Systematic review to evaluate accuracy studies of the diagnostic criteria for periodontitis in pregnant women

Sarah dos Santos Conceição; Josicélia Estrela Tuy Batista; Simone Seixas da Cruz; Isaac Suzart Gomes-Filho; Alexandre Marcelo Hintz; Julita Maria Freitas Coelho; Johelle de Santana Passos-Soares; Peter Michael Loomer; Amanda Oliveira Lyrio; Elivan Silva Souza; Ana Cláudia Morais Godoy Figueiredo; Mauricio Gomes Pereira

doi:10.1371/journal.pone.0304758

Peer Review History

Original SubmissionNovember 2, 2023
19 Feb 2024 Decision Letter - Erika Barbara Abreu Fonseca Thomaz, Editor PONE-D-23-35573Diagnosis of Periodontitis in Pregnant Women: Systematic Review with Prevalence Meta-Analysis of Validity of CriteriaPLOS ONE Dear Dr. Gomes-Filho, 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 is very interesting and has scientific merit. Thank you for the submission to Plos One. However, special attention should be paid to the meta-analysis and the searches carried out, given the possibility of selection bias. I recommend that authors address the issues raised and submit a letter with changes and justifications. ============================== Please submit your revised manuscript by Apr 04 2024 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'. 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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, Erika Barbara Abreu Fonseca Thomaz, Ph.D Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 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 2. Note from Emily Chenette, Editor in Chief of PLOS ONE, and Iain Hrynaszkiewicz, Director of Open Research Solutions at PLOS: Did you know that depositing data in a repository is associated with up to a 25% citation advantage (https://doi.org/10.1371/journal.pone.0230416)? If you’ve not already done so, consider depositing your raw data in a repository to ensure your work is read, appreciated and cited by the largest possible audience. You’ll also earn an Accessible Data icon on your published paper if you deposit your data in any participating repository (https://plos.org/open-science/open-data/#accessible-data). 3. Please include a copy of Table 1,2 and 3 which you refer to in your text on page 8, 13, 14 and 18. Additional Editor Comments: Dear authors, The manuscript has great merit and is within the scope of the Plos One magazine. However, I recommend that you consider the reviewers' observations and others presented below. INTRODUCTION Lines 61 to 63: The authors state that “Different criteria used for diagnosing periodontitis in pregnant women have been reported (Offenbacker et al., 2001 (8); Page and Eke (2007) (9) and Eke et al. (2012) (10), Tonetti; Greenwell; Kornman (2018) (11); Lopez et al. (2002) (12); Gomes-Filho et al. (2018) (13); Bassani et al. (2007) (14); Community Periodontal Index of Treatment Needs (15), etc.). Are, in fact, all these diagnostic criteria proposed for use in pregnant women? Do these studies present diagnostic values? Why were these studies not included in the Systematic Review (SR)? METHOD Line 78: Insert S= Study design Line 85 to 109 (Search strategies and source of records): specify that the search strategy was P.O.S., given that the words used in the search referred to population, outcome and study design. Line 106: was the search updated after April/2023? I recommend updating. Lines 106 to 109: Why didn't the authors include a Google Scholar search? This database has been widely recommended in Systematic Review studies due to its high sensitivity. Lines 119 to 122: I recommend including in the qualitative synthesis the age range of the pregnant women included in the primary studies, as well as, when available, the gestational age range of the women when evaluated in these studies. This information is important given the differences in periodontal health depending on age and gestational age. I also recommend mentioning whether the exams included index teeth or the entire mouth, as well as the number of sites on each tooth. As the authors performed a meta-analysis of the prevalence of periodontitis, I suggest that the sample size and sampling design of each primary study be reported. Line 121: “In addition, studies involving animal models were excluded” – was this the only exclusion criterion? Were studies including high-risk twin pregnancies, women with different comorbidities, smokers, etc. included? Were studies with women at any time during pregnancy included? I suggest specifying the eligibility criteria further. The systematic review was designed to identify the studies´ accuracy but did not to identify studies that assessed the prevalence of periodontitis in pregnant women. Many prevalence studies were left out of the analyses, so the summary estimate of prevalence may be influenced by selection bias. RESULTS The search strategy was likely unable to identify some of the studies that met the inclusion criteria of this work - for example “Li Hui-Jun et al. Diagnostic performance of the AAP/EFP classification and the CDC/AAP case definition among pregnant women and a practical screening tool for maternal periodontal