Genomics of human and chicken Salmonella isolates in Senegal: Broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections

Yakhya Dieye; Dawn M. Hull; Abdoul Aziz Wane; Lyndy Harden; Cheikh Fall; Bissoume Sambe-Ba; Abdoulaye Seck; Paula J. Fedorka-Cray; Siddhartha Thakur

doi:10.1371/journal.pone.0266025

Peer Review History

Original SubmissionAugust 6, 2021
24 Jan 2022 Decision Letter - Patrick Butaye, Editor PONE-D-21-24873Genomic comparison of clinical human to chicken meat Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infectionsPLOS ONE Dear Dr. Dieye, 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 indicated some minor problems with the manuscript. Please reply to all and adapt the manuscript appropriately, highlighting the changes. Please submit your revised manuscript by Mar 10 2022 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. 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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: Title of Manuscript (PONE-D-21-24873): Genomic comparison of clinical human to chicken meat Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections 1st Author: Yakhya Dieye, PhD Review Comments 1. Throughout the manuscript you have used ‘antibiotics’ and ‘antimicrobials’ interchangeably. Best to use one consistently – I think ‘antimicrobials’ would be more suitable for this type of manuscript that compares clinical (human) and animal isolates 2. Page 74-75: Please revise sentence to read Food animals (poultry, cattle and pigs) and their products (including eggs, milk and pork) constitute …. 3. Line 371-372: You could add to that statement on these lines a further statement to read, ‘or where such regulations exist, they are often not enforced’ Overall verdict: The paper is well written and offers analysis of AMR from a somewhat one-health approach (has human and animal samples). Future similar analyses will be strengthened by incorporating environmental and plant samples in an expanded dataset. I recommend it for publication once the above minor corrections have been addressed. Reviewer #2: In the present study, the authors performed whole genome sequencing of 72 Salmonella isolates recovered from humans (n=19) and chicken meat (n=53) during a surveillance project in Dakar, Senegal. The aim of their study was to determine the resistance profile of nontyphoidal Salmonella strains from clinical cases in humans, and the potential origin of these strains from retail chicken meat. Their results suggested possible transmission of the emerging multidrug resistant (MDR) Kentucky ST198 and serotype Schwarzengrund from chicken to human. The title and the introductory part (L22-31) in the abstract are too wordy Abstract Line 37: cephalosporins are not historical first-line drugs Lines 38-39: ‘..pointing to the concern posed by the excessive use of antimicrobials in farming.’: do the authors have data to sustain this statement, at least for Senegal? Introduction Lines 53-62: Introducing Salmonella and Samonella infections is too wordy Line 65: The term “developing countries” is no longer preferred. Recommend using the World Bank classification of low- and middle-income countries. Same for “developed countries” (high-income countries). + Line 370 and 372 Lines 69-72: some other data are available (see hereafter) Carey ME et al. The Surveillance for Enteric Fever in Asia Project (SEAP), Severe Typhoid Fever Surveillance in Africa (SETA), Surveillance of Enteric Fever in India (SEFI), and Strategic Typhoid Alliance Across Africa and Asia (STRATAA) Population-based Enteric Fever Studies: A Review of Methodological Similarities and Differences. Clin Infect Dis. 2020 Jul 29;71(Suppl 2):S102-S110. doi: 10.1093/cid/ciaa367. PMID: 32725221; PMCID: PMC7388711. Nikiema MEM et al. Contamination of street food with multidrug-resistant Salmonella, in Ouagadougou, Burkina Faso. PLoS One. 2021 Jun 17;16(6):e0253312. doi: 10.1371/journal.pone.0253312. PMID: 34138936; PMCID: PMC8211238. Pulford CV, et al. Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa. Nat Microbiol. 2021 Mar;6(3):327-338. doi: 10.1038/s41564-020-00836-1. Epub 2020 Dec 21. PMID: 33349664; PMCID: PMC8018540. Kalonji LM, et al. Invasive Salmonella Infections at Multiple Surveillance Sites in the Democratic Republic of the Congo, 2011-2014. Clin Infect Dis. 2015 Nov 1;61 Suppl 4:S346-53. doi: 10.1093/cid/civ713. PMID: 26449951. Kariuki S, Onsare RS. Epidemiology and Genomics of Invasive Nontyphoidal Salmonella Infections in Kenya. Clin Infect Dis. 2015 Nov 1;61 Suppl 4(Suppl 4):S317-24. doi: 10.1093/cid/civ711. PMID: 26449947; PMCID: PMC4596933. Langendorf C et al. