Molecular characterization of Cryptosporidium spp. from humans in Ethiopia

Ambachew W. Hailu; Abraham Degarege; Haileeyesus Adamu; Damien Costa; Venceslas Villier; Abdelmounaim Mouhajir; Loic Favennec; Romy Razakandrainibe; Beyene Petros

doi:10.1371/journal.pone.0253186

Peer Review History

Original SubmissionFebruary 26, 2021
8 Apr 2021 Decision Letter - Maria Stefania Latrofa, Editor Transfer Alert This paper was transferred from another journal. As a result, its full editorial history (including decision letters, peer reviews and author responses) may not be present. PONE-D-21-06475 Characterization of Cryptosporidium spp. in humans in Ethiopia PLOS ONE Dear Dr. Woreta, 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. Please submit your revised manuscript by 27th of April. 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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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: The manuscript focus on human criptosporidiosis in Ethiopia by comparing different standard and molecular techniques. Results are impressive and deserves of being published, given their importance. My only suggestions is to improve comparision with other realities and also in one health approach, considering also animal reservoir. These recent papers can be included into the discussion. Line 258 and after: Dessì, G., Tamponi, C., Varcasia, A., Sanna, G., Pipia, A.P., Carta, S., Salis, F., Díaz, P., Scala, A. Cryptosporidium infections in sheep farms from Italy (2020) Parasitology Research, 119 (12), pp. 4211-4218. Díaz, P., Varcasia, A., Pipia, A.P., Tamponi, C., Sanna, G., Prieto, A., Ruiu, A., Spissu, P., Díez-Baños, P., Morrondo, P., Scala, A. Molecular characterisation and risk factor analysis of Cryptosporidium spp. in calves from Italy (2018) Parasitology Research, 117 (10), pp. 3081-3090. Reviewer #2: Study provides data on the prevalence and genetic diversity of Cryptosporidium in human patients in Ethiopia. Study surely fills a gap I knowledge on Cryptosporidium species involved in human cryptosporidioses in the area, however, relatively small sample set does not allow for robust interpretation. Considering this fact, some parts of the study seem a bit over-interpreted, mainly when discussing zoonotic vs. anthroponotic transmission. It is questionable, how much the fact, that some of the genotypes are shared among animals and humans, suggests an infection from animal reservoir. For such an assumptions, results from animals living in proximity of tested subjects can be of great value. Relatively high number of samples proved positive only in NAATs, which opens a question of passive transfer of the oocysts through human digestive system. For humans living in highly contaminated environment this can be expected. This part might deserve some explanation or justification… otherwise the “true” prevalence mentioned might be the “distorted one” (Line 198). Paragraph in lines 308-315 raises several doubts about part of the results and mainly about conclusiveness of the study. In my opinion, its placement before Conclusions without explanations is misleading. This deserves some attention and explanations… possibly in respective parts of the results and discussions. I can only suggest the MS for publication after some revisions that consider also interpretation of results. Some minor comments follows: Line 55: consider replacing of “for identifying” by “for detection” Line 66-67: mentioning fairly distant and non-zoonotic abomasal C. andersoni without any explanation is confusing. Line 71: replace “genetic distribution” by more proper term Line 75: the goal “identifying genetic diversity… … in Ethiopia” is over-ambitious, considering the small number of samples from a single geographic region… Line 99 (and some other places): double check using the upper case letters Line 175: “55.1% reported gastrointestinal symptoms with diarrhea”… not clear to me, if this was in time of sample collection or in “any” time before visiting the hospital Line 179:”infection” not Italic Line 241-245: it is always high to compare data from various studies with various methodology and robustness of diagnostics, however, the option, that lower prevalences can be attributable to lower performance of diagnostic procedures deserves mentioning, before searching for other explanations. Line 249-252: not clear to me, why zoonotic transmission is considered more plausible than human-to-human Line 252-253 requires references Line 270-272: you say “Moreover, this subtype was recorded in immunocompetent adults in Slovakia [42] and children in Mexico [43], which provides evidence for its role in animal-to-human transmission”… this is not clear… how this relates to animal-to-human transmission? Please, clarify… Lines 272-274: the statement about sylvatic transmission is purely speculative in given context, mentioning feral horses but also (probably?) domestic calves and goats. Lines 283-302: this deserves some shortening, considering the sample set size and low significance of the results. In discussed aspects the study revealed nothing new. Last but not least, please, pay attention to formatting of references ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). 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Revision 1
