PONE-D-22-22276Seroepidemiological Investigation of Crimean Congo Hemorrhagic fever virus in Livestock in Uganda, 2017PLOS ONE

Dear Dr. Luke Nvakarahuka, 

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.

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ACADEMIC EDITOR: The manuscript needs a revision in the writing process and language editing. The reviewers comments should be replied clearly.  

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Please submit your revised manuscript by Oct 24 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. When you're 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.

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Shawky M Aboelhadid, PhD

Academic Editor

PLOS ONE

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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: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

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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: No

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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 study shows the results of a comprehensive serological survey looking at the seroprevalence of CCHFv in livestock in Uganda. The study included 3 different species known to be amplifier hosts for the virus and the risk factors associated with seropositivity are explored. CCHF is a disease of public health importance, and in Uganda the recent identification of clinical cases supports the need of further investigations aimed to understand its epidemiology and project the risk for humans, especially at-risk populations. It was great to see that the whole country was represented in the survey, and the large sample size is a positive aspect. While I recommend revisions, I am aware of the potential of this manuscript once these aspects are addressed.

Comments

Major

� Improve its clarity and the flow of ideas of the manuscript. At the moment, it is not easy to read the manuscript and some changes are required to make the writing flow so that the story and the message are clear.

� From an epidemiological perspective, there seems to be an underlying well-thought study design that is crucial for the conclusions made for the country. However, many important details were not included in the text leaving many questions unanswered for potential readers. The authors indicate that the sample size is one of the greatest strengths but without further information to understand the design and the context the large number of animals sampled loses relevance.

� The results could be more informative. Considering the scope of the analysis in a study conducted in several districts and including 3 species, many more details that are fundamental to understand the burden of the disease in the country and the implications of the findings.

� The discussion requires a more critical point of view. Currently, it is focused in comparing the results of the survey with the results from previous studies including systematic reviews but considering the complexity of CCHFv with a clear ecological component (vector, reservoirs, transmission to humans), the discussion should be able to critically explain this results in relation to the design, the implications and the limitations of the analysis conducted.

� The authors are referred to The STROBE Statement – Checklist of items that should be included in reports of cross-sectional studies to improve the manuscript.

Minor

� Requires more attention to little details including punctuation, use of language, and percentages presented.

Notes

- Keywords should be indexed terms.

- More details of the funders as indicated in the guidance.

1. Abstract

� “Adult animals 36 represented 70.6% and 78% of the sampled animals were females whereas local breeds represented 71.5%” (Line 35-37). Not clear what the two percentages mean as it seems to be talking only about adult animals, so I would expect only one percentage. Please review this idea and re-write for clarity.

� Worried about making conclusions about spatial trends without formally testing (Line 39-40).

� For clarity, invert the risk across species and start by indicating that sheep and goats had a higher risk, otherwise, it is not immediately clear how cattle had lower odds when only the OR for sheep and goats is presented (Line 40-41)

� Line 44: Missing p for p value of p>0.01. A little misleading that some of the differences are expressed as OR with confidence intervals and other with p-values. I suggest standardising for the abstract.

� Would be careful to say that the study shows that CCHFv is endemic in Uganda based on this (Line 50-51). Maybe say is actively circulating? What are the criteria to declare a disease endemic? Maybe as it is the first serological survey of this type, more evidence is required before making such a conclusion.

� For the abstract, I suggest focussing on the results of the multivariable model in more detail. Presenting both univariate and multivariable results can be misleading.

2. Background

� Complete some references (e.g. Line 56) and review punctuation (e.g. Line 63). Along the text there are many statements including the reports of the cases in the districts, the percentage of animals positive in Wakiso and Kiboga, etc that would need a reference to the report or at least the source which I assume is the Ugandan Virus Research Institute.

� CCHFv is transmitted directly and indirectly, but for animals in the absence of clinical signs it is more frequently tick-mediated. Indicating that is animal-to-animal gives the wrong impression, in my opinion (Line 59).

� While the information contained in the introduction is relevant, it lacks writing flow, so it is not an engaging introduction to read. I would suggest splitting into small paragraphs and improving the connections between sentences and paragraphs for a more enjoyable read.

� When I read the objective, I think about the seropositivity but it is also clear that you’re looking to explore the risk factors associated to seropositivity and to assess the links to reproductive problems. Would be worth mentioning here for clarity and to manage expectations of readers.

� Would be interesting to mention which tick vectors are involved. This would give some information to the readers in relation to why you’re thinking CCHFv might be found in Uganda, even in districts that have not reported cases. Is it likely that the ticks that transmit it are there?