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoS One. 2015 Mar 23;10(3):e0120275. doi: 10.1371/journal.pone.0120275. PMID: 25799400; PMCID: PMC4370739. …. and many more i.e. type https://pubmed.ncbi.nlm.nih.gov/?term=Jacobs+J+and+salmonella+and+africa&sort=date and https://pubmed.ncbi.nlm.nih.gov/?term=Weill+FX+and+salmonella+and+africa&sort=date Quoted in Ref 18 Please rephrase this part (Lines 69-72) according to the supplied information Line 75: eggs and milk are not food animals but remained important vehicles of Salmonella, especially eggs Lines 90-94: Still accurate for some parts of the world but banned in other parts (In 2006, the EU banned the use of antibiotics as feed additives for growth promotion). This sentence has to be nuanced Line 103: which COULD promote M&M Line 120: Human Salmonella isolates dated from 2012-2013. Same period for the Isolates from chicken. Make it clear at line 123. It is clearly enounced at lines 175-176. Lines 132-139: For antibiotics abbreviations try to use some internationally recognized ones such as http://bsacsurv.org/science/antimicrobials/ OR from EUCAST https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/Disk_abbreviations/EUCAST_system_for_antimicrobial_abbreviations.pdf Interestingly, those abbreviations were only used later in Table 3 Line 142: MasterPureTM Gram Positive DNA Purification Kit for Gram negative bacteria Results Lines 178-180: these are repetitions of what was mentioned in the M&M section Line 193: were absent in chicken Not appropriate: were not found in Salmonella isolates from chicken. Line 197: yes, clearly, serotypes Kentucky and Virchow are known to be closely associated with poultry Lines 272-273 + 420-421: Additionally, one isolate of Kentucky ST198 was resistant to sulfamethoxazole-trimethoprim while possessing a sul1 only without a dfrA gene. We made the same observation in S. maltophilia isolates where the dfrA gene was absent and where the dihydrofolate reductase was mutated and was conferring resistance to trimethoprim (not yet published, only in biorxiv) Lines 274-278: would have be better if MIC to fluoroquinolone antibiotic had been performed Lines 296-298: I do not know about the performance of plasmidSPAdes algorithm for assembling large plasmids from whole genome sequencing data, but the most detected plasmids were only from the Col plasmid family (high copy number and small in size <10kb). Could this affect the results for larger plasmids from the IncH or IncI or F? If yes, this should be mentioned in the Limitations section. PlasmidFinder also allows to find replicons from WGS data. Discussion Line 348: a local market in Senegal. Add the city name where chicken meat was sold Lines 388-392: add reference i.e. Line 401: add doi: 10.1136/bmjgh-2021-005659 to Ref 6 Line 424-427: Not sure family units use antibiotics as growth promotors. Therefore, the link between improper use of antibiotics (line 425), small-scale farming (426) and continuous selection of MDR strains (427) is unclear to me. Do data on antibiotic consumption in human and animals exist in Senegal? If yes, authors should refer to those data in the discussion section, especially in lines 432-439. ****** 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: Yes:** Prof. Samuel Kariuki 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. Attachments Attachment Submitted filename: Review Comments_PONE-D-21-24873.docx https://doi.org/10.1371/journal.pone.0266025.r001
Revision 1
2 Feb 2022 Author Response Responses to reviewers Dear Editor, We are submitting a revised version of manuscript PONE-D-24873 entitled “Genomic comparison of clinical human to chicken meat Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections”. We have made all the revisions requested. We thank both reviewers for their comments and suggestions that significantly improved the quality of our manuscript. Below are the responses to the academic editor and reviewers. Responses to the academic editor 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf Done 2. Please upload a copy of Figure 2, to which you refer in your text on page 19. If the figure is no longer to be included as part of the submission please remove all reference to it within the text. Figure 2 was mistakenly mentioned on page 19 of the submitted manuscript. It has been changed to “S2 Table”, page 19, lines 327, 329 and 332 of the revised manuscript. 3. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. Captions (SI Table and S2 Table) have been added for Supporting Information files at the end of the Discussion section, page 24, lines 438 and 440 of the revised manuscript. 4. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. The reference list has been updated. All the added citations are mentioned in the responses to the reviewers. 5. We have made the additional changes: • Line 343 of the original manuscript, line 336 of the revised version: “form” changed to “from”. Responses to Reviewer 1 1. Throughout the manuscript, you have used ‘antibiotics’ and ‘antimicrobials’ interchangeably. Best to use one consistently – I think ‘antimicrobials’ would be more suitable for this type of manuscript that compares clinical (human) and animal isolates The changes requested by the reviewer have been made lines 77, 96 and 233 of the revised manuscript. 