10 May 2021 Author Response PONE-D-21-06475 Molecular characterization of Cryptosporidium spp. from humans in Ethiopia PLOS ONE Dear Dr. Maria Stefania Latrofa Thank you for your comments and sending us the reviewers' comments. We thank also the reviewers for their constructive comments. We have revised the manuscript following the reviewers' suggestions. describe these changes in the below paragraphs. We hope that you will find our responses acceptable and we look forward to your decision. Editors 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 https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf Response: We have checked the author guidelines for formatting of the manuscript. The revised MS meets the Plos one requirements. 2. We note you have included a table to which you do not refer in the text of your manuscript. Please ensure that you refer to Table 3 in your text; if accepted, production will need this reference to link the reader to the Table. Response: We thank the editor for picking this. We have insereted table 3 in the text in line # 221 3. We note that Figure 1 in your submission contain map images which may be copyrighted. All PLOS content is published under the Creative Commons Attribution License (CC BY 4.0), which means that the manuscript, images, and Supporting Information files will be freely available online, and any third party is permitted to access, download, copy, distribute, and use these materials in any way, even commercially, with proper attribution. For these reasons, we cannot publish previously copyrighted maps or satellite images created using proprietary data, such as Google software (Google Maps, Street View, and Earth). For more information, see our copyright guidelines: http://journals.plos.org/plosone/s/licenses-and-copyright. Response: We acknowledge the editor suggestion and have removed Fig 1 from the revised manuscript . Reviewers' comments: Reviewer #1: 1. The manuscript focus on human criptosporidiosis in Ethiopia by comparing different standard and molecular techniques. Results are impressive and deserves of being published, given their importance. My only suggestions is to improve comparision with other realities and also in one health approach, considering also animal reservoir. These recent papers can be included into the discussion. Line 258 and after: Dessì, G., Tamponi, C., Varcasia, A., Sanna, G., Pipia, A.P., Carta, S., Salis, F., Díaz, P., Scala, A. Cryptosporidium infections in sheep farms from Italy(2020) Parasitology Research, 119 (12), pp. 4211-4218. Díaz, P., Varcasia, A., Pipia, A.P., Tamponi, C., Sanna, G., Prieto, A., Ruiu, A., Spissu, P., Díez-Baños, P., Morrondo, P., Scala, A.Molecular characterisation and risk factor analysis of Cryptosporidium spp. in calves from Italy(2018) Parasitology Research, 117 (10), pp. 3081-3090. Response: Thank you for the suggestion. We have expanded the discussion that compares our findings with others and added the suggested references. We have also commented on the importance of one health approach to control zoonotic cryptosprordiasis (line 266-275). The revised text reads as follows ‘“Altogether, these findings may suggest human and animals as reservoirs for the C. parvum [49,50]. Thus, an integrated, transdisciplinary and multilevel one health approach strategies/intervention that target humans, animals and their shared environment/transmission routes would be necessarily to effectively control cryptosporidiosis in regions endemic for C. parvum infection [51]. An integerated research involving veterinary, public health and environmental fields would help better understand the burden, risk factors, transmission routes of the zoonotic C. parvum infection and plan collaborative one health approach to treat or prevent infection in animals and humans, reduce environmental contamaination and block transmission in endemic regions [51]”. Reviewer #2: Study provides data on the prevalence and genetic diversity of Cryptosporidium in human patients in Ethiopia. Study surely fills a gap I knowledge on Cryptosporidium species involved in human cryptosporidioses in the area, however, relatively small sample set does not allow for robust interpretation. Considering this fact, some parts of the study seem a bit over-interpreted, mainly when discussing zoonotic vs. anthroponotic transmission. It is questionable, how much the fact, that some of the genotypes are shared among animals and humans, suggests an infection from animal reservoir. For such an assumptions, results from animals living in proximity of tested subjects can be of great value. Relatively high number of samples proved positive only in NAATs, which opens a question of passive transfer of the oocysts through human digestive system. For humans living in highly contaminated environment this can be expected. This part might deserve some explanation or justification… otherwise the “true” prevalence mentioned might be the “distorted one” (Line 198). Response: We acknowledge your suggestions and have revised the discussion to avoid over interpretation of the current finding related to zoonotic/anthropmetric transmission.We have also discussed the reasons for the low prevalence of infection detected through the microscope (line 238-251). 2. Paragraph in lines 308-315 raises several doubts about part of the results and mainly about conclusiveness of the study. In my opinion, its placement before Conclusions without explanations is misleading. This deserves some attention and explanations… possibly in respective parts of the results and discussions. Response: We thank the reviwer for this suggestion. We have rephrased the statement in the paragraph from the revised manuscript in line # 297- 300 3.Line 55: consider replacing of “for identifying” by “for detection” Response : we have replaced ‘ identifying’” by ‘detecting’ in line 54 4. Line 66-67: mentioning fairly distant and non-zoonotic abomasal C. andersoni without any explanation is confusing. Response: We have revised the text in line 66-67. It read as “Indeed, a study reported Cryptosporidium parvum among 35 (87.5%) pre-weaned calves specimens examined in central Ethiopia” 5. Line 71: replace “genetic distribution” by more proper term Response : We have replaced the phrase ‘genetic distribution” with “ genetic diversity “ ( line # 71 ) 6. Line 75: the goal “identifying genetic diversity… … in Ethiopia” is over-ambitious, considering the small number of samples from a single geographic region… Response: We have revised the objectives of the study in the background considering the nature of the samples( line # 76). The revised text reads as ‘identify genetic diversity of the parasite circulating in human population living in Wurgissa district and Hawassa in Ethiopia”. 