diseases. Journal of Periodontal Research, Volume 57, Issue 5, p. 960-968, 2022”. Suggested other keywords to include in the search: Self-Assessment Periodontal Disease Predictive Value of Tests Predictive Value of Test Predictive Values of Tests Negative Predictive Value Negative Predictive Values Predictive Value, Negative Positive Predictive Value Positive Predictive Values Predictive Value, Positive Diagnostic Errors Diagnostic Error Error, Diagnostic Errors, Diagnostic Misdiagnosis Misdiagnoses Diagnostic Blind Spots Blind Spot, Diagnostic Blind Spots, Diagnostic Diagnostic Blind Spot Diagnosis Diagnoses Diagnose Diagnoses and Examinations Examinations and Diagnoses Diagnoses and Examination Examination and Diagnoses I suggest that Figure 2 be included in the text – not as Complementary Material. The estimated prevalences in each study are not presented, as well as the sample size. No study presented data regarding the area under the ROC curve DISCUSSION I recommend discussing the QUADAS-2 instrument used to analyze the risk of bias. Lines 331 to 342: This section does not discuss the low external validity of these findings, given that the search was not carried out for studies on the prevalence of periodontitis in pregnant women, but for studies of “diagnostic values”. [Note: HTML markup is below. Please do not edit.] 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: Yes Reviewer #2: Yes Reviewer #3: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: I Don't Know Reviewer #3: Yes ****** 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 Reviewer #3: 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 Reviewer #3: 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: Prezados autores, Considero artigo excelente, com tema relevante para a pesquisa periodontal, especialmente para os estudos populacionais. Como recomendação, poderia enfatizar a importância de um sistema de diagnóstico periodontal específico/ mais preciso para a gestante. Para a população em geral, já existe este consenso do método de diagnóstico? Esclarecer na justificativa/ Introdução. Outo ponto: justificar a presença de um estudo antigo na revisão sistemática (Kugahara, 2008, o qual realizou teste salivar - ainda está em uso este diagnóstico, não seria muito antigo e não usual?). Reviewer #2: Queries 1. Methods: Kindly include start up and end date of the data search 2. Kindly check the objective/aim in abstract and the goal of the study in the last paragraph in introduction. Both should be same. 3. Also check the research question R1 and R2 and then frame the objectives. 4. Mention about grey literature search and whether the articles from grey literature included or not. 5. Discussion: Add new research results or systematic reviews that validate the use of different diagnostic criteria of periodontitis in pregnant woman. 6. Add new references after adding their results to the discussion. Reviewer #3: The article aims to present a systematic review of the literature on validation studies of periodontitis diagnosis methods in pregnant women. This is a relevant topic, which can contribute to increasing the quality of periodontal disease screening in this specific population group. In general, the study is well conducted, methodologically adequate and with an appropriate discussion of the results found. However, in practical terms, the article describes two distinct studies, a systematic review on validation studies and a meta-analysis on the prevalence of periodontal disease in pregnant women, the latter making use of the same database obtained in the systematic review. I think this strategy presents some important biases, which I will comment on below. The search strategy was clearly aimed at finding validation studies and not cross-sectional studies that would really express the prevalence of periodontal disease in pregnant women. The same can be applied for all other review procedures, such as the methodological quality assessment tool, QUADAS-2, which is specific for evaluate the risk of bias and applicability of primary diagnostic accuracy studies. Therefore, the review will obviously only include studies with such characteristics, which did not necessarily aim to estimate the prevalence of periodontal disease in pregnant women. Therefore, although the 4 studies that were included are cross-sectional type, they do not present representativeness to illustrate prevalence. A specific systematic review for studies on the prevalence of periodontal disease in pregnant women would certainly find another set of articles. It seems clear that the authors, upon realizing that it would not be possible to carry out the meta-analysis with the accuracy results, decided to seize the opportunity and use the same database to do so with a focus on prevalence. However, I think this strategy is not appropriate and can lead to some misguided conclusions. Among them, the one that states that a “high heterogeneity in the prevalence of periodontitis was observed amongst the included studies” (line 332). It is impossible to state that because, as I highlighted previously, the 4 studies included are not