2. Lines 74-75: Please revise sentence to read Food animals (poultry, cattle and pigs) and their products (including eggs, milk and pork) constitute …. The changes requested by the reviewer have been made lines 67-68 of the revised manuscript. 3. Line 371-372: You could add to that statement on these lines a further statement to read, ‘or where such regulations exist, they are often not enforced’ The changes requested by the reviewer have been made line 365 of the revised manuscript. Overall verdict: The paper is well written and offers analysis of AMR from a somewhat one-health approach (has human and animal samples). Future similar analyses will be strengthened by incorporating environmental and plant samples in an expanded dataset. I recommend it for publication once the above minor corrections have been addressed. We thank the reviewer for his valuable suggestions that contributed to improving the quality of our manuscript. Responses to Reviewer 2 The title and the introductory part (L22-31) in the abstract are too wordy The title and the introductory part of the abstract have been shortened according to the reviewer’s suggestion (lines 21-27 of the revised manuscript). Abstract Line 37: cephalosporins are not historical first-line drugs The corresponding sentence has been modified line 33 of the revised manuscript, to correct the mistake identified by the reviewer. Lines 38-39: ‘..pointing to the concern posed by the excessive use of antimicrobials in farming.’: do the authors have data to sustain this statement, at least for Senegal? There are several publications reporting surveys on antimicrobial use African countries. In the original manuscript, we mention a reference (Ref 41; Ref 45 in the revised version) lines 423-425 in the Discussion section (lines 416-417 of the revised manuscript) that reported a survey in chicken farms. We have further evidences from a survey (unpublished) made in 2020 on behalf of the AMR Working Group of the Permanent Secretariate of the High National Counsel for Global health Security Agenda (to which we are a member). The survey mentioned the following among others: • Importers of antimicrobials (AM) distribute molecules without compliance to existing recommendations • There is no control of the distribution • 37.5% of the veterinary pharmacists provide AM without prescription • 60% of the veterinary doctors prescribe AM treatment without antimicrobials susceptibility testing • 50% of the veterinary doctors prescribe human AM for animal treatment • Only 53% of the veterinary doctors follow guidelines for AM use in animals • Etc. Introduction Lines 53-62: Introducing Salmonella and Samonella infections is too wordy The introduction on Salmonella has been shorten according to the reviewer’s suggestion (lines 49-54 of the revised manuscript). Line 65: The term “developing countries” is no longer preferred. Recommend using the World Bank classification of low- and middle-income countries. Same for “developed countries” (high-income countries). + Line 370 and 372 The changes requested by the reviewer have been made lines 24, 25, 57, 363 and 365 of the revised manuscript. Lines 69-72: some other data are available (see hereafter) Please rephrase this part (Lines 69-72) according to the supplied information We thank the reviewer for bringing to our attention these important data. We have reformulated the pointed section, lines 61-65 of the revised manuscript and added a few of the suggested references (refs 6-9 of the revised manuscript). Line 75: eggs and milk are not food animals but remained important vehicles of Salmonella, especially eggs The changes requested by the reviewer have been made line 68 of the revised manuscript. Lines 90-94: Still accurate for some parts of the world but banned in other parts (In 2006, the EU banned the use of antibiotics as feed additives for growth promotion). This sentence has to be nuanced The sentence has been change lines 83-87 to incorporate the reviewer’s suggestion. Line 103: which COULD promote The changes suggested by the reviewer have been made line 96 of the revised manuscript. M&M Line 120: Human Salmonella isolates dated from 2012-2013. Same period for the isolates from chicken. Make it clear at line 123. It is clearly enounced at lines 175-176. The changes suggested by the reviewer have been made line 114 of the revised manuscript. Lines 132-139: For antibiotics abbreviations try to use some internationally recognized ones such as http://bsacsurv.org/science/antimicrobials/ OR from EUCAST https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/Disk_abbreviations/EUCAST_system_for_antimicrobial_abbreviations.pdf. Interestingly, those abbreviations were only used later in Table 3 We do agree with the reviewer regarding the abbreviations used for antimicrobials. We used a two-letter code instead of the more commonly used three-letter code for a formatting purpose, in order to have all the information fit in Table 3. This Table is quite long and spans across three pages. The two-letter code helped minimize it length while avoid case breaking between pages. Line 142: