ESBL isolates. If any other predominating beta-lactamase type was found, add this information. If not, state this. Authors’ response: This been added to the text to highlight that CTX-M-15 was the most prevalent accounting for 59% of the ESBL phenotypes of E. coli. Also highlighted that OXA-1/30 was the next most prevalent but in most isolates was co-expressed with CTX-M-15. Page 8 Susceptibility of blaCTX-M-15 genotypes Table 3: Correct year in title of Table 3 (2017 rather than 2016). Authors’ response: This has now been corrected to reflect 2017 Page 8 Susceptibility of blaCTX-M-15 genotypes Line 221: Should read "of the carbapenems" not "carbapenem". Authors’ response: This has been corrected Page 9 Paragraph 2: Comment on the % blaCTX-M-15 found. Authors’ response: Added the following text: “Furthermore, blaCTX-M-15 was the most prevalent genotype among the UTI isolates of E. coli accounting for 59% of all the ESBL phenotypes Page 10: Nitrofurantoin and fosfomycin data are not presented-add this as a limitation of the study. Authors discuss the need for new oral antibiotics particularly from carbapenem class but perhaps testing of fosfomycin would have shown susceptibility among these pathogens. Fosfomycin is an old antibiotic, used as an oral treatment for uncomplicated urinary tract infections. Fosfomycin has been shown to have activity against some resistant uropathogens suggesting that this antibiotic may provide a useful option for the treatment of patients with difficult-to-treat-infections. Authors’ response: We have added some text to the discussion regarding fosfomycin and nitrofurantoin as oral options for uncomplicated UTI. We included an explanation of why fosfomycin was not tested because of the requirement for agar dilution and therefore a limitation of the current study. Also included a sentence on nitrofurantoin and although a good option of uUTIs caused by E. coli it is not suitable for complicated UTIs where other pathogens such as K. pneumoniae and P. mirabilis are not well covered with this agent. Additional Author Response to Reviewer Questions: 1. We noticed you have some minor occurrence(s) of overlapping text with the following previous publication(s), which needs to be addressed: https://aac.asm.org/content/61/11/e01045-17 In your revision ensure you cite all your sources (including your own works), and quote or rephrase any duplicated text outside the Methods section. Further consideration is dependent on these concerns being addressed. Authors’ response: All the overlapping text is from the methods section only and there is no duplicated text from outside the Methods section. Both studies were conducted in the same laboratory and used the same methods to molecularly characterize the isolates. To make it clear we have added a reference citation in the methods section to the article by Sader et al. (https://aac.asm.org/content/61/11/e01045-17) to reference the methods used in that study. 2. Thank you for including your competing interests statement; "Ian Critchley, Nicole Cotroneo and Michael J. Pucci are employees of Spero Therapeutics. Rodrigo Mendes is an employee of JMI Laboratories" We note that one or more of the authors are employed by a commercial company: name of commercial company. Authors’ response: The companies listed above are still relevant as described above for all the authors 3. Please provide an amended Funding Statement declaring this commercial affiliation, as well as a statement regarding the Role of Funders in your study. If the funding organization did not play a role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript and only provided financial support in the form of authors' salaries and/or research materials, please review your statements relating to the author contributions, and ensure you have specifically and accurately indicated the role(s) that these authors had in your study. You can update author roles in the Author Contributions section of the online submission form. Authors’ response: Our respective employers (Spero Therapeutics and JMI Laboratories) did not have any role in the study design and only provided financial support in the form of salaries and research materials. All authors played an equal role in the design and analyses and presentation of the data arising from this surveillance study. Please also include the following statement within your amended Funding Statement. “The funder provided support in the form of salaries for authors [insert relevant initials], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.” If your commercial affiliation did play a role in your study, please state and explain this role within your updated Funding Statement. 2. Please also provide an updated Competing Interests Statement declaring this commercial affiliation along with any other relevant declarations relating to employment, consultancy, patents, products in development, or marketed products, etc. Within your Competing Interests Statement, please confirm that this commercial affiliation does not alter your adherence to all PLOS ONE policies on sharing data and materials by including the following statement: "This does not alter our adherence to PLOS ONE policies on sharing data and materials.” (as detailed online in our guide for authors http://journals.plos.org/plosone/s/competing-interests) . If this adherence statement is not accurate and there are restrictions on sharing of data and/or materials, please state these. Please note that we cannot proceed with consideration of your article until this information has been declared. Authors' response: We confirm our adherence to all PLOS ONE policies on sharing data and materials and provide the following statement "This does not alter our adherence to PLOS ONE policies on sharing data and materials." (as detailed in your guide for authors http://journals.plos.org/plosone/s/competing-interests) Please include both an updated Funding Statement and Competing Interests Statement in your cover letter. We will change the online submission form on your behalf. Please know it is PLOS ONE policy for corresponding authors to declare, on behalf of all authors, all potential competing interests for the purposes of transparency. PLOS defines a competing interest as anything that interferes with, or could reasonably be perceived as interfering with, the full and objective presentation, peer review, editorial decision-making, or publication of research or non-research articles submitted to one of the journals. Competing interests can be financial or non-financial, professional, or personal. Competing interests can arise in relationship to an organization or another person. Please follow this link to our website for more details on competing interests: http://journals.plos.org/plosone/s/competing-interests Attachments Attachment Submitted filename: Responses to reviewers comments rev.docx https://doi.org/10.1371/journal.pone.0220265.r002
26 Nov 2019 Decision Letter - Adriano Gianmaria Duse, Editor The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017 PONE-D-19-18189R1 Dear Dr. Critchley 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, Adriano Gianmaria Duse, MD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0220265.r003
Formally Accepted
2 Dec 2019 Acceptance Letter - Adriano Gianmaria Duse, Editor PONE-D-19-18189R1 The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017 Dear Dr. Critchley: 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. Adriano Gianmaria Duse Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0220265.r004

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