7. Line 99 (and some other places): double check using the upper case letters Response: we have doubled check all the words in the manuscript for proper capitalization 8. “55.1% reported gastrointestinal symptoms with diarrhea”… not clear to me, if this was in time of sample collection or in “any” time before visiting the hospital Response; the patients reported they have had diarrhea perior to their health center visit [ line # 170-171). The revised text reads as ‘Of the adults, 55.1% reported gastrointestinal symptoms with diarrhea perior to visiting the health center.” 9. Line 179:”infection” not Italic Response : we have removed the italization for the word infection in line 173.. 10. Line 241-245: it is always high to compare data from various studies with various methodology and robustness of diagnostics, however, the option, that lower prevalences can be attributable to lower performance of diagnostic procedures deserves mentioning, before searching for other explanations. Response: We have revised the text that explain the reason for the higher prevalence of infection in the current study compared to the reports in the other regions of the Ethiopia. The revised text reads as (line # 237-239“. The lower prevalence of cryptosporidiosis reported in the aforementioned studies in Ethiopia could be due to the less sensitivity of the microscopy procedures used for diagnosing Cryptospordium infection [26]´. 11. Line 249-252: not clear to me, why zoonotic transmission is considered more plausible than human-to-human Response: Thank you picking this. We have commented on the risk of human to human transmission which might have contribuited to the increased prevalence of infection in the current study area. The revised text reads as “ Altogether, these findings may suggest human and animals as reservoirs for the C. parvum [49,50]. Thus, an integrated, transdisciplinary and multilevel one health approach strategies/intervention that target humans, animals and their shared environment/transmission routes would be necessarily to effectively control cryptosporidiosis in regions endemic for C. parvum infection [51].” (line 266-270) 12. Line 252-253 requires references Response: we have included a reference [ line #264-265]. The revised text reads as ‘in human samples from Egypt, Ethiopia, and Malaysia [15, 44-46] ” 13. Line 270-272: you say “Moreover, this subtype was recorded in immunocompetent adults in Slovakia [42] and children in Mexico [43], which provides evidence for its role in animal-to-human transmission”… this is not clear… how this relates to animal-to-human transmission? Please, clarify… Response. We acknowledge the reviewers comment and have rewritten in the text (line 259-261) “ The IIaA16G1R1 subtype was reported in lamb, calves, and humans, as well as water sources in Romania [36], Estonia [37], and Slovakia [38].”. 14. Lines 272-274: the statement about sylvatic transmission is purely speculative in given context, mentioning feral horses but also (probably?) domestic calves and goats. Response. We have revised the text to read as “….Altogether, these findings may suggest human and animals as reservoirs for the C. parvum [49,50]. Thus, an integrated, transdisciplinary and multilevel one health approach strategies/intervention that target humans, animals and their shared environment/transmission routes would be necessarily …. 15. Lines 283-302: this deserves some shortening, considering the sample set size and low significance of the results. In discussed aspects the study revealed nothing new. Response: We thank the reviwer for this suggestion. We have shortned the text on the discussion including lines 283-302 the shortened paragraph read as “…. In addition, as genotyping was performed for small human samples, confirmation of zoonotic transmission was limited in this study….” 16. Last but not least, please, pay attention to formatting of references Response: we have formatted the references following the Plos one authors guideline Attachments Attachment Submitted filename: Response to reviewers.docx https://doi.org/10.1371/journal.pone.0253186.r002
31 May 2021 Decision Letter - Maria Stefania Latrofa, Editor Molecular characterization of Cryptosporidium spp. from humans in Ethiopia PONE-D-21-06475R1 Dear Dr. Woreta, 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, Maria Stefania Latrofa Academic Editor PLOS ONE Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #3: All comments have been addressed ******** 2. 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 #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #3: Yes ****** 4. 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 #3: Yes ****** 5. 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 #3: Yes ****** 6. 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 #3: Dear author The manuscript is impressive and deserve of being published, given their importance. My only suggestion is to refer to an animal reservoir. If you had been worked on animal type besides Human type maybe gave more information and clear at the site of study. The manuscript has robust interpretation and unambiguous for Cryptosporidium species distribution that infecting Human beings in both sites. ****** 7. 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 #3: No https://doi.org/10.1371/journal.pone.0253186.r003
Formally Accepted
4 Jun 2021 Acceptance Letter - Maria Stefania Latrofa, Editor PONE-D-21-06475R1 Molecular characterization of Cryptosporidium spp. from humans in Ethiopia. Dear Dr. Hailu: 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 Dr. Maria Stefania Latrofa Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0253186.r004

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