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PONE-D-20-11384

Prevalence and factors associated with asymptomatic malaria and anemia among pregnant women in Kwale County, Kenya: A hospital based cross sectional study

PLOS ONE

Dear Mr Nyamu,

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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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

Reviewer #2: No

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

Reviewer #1: Yes

Reviewer #2: No

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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: Yes

Reviewer #2: Yes

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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: Yes

Reviewer #2: 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 investigators have surveyed pregnant women in their district of Kenya for malaria and anaemia at first antenatal visit. With a cohort of just over 300 women they have a reasonable power to identify risk factors for these conditions, as well as estimating their prevalence with reasonable precision. The observations are not particularly novel, but the study is of some interest in examining these important pregnancy-associated morbidities.

Major comments

1. Abstract results: make it clear whether the results presented are adjusted odds ratios throughout.

2. Risk factors for AIP: The authors need to better explain how anaemia risk is apparently associated with BOTH first trimester, AND gestation >16 weeks. There are problems with results presentation in Table 3 and it seems they have got the reference and comparator groups switched for the gestation comparison. In addition, part of the results in the table are presented as percentages of women with risk factor who are anaemia (the table column heading) and part are presented as percentage of anaemic women who fall into each risk factor category (not what we want). Please redo this table and recheck your AORs and revise text accordingly.

3. Discussion: differences in malaria prevalence between Kenya and Burkina Faso are more likely related to malaria transmission intensity, prevalence falls with gestation, and falls more in women receiving IPTp. (Related to this, please also discuss role of IPTp in controlling MIP in conclusions).

4. Similarly, end P 11, haemodilution over pregnancy seems more likely to explain declining hb over pregnancy. If postulating dfetal needs please provide reference.

Minor comments

1. Abstract: line 1 “pregnancy”. Results 3rd sentence rewrite “ Women who had MIP were 12.9%”. Last line of results: rewrite for clarity.

2. There were a lot of spacing issues in the pdf, e.g. words joined together, or words and brackets without spaces before them. Examples in abstract methods: odds ratios(OR) and confidence intervals(CI)- there are many others.

3. Introduction 3rd sentence change “malaria with AIP and consumption of soil (geophagy)”, needs different punctuation?

4. Next sentence: is this risk factors for MIP (parasitic infections? High gravidity is NOT associated with MIP) Or AIP?

5. “In sub-Saharan Africa, MIP affects approximately 125 million pregnant women every year”- this is a major misreading of the cited reference.

6. Top of P 5 “a cross sectional”

7. Inclusion/exclusion: “as well as those who”

8. Sample size “desired level” of what was 5%?

9. Data management “ between a variety…”

10. Page 8: “prevalence and risk factors for malaria parasitemia”. Latent malaria is not a recognised phrase. Next line remove “who”.

11. Parasite counts are best expressed as geometric mean not median.

12. P 9 define mild, moderate, severe anaemia.

13. Page 11 first paragraph contains multiple grammatical errors, please rewrite

14. Third paragraph same page please rewrite.

15. A lot of the references are incomplete (lacking volumes/pages), or not enough details are given to retrieve them, or have formatting issues. Refs 2, 5, 6 (what is MOH? Where can this be obtained- similar comments for some others), 7, 17-22, 33.

16. Table groups need editing to ensure e.g. it is clear which group women with 8 y school fall into. Same for gestation. And make table 2 N column wider so numbers are readable.

17.

Reviewer #2: Malaria in pregnancy (MiP) remains a serious public health issue in sub-Saharan African countries despite efficient preventive measures, making difficult for the overall control of malaria. This present study aims to determine the prevalence and risk factors associated with asymptomatic malaria and anaemia among pregnant women in Kwale county, Kenya. The topic of asymptomatic malaria (potential reservoir) is relevant, however, as presented, this article is not original. In addition, the manuscript still requires significant grammatical editing to improve its readability and clarity.

The authors should highlight the fact that asymptomatic malaria is an important concern especially in the first ANC visit where any preventive measures are not yet implemented. Also, they have to underline the importance of the first trimester which is a critical risk period for pregnant women in terms of malaria and anaemia as found in their results.