representative of the prevalence of periodontal disease in pregnant women. For the same reason, it is not also possible to state that “the summary measurement of periodontitis prevalence was 39.47% [95% Confidence Interval (95%CI): 9.34%-69.6%]” (line 193). Therefore, I think that the second objective proposed for the study (lines 68 to 69) is not possible to be achieved. I can see two solutions for the article: (1) remove the meta-analysis study, keeping only the systematic review, which, I repeat, is very well done, has relevance and can be published. (2) Redo the meta-analysis based on another literature review, focused on sectional studies on periodontal disease in pregnant women. The second solution seems more complex to me and may make the article excessively long. I think that the results found for the systematic review are already sufficient to justify publication. ****** 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: No Reviewer #2: No Reviewer #3: 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. https://doi.org/10.1371/journal.pone.0304758.r001
Revision 1
4 May 2024 Author Response Dear Erika Barbara Abreu Fonseca Thomaz, Ph.D Academic Editor PLOS ONE Provided below are the responses to the reviewers’ comments to the manuscript, “Systematic Review to Evaluate Accuracy Studies of the Diagnostic Criteria for Periodontitis in Pregnant Women” (PONE-D-23-35573). Journal Requirements: When submitting your revision, we need you to address these additional requirements. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at 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 Response: We would like to thank the reviewer for the instructions. Note from Emily Chenette, Editor in Chief of PLOS ONE, and Iain Hrynaszkiewicz, Director of Open Research Solutions at PLOS: Did you know that depositing data in a repository is associated with up to a 25% citation advantage (https://doi.org/10.1371/journal.pone.0230416)? If you’ve not already done so, consider depositing your raw data in a repository to ensure your work is read, appreciated and cited by the largest possible audience. You’ll also earn an Accessible Data icon on your published paper if you deposit your data in any participating repository (https://plos.org/open-science/open-data/#accessible-data). Response: We would like to thank again the reviewer’s information. Please include a copy of Table 1, 2, 3, and 4 which you refer to in your text on page 8, 13, 14 and 18. Response: As suggested, the copy of Tables 1, 2, 3, and 4 were included on pages 7, 8, 13, 14, 15, 16, 17, and 18, 19, respectively. REVIEWERS’ COMMENTS TO AUTHOR # Additional Editor Comments: General Comments Dear authors, The manuscript has great merit and is within the scope of the Plos One magazine. However, I recommend that you consider the reviewers' observations and others presented below. INTRODUCTION Lines 61 to 63: The authors state that “Different criteria used for diagnosing periodontitis in pregnant women have been reported (Offenbacker et al., 2001 (8); Page and Eke (2007) (9) and Eke et al. (2012) (10), Tonetti; Greenwell; Kornman (2018) (11); Lopez et al. (2002) (12); Gomes-Filho et al. (2018) (13); Bassani et al. (2007) (14); Community Periodontal Index of Treatment Needs (15), etc.). Are, in fact, all these diagnostic criteria proposed for use in pregnant women? Do these studies present diagnostic values? Why were these studies not included in the Systematic Review (SR)? Response: All of these criteria were used to diagnose periodontitis and were reported in different studies that evaluated the association of periodontitis with undesirable pregnancy outcomes. Therefore, they were not included in the present review as they were not intended to study diagnostic values. To make reading more understandable, the paragraph was rewritten, as follows: “Different criteria used for diagnosing periodontitis in pregnant women have been reported: Offenbacker et al., 2001 (8); Page and Eke, 2007 (9), and Eke et al., 2012 (10), Tonetti; Greenwell; Kornman, 2018 (11); Lopez et al., 2002 (12); Gomes-Filho et al., 2018 (13); Bassani et al., 2007 (14); Community Periodontal Index of Treatment Needs (15), etc. Which of these is the best criterion to diagnose periodontitis in pregnant women has not been agreed upon; however, they are important to estimate the frequency of maternal periodontitis and, thus, evaluate the effectiveness of preventive or therapeutic procedures and to determine individual risk (16,17).” METHOD Line 78: Insert S= Study design Response: The S= Study design is just at the end of line 78. Line 85 to 109 (Search strategies and source of records): specify that the search strategy was P.O.S., given that the words used in the search referred to population, outcome and study design. Response: As recommended, the sentence was included, line 82, as follows: “Search strategies and source of records According to the acronym PIROS, the search phrase used to identify the condition of interest, periodontitis, was developed as follows…” Line 106: was the search updated after April/2023? I recommend updating. Response: The search was