MasterPureTM Gram Positive DNA Purification Kit for Gram negative bacteria This kit was used because it yielded from Salmonella genomic DNA of better quality for sequencing using an Illumina platform. This was added lines 137-139 in the revised manuscript. Results Lines 178-180: these are repetitions of what was mentioned in the M&M section We deleted the sentences mentioned from the Results section. Line 193: were absent in chicken Not appropriate: were not found in Salmonella isolates from chicken. The changes suggested by the reviewer have been made line 186 of the revised manuscript. Line 197: yes, clearly, serotypes Kentucky and Virchow are known to be closely associated with poultry Agree. Lines 272-273 + 420-421: Additionally, one isolate of Kentucky ST198 was resistant to sulfamethoxazole-trimethoprim while possessing a sul1 only without a dfrA gene. We made the same observation in S. maltophilia isolates where the dfrA gene was absent and where the dihydrofolate reductase was mutated and was conferring resistance to trimethoprim (not yet published, only in biorxiv) We are very grateful to the reviewer for sharing this discovery. We would be very interesting to know more about the mentioned biorxix manuscript. We are trying to identify the genetic determinant supporting the resistance to trimethoprim and would be interested to collaborate with the reviewer in this topic. Lines 274-278: would have be better if MIC to fluoroquinolone antibiotic had been performed We do agree with the reviewer. Unfortunately, a MIC system is currently not available in our laboratory to perform the suggested analysis. Lines 296-298: I do not know about the performance of plasmidSPAdes algorithm for assembling large plasmids from whole genome sequencing data, but the most detected plasmids were only from the Col plasmid family (high copy number and small in size <10kb). Could this affect the results for larger plasmids from the IncH or IncI or F? If yes, this should be mentioned in the Limitations section. PlasmidFinder also allows to find replicons from WGS data. We tested both plasmidSpades and PlasmidFinder and found the former to give results that are more reliable since it permits to get most of the plasmid sequences. In other genomics studies, we recovered sequences of large plasmids (the biggest being +300 kb) using plasmidSpades. We did not find any bias regarding plasmid size in the strains analyzed in this study and in others not published yet. We will be happy to share more on our experience using plasmidSpades. Discussion Line 348: a local market in Senegal. Add the city name where chicken meat was sold The changes suggested by the reviewer have been made line 341 of the revised manuscript. Lines 388-392: add reference i.e. A reference (ref 53 of the revised version) has been added line 383 as requested by the reviewer. Line 401: add doi: 10.1136/bmjgh-2021-005659 to Ref 6 The indicated article has been added as ref. 60 and mentioned line 394 of the revised manuscript. Line 424-427: Not sure family units use antibiotics as growth promotors. Therefore, the link between improper use of antibiotics (line 425), small-scale farming (426) and continuous selection of MDR strains (427) is unclear to me. In Senegal, broilers available to consumers come mostly from family units that raise chicken for consumption and for limited commercialization, and from small and mid-size chicken farms. There is no legislation banning the use of antimicrobials as growth promoter in farming, but only recommendations to which farmers are often not aware of. Consequently, empirical use of antimicrobials to promote animal growth is a common practice. Do data on antibiotic consumption in human and animals exist in Senegal? If yes, authors should refer to those data in the discussion section, especially in lines 432-439. Data on human and animal consumption of antimicrobial are not systematically collected and made available in Senegal. However, Permanent Secretariate of the High National Counsel for Global health Security Agenda, through its AMR Working Group is currently putting in place recommendations what would lead to regulations and legislations in the near future. We would like to thank the reviewer for his thorough review and for the interesting suggestions and guidance he provided. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0266025.r002
14 Mar 2022 Decision Letter - Patrick Butaye, Editor Genomics of human and chicken Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections PONE-D-21-24873R1 Dear Dr. Dieye, 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.0266025.r003
Formally Accepted
16 Mar 2022 Acceptance Letter - Patrick Butaye, Editor PONE-D-21-24873R1 Genomics of human and chicken Salmonella isolates in Senegal: broilers as a source of antimicrobial resistance and potentially invasive nontyphoidal salmonellosis infections Dear Dr. Dieye: 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.0266025.r004

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