There are below some comments for the authors that they should take into consideration for improving the manuscript. Moreover, a numbered manuscript would have making easier the review.

1) Suggested title: “Prevalence and risk factors associated with asymptomatic Plasmodium falciparum infection and anaemia among pregnant women at the first antenatal care visit: A hospital based cross-sectional study in Kwale County, Kenya. Use asymptomatic malaria is less specific.

2) Abbreviations: Malaria in pregnancy (MiP and not MIP), Anaemia in pregnancy (AiP and not AIP)

3) Abstract:

a. Background sub-session: Prevalence of malaria in pregnancy, not … in pregnant

b. Results sub-session: please specify what type of odds you used for AiP (crude or adjusted)

4) Key words: important key words do not appear. Please use “asymptomatic malaria” instead of “parasitaemia” which could lead confusion as including symptomatic and asymptomatic cases.

5) Introduction

a. The authors should provide more detail on the current policies against malaria and anaemia during pregnancy used in Kenya, particularly IPTp administration and timeline, iron and folate supplementation? Who in charge of these measures (Government or pregnant women themselves)?

b. Page 3, line 6: “Other factors associated with MiP are……” Use “Other” supposes that you have cited first factors which is not the case. Please rephrase the sentence to make it clear.

c. Page 3, line 7: The authors state that “high parity” is associated with malaria. What do you mean by high parity? Multigravidae women? If yes, I think it’s a wording mistake as it’s well-known that is the primigravidae who are higher risk of MiP, so ‘less parity”.

d. The rational of the study is unclear as presented. Please, give more details explaining what the study brings for the scientific community which are not already known. The only fact that “factors contributing to MiP are not well-described in this part of Kenya” is not sufficient.

e. What is the most common species of malaria parasites in Kenya? I suppose “P. falciparum”. Hence, it would interesting to adjust the title of manuscript accordingly.

6) Methods

a. Ethical statement should be presented in the main text.

i. Did the pregnant women receive IPTp at the 1st ANC if they were eligible?

ii. Did the pregnant women with asymptomatic malaria receive curative treatment? What and how (uncomplicated and severe malaria)? If not, why? Same concerns regarding the anaemia, particularly severe cases?

iii. Any written informed consent? Any ethical committee approval?

b. Study population: give more detail on the strategy of participants selection

c. Did you consider among the symptoms of malaria the history of fever the past 48 h before the visit?

d. Exclusion criteria: Pregnant women who had taken antimalarial drugs within the past two weeks were excluded. What about the women who had taken fever drug? There is a risk to consider women asymptomatic while they just took fever drug the day before the visit.

e. Sample size: The authors have considered a prevalence of MiP from a study in Burkina Faso (24%) while the malaria transmission is different to both countries.

f. Data collection: give more details on socio-demographic characteristics, obstetric and clinical history. How did you assess the LLIN use? Please define the different trimesters of pregnancy (1st, 2nd, 3rd)? Give more details on how the gestational age was assessed?

g. Quality control: Please precise if the 10% of slides chosen was for all sides or positive slides.

h. Statistical analysis: What procedure did you use for variable selection in the final model (multivariate model)?

7) Results

a. Table 1: The proportion of pregnant women in the first trimester at the 1st ANC visit was 9.4% while the authors found that the proportion of pregnant women with gestational age < 16 wg was 15.9%. Why this discrepancy when the first trimester finished at 15 wg.

b. Table 2:

i. Why did you keep in the final multivariate model, the variable gestational age even if not significant in bivariate analysis?

ii. In the same way, why did you keep in the multivariable model “slept under bed net previous night” and “frequency of sleeping under bed net”. Both variables seems to be correlate.

iii. However, you drop out the variable “gravidity” which should be forced in the final model even if not significant because it’s a well-know factors strongly associated with MiP. Furthermore, I would like to suggest to the authors to make an sensitivity analysis by pooling primigravidae and secundigravidae in comparison to multigravidae.

c. Prevalence and factors associated with latent malaria:

i. Please define latent malaria?

ii. What is the prevalence of asymptomatic malaria among pregnant women in the 1st, 2nd and 3rd trimesters at the first ANC visit?

iii. What are the proportion of different species of parasites (P.f.; P.o; P.v; P.m)

iv. Please define POR at the first time it use in the text.

d. Prevalence and factors associated with anaemia:

i. Among the 3.6% of severe anaemia, how many are infected by malaria?