updated up to 03/30/2024, line 102. Lines 106 to 109: Why didn't the authors include a Google Scholar search? This database has been widely recommended in Systematic Review studies due to its high sensitivity. Response: We would like to thank the reviewer for his comment. A total of 8 databases, including gray literature databases, were included in the present systematic review. According to AMSTAR 2, the minimum required would be 4 databases. Therefore, this research was a broad literature search. There are few studies on the topic, a preliminary search on Google Scholar did not bring results that were very different from those found in other databases. However, in future studies, we will take this into account. Lines 119 to 122: I recommend including in the qualitative synthesis the age range of the pregnant women included in the primary studies, as well as, when available, the gestational age range of the women when evaluated in these studies. This information is important given the differences in periodontal health depending on age and gestational age. I also recommend mentioning whether the exams included index teeth or the entire mouth, as well as the number of sites on each tooth. As the authors performed a meta-analysis of the prevalence of periodontitis, I suggest that the sample size and sampling design of each primary study be reported. Response: We would like to thank the reviewer’s comment. Information about age and gestational period was added throughout the text. Line 121: “In addition, studies involving animal models were excluded” – was this the only exclusion criterion? Were studies including high-risk twin pregnancies, women with different comorbidities, smokers, etc. included? Were studies with women at any time during pregnancy included? I suggest specifying the eligibility criteria further. Response: As mentioned throughout the text of the manuscript, validation studies on the specific topic of periodontitis in pregnant women are not frequent, and this statement is confirmed by the results of the searches carried out. Therefore, in the present systematic review, the only exclusion criteria were studies involving animals. The eligibility criteria for each study were included throughout the text in the description of the results. The systematic review was designed to identify the studies´ accuracy but did not to identify studies that assessed the prevalence of periodontitis in pregnant women. Many prevalence studies were left out of the analyses, so the summary estimate of prevalence may be influenced by selection bias. Response: We would like to thank the reviewer’s comment. As the third reviewer suggested, we found it pertinent to remove the prevalence meta-analysis, precisely due to the factors mentioned above. RESULTS The search strategy was likely unable to identify some of the studies that met the inclusion criteria of this work - for example “Li Hui-Jun et al. Diagnostic performance of the AAP/EFP classification and the CDC/AAP case definition among pregnant women and a practical screening tool for maternal periodontal diseases. Journal of Periodontal Research, Volume 57, Issue 5, p. 960-968, 2022”. Suggested other keywords to include in the search: Self-Assessment Periodontal Disease Predictive Value of Tests Predictive Value of Test Predictive Values of Tests Negative Predictive Value Negative Predictive Values Predictive Value, Negative Positive Predictive Value Positive Predictive Values Predictive Value, Positive Diagnostic Errors Diagnostic Error Error, Diagnostic Errors, Diagnostic Misdiagnosis Misdiagnoses Diagnostic Blind Spots Blind Spot, Diagnostic Blind Spots, Diagnostic Diagnostic Blind Spot Diagnosis Diagnoses Diagnose Diagnoses and Examinations Examinations and Diagnoses Diagnoses and Examination Examination and Diagnoses Response: We would like to thank the reviewer’s comment. After updating the searches, this study was incorporated into this systematic review, as follows: “Li Hui-Jun et al. Diagnostic performance of the AAP/EFP classification and the CDC/AAP case definition among pregnant women and a practical screening tool for maternal periodontal diseases. Journal of Periodontal Research, Volume 57, Issue 5, p. 960-968, 2022”. I suggest that Figure 2 be included in the text – not as Complementary Material. The estimated prevalences in each study are not presented, as well as the sample size. Response: We would like to thank the reviewer’s comment. However, following the suggestions explained previously, the meta-analysis was removed. No study presented data regarding the area under the ROC curve Response: We would like to thank the reviewer’s comment. The studies by Kugahara, Shosenj, Ohashi et al., 2008 and Li et al., 2022 mentioned the ROC curve, which are also mentioned in the manuscript. DISCUSSION I recommend discussing the QUADAS-2 instrument used to analyze the risk of bias. Response: As recommended, this information was added in the study strengths and limitations, line 444-447. Lines 331 to 342: This section does not discuss the low external validity of these findings, given that the search was not carried out