3. Methods

� Study design: All the information is there but once again I find that the writing and flow of ideas needs to be improved. For instance: Start with study locations and how/why these were selected and later move on to describe the types of herds included. Additional details of the classification of the districts into high and low risk is important, especially because you have not mentioned before any details of the possible tick vectors implicated in transmission. Of the list, which are the high-risk districts, which are low risk districts and which ticks are found there. I suggest including a map to visually present this information, as this part of the design is crucial for the conclusions made later on.

� Sample size calculation and data collection: Reference the software used for calculating the sample size. Also, all the parameters including error should be disclosed so this calculation can be replicated (Line 107-108). Once the sample size is calculated how was it distributed across districts? What is the selection criteria for the animals (inclusion and exclusion) including age, sex, production system and how were the species distributed? Was it a random or convenience sample? Was it stratified in any way, for instance the production system (transhumant vs non-nomadic)? How were herds selected? There needs to be clarity of the population selected to be able to interpret the results of the study appropriately.

� Data analysis: More information of the procedure used from analysis. You started with a bivariate analysis, but no detailed tests are included. Same for the multivariable model, which model (I assume it is a logistic regression), however, more details are required as to how variables are selected in the model, if the structured nature of the data (herds within districts) was considered and how you selected and assessed the final model. If R was used for data analysis, the packages should be included and referenced. In addition, there seems to be an additional hypothesis being tested here related to the reproductive history. I am aware that this needs further evidence but at the moment it is presented without contexts as to why you’re looking for this association if the initial goal and justification for the study was mainly to identify which areas might be at risk using livestock as sentinels for CCHFv. If this part is kept, it needs to be additional information to introduce why this is interesting and then the gap that this is filling. Also details on how many animals have information of this and how we can trust it given that it is incomplete. How did you choose the cut off point for elevation? Does it make sense to think about it like this considering possible ideal habitats for the ticks?

� Ethics statement: Not clear, partially because there are many acronyms that should be defined (e.g., CFR, IBR, UVRI). I suggest to re-write this part and improve the flow of information presented for clarity.

4. Results

� Table 1: Does not present the overall seroprevalence but the description of the study population. It would be good to be clear on the cut-off points or definitions for some of the variables. For example, criteria to classify an animal as an infant, ‘medium’, and adult. Also, what was accepted as healthy vs unhealthy for current and past health (eligibility criteria), abortion and still birth (definition and how did you ask this question (timeframe considered)). Most of these aspects should be better described in the methods so the reader is clear by the time the information is presented here. Were there differences in these categories between species? It would be interesting to know how the population was distributed in relation to the location (as suggested before) and also, in relation to the main features.

� Bivariate analysis of risk factors: Same comment as before for the way to present the comparative risk across species (Lines 186 – 188).

� Please standardise the results p-values or OR. It is more informative to present OR for all as it indicates the magnitude of the risk.

� Table 2: Some of the choices of reference for the comparison are odd. Normally, the reference category is the one that is believed to be at a lower risk and in some of these I don’t understand how this was chosen. For instance, animals zero grazed might be at lower risk than paddocking and communal because the later roam free and are more exposed to ticks. The selection of the reference category needs further thought/justification/discussion.

� Table 3: Same comments as before, consider how the variable that you are evaluating influences the risk and then this makes more sense when analysing and interpreting in the discussion.

� The model that you chose to present is simple considering the structured population (does not include random effects). However, I wonder about the differences between the non-nomadic vs transhumant districts, the high and low-risk districts that you described in the methods, and also the locations that are in the border vs the ones that are not. Lastly, were there fundamental differences across locations or the systems in the districts that explain these differences? what about the different species? Does anything change when you analyse their risk separately?

� The results could have been a little bit more informative, based on the data you collected and the even if the initial aim is only mapping, describing, and evaluating individual risk, my perception is that the study falls short on addressing fundamental aspects related to the epidemiology of CCHF.

� The district names in the figure are not readable.

5. Discussion:

� Line 227: “We designed a study 227 to estimate the burden of the disease in livestock to come up with risk-based health surveillance models for RVF” – Please review should say CCHF. Also, if this is a risk-based health surveillance as indicated here, more details should be included about this in the methods and in the results to support this claim and the results obtained.

� Line 239-234: Maybe commercial essays overestimate but there is no way to be sure. Reasons for variations in seroprevalence are multiple. Unless to you compared and you’re performing quality control of the results by running them in duplicate or any other strategy, not sure if the performance of the diagnostic test is the only possible explanation for this difference. What about real differences? Timing? Population?

� It would have been interesting to have a discussion in relation to the findings of districts that have previously reported the cases, considering that some of these were sampled as part of this survey (e.g. Agago).

� Need to discuss the limitations/possible biases of the study/design and how this affects the conclusions. As well as further perspectives.