8) Discussion

a. Regarding the factors associated to MiP:

i. The authors should also discuss what happens among women in the first trimester of pregnancy. We can observe that women are more at risk of infection than those in 2nd and 3rd trimester (19.7% vs. 12.7% and 10.4%, respectively).

ii. The only factor associated with MiP is young age (< 20 y). The authors should consider to check an interaction between age and gravidity as both are correlated. Hence, this could be explained by that young pregnant women are mostly primigravidae? This deserves a couple of sentence in the discussion.

b. Regarding the factors associated to AiP: First and 3rd trimester are both associated with AiP. This could be also explained by the haemoglobin level variation due to physiopathology of the pregnancy. This should be included in the discussion

c. Study limitations: The authors have stated several limitations for the study. It is a good point. However, they have to explain how they have controlled this bias to ensure the validity of the study.

9) Conclusion: The authors should revise their conclusion in order to highlight the originality of the study.

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Reviewer #1: No

Reviewer #2: No

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PONE-D-20-11384R1

Prevalence and risk factors associated with asymptomatic Plasmodium falciparum infection and anemia among pregnant women at the first antenatal care visit: A hospital based cross-sectional study in Kwale County, Kenya.

PLOS ONE

Dear Dr. Nyamu,

Thank you for submitting your revised 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 newly revised version of the manuscript that addresses the points raised by the reviewers.

Both reviewers were in agreement that the revised manuscript is an improvement on the original submission, but both have nevertheless still raised some issues that require further attention, in particular concerning grammatical errors. Reviewer #1 has taken the time to provide a copy-edited version, appended to this letter, to assist in improving the English throughout. You should address these concerns in your revision along with the specific remaining issues outlined in the appended comments from the reviewers.

Please submit your revised manuscript by Sep 11 2020 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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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: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Adrian J.F. Luty, PhD

Academic Editor

PLOS ONE

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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)

Reviewer #2: All comments have been addressed

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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: Partly

Reviewer #2: Partly

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

Reviewer #1: Yes

Reviewer #2: 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 #1: Yes

Reviewer #2: 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 #1: No

Reviewer #2: No

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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: The authors have addressed many of my comments but I have a few of remaining issues they need to address.

It would have been helpful if the manuscript had page and line numbers.

1. Discussion page 3: The high rates of net ownership cannot really be attributed to the policy of bed net distribution at first ANC visit as women would only receive these nets AFTER enrolment in the study- so no primigravidae would have received nets by this route. The mass distribution campaigns are more likely driving this.

2. Table 3 still needs correction. The column n(%) needs to be the percentage of women who are anaemic as a fraction of the women in that row. From Trimester onwards the figures must be corrected.

3. In the same table the crude POR for secundigravidae is incorrect. They have a higher anaemia prevalence than women in first trimester.

4. Also in Table 3, please switch “gestation >16 weeks” and “gestation ≤ 16 weeks” to be consistent with the rest of the table where lower values come first.

5. In these lines there is an error in n for women ≥16 weeks with anaemia- is it 174?

I have also attached the revised manuscript with highlighting to indicate the many minor formatting, spacing and other editorial issues that need to be corrected. These are mostly around missing spaces, and spaces which should not be there.

Two specific formatting comments:

1. Primigravidae, multigravidae are always written as one word and are nouns. Primi-gravidae is not correct and nor is “primigravidae women.

2. A semi-colon has a different function from the usage here. Colons are appropriate, or the punctuation can be removed.

Reviewer #2: While the revised manuscript has improved, it still requires significant grammatical editing to improve its readability and clarity. Some concepts remain unaddressed for me.

a) In the first review, I have highlighted that the rational of the study is unclear. The authors stated that pregnant women are potential reservoir of P.f parasites; however, the IPTp is one the main strategy protected pregnant women and is administered regardless the malaria status of women. Hence, this should not be a major lack as the women will clean by IPTp. In addition, in their conclusion, the authors recommended to take into account women of reproductive age in malaria control program; but no specific strategy has been suggested. The authors should revise their manuscript to show the scientific add-value of their paper.

b) For positive malaria management, the authors just precised that they used per the government of Kenya

Policy in prevention and control of Malaria in Pregnancy. But they should presented shortly how these cases are managed in the manuscript.

c) Informed consent administration: What is the process for illiterate women who did not write?

d) There is no flow chart diagram? How many pregnant women ineligible were excluded to reach the 308 pregnant women? And what are the reasons? Also compared the baseline characteristics of the pregnant women included and those who did not

e) How many participants have been excluded because of the following criteria: Intake of antipyretic drugs within 48h?

f) I have a concerns with the cut-off used to define 1st, 2nd and 3rd trimester. The authors define first trimester by using a gestational age < 12 wg instead of 14 completed wg, the cut-off usually used. Why ?

g) Two methods were used to measure the gestational age (fundal height and LMP); but there is no precision in what situation one or both are used?

h) QC of positive and negative slides. What is done in case of discrepancy ?

i) The authors showed that the prevalence of malaria were 6.9%; 13.9% and 13.2% in the first, 2nd and 3rd trimester respectively? It is slightly amazing as results as the prevalence should decrease from first trimester to delivery because of preventive measures implemented. How the authors explained this result. this deserve a couple of sentences in the discussion session

j) The authors highlighted the IPTp started from the 12 wg. I'm not sure if this is the current WHO recommendation as the IPTp should started as soon as possible from the 2nd trimester.

k) Number the page of manuscript.

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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 #1: No

Reviewer #2: Yes: Manfred Accrombessi

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Attachments

Attachment

Submitted filename: PONE-D-20-11384_R1_reviewer-1.pdf

Prevalence and risk factors associated with asymptomatic Plasmodium falciparum infection and anemia among pregnant women at the first antenatal care visit: A hospital based cross-sectional study in Kwale County, Kenya.

PONE-D-20-11384R2

Dear Dr. Nyamu,

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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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,

Adrian J.F. Luty, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

This manuscript is now acceptable for publication; however, the English needs again additional improvement.

For example on the clean version, there are some minor errors identified

- Line 1: Plasmodium should be in italic

- Line 2: Typo error on "department"

- Line 26: "Prevalence of malaria in pregnancy" instead of "both asymptomatic and symptomatic"

- Line 30: delete "asymptomatic". Pregnant women could not be asymptomatic

- Line 33: Odds ==> odds

- Line 44: Asymptomatic MiP, not AiP

- Line 46: Please reconsider "Pregnant"; may be "Pregnancy" or "Pregnant women"

- Line 54: Sub - Saharan Africa ==> sub-Saharan Africa

- Line 55: Delete 89324/142896 and keep only the %

- Line 63: Malaria in pregnancy, not Pregnancy with capital P. And we have already defined an abbreviations for that purpose, so use MiP

- Lines 65-67: Rephrase the sentence. Due to...., pregnant women are more at risk of malaria"

-Lines 70-71: Rephrase the sentence to make it clear. What do you mean by focused antenatal care? Use abbreviation of ANC previously defined

- Lines 105, 108: Combine sub-session of study design and study population ==> study design and population

- Lines 111: Inclusion and exclusion criteria should be included in the "study population" session

- Line 128-136: Rephrase the sub-session "sample size determination" by making an unique block without bullets.

- Line 156: Delete were, there is a repetition of "were" with those of line 155

- Line 174: Why abbreviate No Parasit Found (NPF) as you did not use it after in the mansucript

- Line 217: First bracket missing for 56.2%

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: All comments have been addressed

Reviewer #2: All comments have been addressed

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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: (No Response)

Reviewer #2: Yes

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

Reviewer #1: (No Response)

Reviewer #2: 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 Response)

Reviewer #2: Yes

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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: (No Response)

Reviewer #2: No

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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: (No Response)

Reviewer #2: (No Response)

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Reviewer #1: No

Reviewer #2: No