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Reviewer #1: No

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PONE-D-22-22276R1Seroepidemiological Investigation of Crimean Congo Hemorrhagic fever virus in Livestock in Uganda, 2017PLOS ONE

Dear Dr. Nyakarahuka,

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 manuscript needs a revision according to the reviewer's comments.

Please submit your revised manuscript by May 25 2023 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. When you're 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.

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). You should upload this letter as a separate file labeled 'Response to Reviewers'.
• A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Shawky M Aboelhadid, PhD

Academic Editor

PLOS ONE

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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.

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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 #1: (No Response)

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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 #1: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

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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 #1: No

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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 #1: Yes

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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 #1: Thanks for addressing the initial comments. The manuscript has been improved and reads well. Only minor comments:

Abstract:

1. In this sentence “CCHFV seropositivity appeared to be generally higher in northern districts of the country, though spatial trends among sampled districts were not obvious”, I suggest replacing ‘obvious’ to ‘examined’.

2. Make sure that decimals all along are the same, either 1 or 2. For example the total of the percentages of seropositive animals for all species does not add 100%. Please check this all along.

Methods:

1. “Herds were selected for sampling to be followed prospectively” – Not sure what this means, adding the word prospectively to the methods when this is a survey is confusing. Please clarify or remove.

2. “Assuming an average of 15 animals per herd, we 118 expected to sample 156 herds, distributed evenly throughout the 27 districts selected for sampling”- Ok, but it would be good to add how you selected the herds within each district and the 15 animals within each herd (when the herd had more than 15 animals). Add one sentence if each one of these steps was random or convenience sampling.

Results:

1. In table 1 please check that all the total of the animals for each variable is 3181. Some are not at the moment (e.g. Sex). Suggest to double check too in table 2 and 3, just in case.

2. “Holding all other variables in the model constant, the associations between CCHF seropositivity and animal breed and elevation were not statistically significant based on a 95% confidence limit, however, the estimated odds of seropositivity were lower among cross and exotic breeds compared to indigenous breeds, and the estimated odds of seropositivity among animals at lower elevations was higher than that among animals at higher elevations (Table 3)” – Don’t agree with what you say after 'however' because clearly you have your odds ratio indicating that based on your data there is no association. Suggesting otherwise might be misleading, maybe if you’d like to leave it better for a point of discussion.

Discussion

1. “However, Balinandi et al (2021) also performed serology on cattle samples using 278 a commercial CCHF serological testing kit, the ID screen CCHF double antigen multi-species 279 (IDVet), and found seropositivity of 75% in cattle (Balinandi, von Brömssen, et al., 2021; Sas et 280 al., 2018), thus suggesting some commercial assays may overestimate the true livestock 281 seroprevalence of CCHFV” – Still not sure if you can say this… not sure unless you’re sure it is the same area, same population and timing or if you have any evidence to support the claim that commercial tests overestimate CCHFv seroprevalence.

2. “We also found that the odds of seropositivity were higher among 315 animals sampled at lower elevations. Seroprevalence was also higher in animals with reported 316 stillbirth and abortion” – Agree but some of these aspects didn’t go to the multivariable model or didn’t come up as significant when all variables considered, for example elevation. I suggest that you make this distinction because sounds like you’d really like elevation to be one of the variables associated, but your risk model does not support that.

3. “However, as CCHF is not known to be symptomatic in animals, there is a 317 need to investigate further the impact of the CCHFV infection on animal production in terms of 318 reducing herd size and milk production. However, the interpretation and association of CCHFV 319 seropositivity with stillbirth and abortion could be confounding since the same animal populations 320 in Uganda are susceptible to other diseases that cause abortions such as brucellosis and Rift Valley 321 fever virus” – Double use of however, maybe rephrase.

4. “However, the interpretation and association of CCHFV 319 seropositivity with stillbirth and abortion could be confounding since the same animal populations 320 in Uganda are susceptible to other diseases that cause abortions such as brucellosis and Rift Valley 321 fever virus” – True, also the fact that this is a cross sectional study makes it impossible to test causation, only association.

5. “However, a stratified analysis limited to adult animals produced an odds ratio 336 approximately equal to that in the full analysis for female animals compared to male animals, 337 suggesting that age is not the primary explanation for the difference in seroprevalence between 338 male and female animals.” – Seems like adding results here, beware how you present this as it was not in your results.

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Reviewer #1: No

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Seroepidemiological Investigation of Crimean Congo Hemorrhagic fever virus in Livestock in Uganda, 2017

PONE-D-22-22276R2

Dear Dr. Luke,

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.

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Kind regards,

Shawky M Aboelhadid, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

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