for studies on the prevalence of periodontitis in pregnant women, but for studies of “diagnostic values”. Response: We would like to thank the reviewer’s comment. However, following the suggestions explained previously, the meta-analysis of the prevalence of periodontitis was removed. #1 Reviewer General Comments Dear authors, I consider it an excellent article, with a relevant topic for periodontal research, especially for population studies. Comments As a recommendation, I could emphasize the importance of a specific/more accurate periodontal diagnosis system for pregnant women. For the general population, does this consensus on the diagnostic method already exist? Clarify in the justification/Introduction. Response: We would like to thank the reviewer’s comment. There is still no consensus regarding the best diagnostic criteria for periodontitis in pregnant women. This information was added to the justification/introduction, as recommended, as follows: “Introduction … Different criteria used for diagnosing periodontitis in pregnant women have been reported: Offenbacker et al., 2001 (8); Page and Eke, 2007 (9), and Eke et al., 2012 (10), Tonetti; Greenwell; Kornman, 2018 (11); Lopez et al., 2002 (12); Gomes-Filho et al., 2018 (13); Bassani et al., 2007 (14); Community Periodontal Index of Treatment Needs (15), etc. Which of these is the best criterion to diagnose periodontitis in pregnant women has not been agreed upon; however, they are important to estimate the frequency of maternal periodontitis and, thus, evaluate the effectiveness of preventive or therapeutic procedures and to determine individual risk (16,17).” Another point: justify the presence of an old study in the systematic review (Kugahara, 2008, which performed a salivary test - this diagnosis is still in use, wouldn't it be very old and unusual?). Response: We believe it is important to include it, even though it is an article from 2008 since salivary markers are considered a good diagnostic method. However, recent articles not carried out in the group of pregnant women prove this statement: - Zhang Y, Kang N, Xue F, Qiao J, Duan J, Chen F, Cai Y. Evaluation of salivary biomarkers for the diagnosis of periodontitis. BMC Oral Health. 2021 May 17;21(1):266. doi: 10.1186/s12903-021-01600-5. PMID: 34001101; PMCID: PMC8130171. - Abdullameer MA, Abdulkareem AA. Salivary interleukin-1β as a biomarker to differentiate between periodontal health, gingivitis, and periodontitis. Minerva Dent Oral Sci. 2023 Oct;72(5):221-229. doi: 10.23736/S2724-6329.23.04778-2. Epub 2023 May 10. PMID: 37162330. -Mohammed HA, Abdulkareem AA, Zardawi FM, Gul SS. Determination of the Accuracy of Salivary Biomarkers for Periodontal Diagnosis. Diagnostics (Basel). 2022 Oct 14;12(10):2485. doi: 10.3390/diagnostics12102485. PMID: 36292174; PMCID: PMC9600931. #2 Reviewer General Comments 1. Methods: Kindly include start up and end date of the data search Response: We would like to thank the reviewer’s comment. The date has been included, line 102-103. 2. Kindly check the objective/aim in abstract and the goal of the study in the last paragraph in introduction. Both should be same. Response: We would like to thank the reviewer’s comment. Suggestions have been incorporated. 3. Also check the research question R1 and R2 and then frame the objectives. Response: We would like to thank the reviewer and the research question was checked, as recommended. 4. Mention about grey literature search and whether the articles from grey literature included or not. Response: In lines 104 and 105, we inform that additionally, searches were carried out in the reference lists of the selected articles and the gray literature using the ProQuest and CINAHL databases. 5. Discussion: Add new research results or systematic reviews that validate the use of different diagnostic criteria of periodontitis in pregnant woman. Response: We would like to thank the reviewer’s comment. Suggestions have been incorporated. 6. Add new references after adding their results to the discussion. Response: As recommended, suggestions have been included. #3 Reviewer General Comments The article aims to present a systematic review of the literature on validation studies of periodontitis diagnosis methods in pregnant women. This is a relevant topic, which can contribute to increasing the quality of periodontal disease screening in this specific population group. In general, the study is well conducted, methodologically adequate and with an appropriate discussion of the results found. However, in practical terms, the article describes two distinct studies, a systematic review on validation studies and a meta-analysis on the prevalence of periodontal disease in pregnant women, the latter making use of the same database obtained in the systematic review. I think this strategy presents some important biases, which I will comment on below. The search strategy was clearly aimed at finding validation studies and not cross-sectional studies that would really express the prevalence of periodontal disease in pregnant women. The same can be applied for all other review procedures, such as the methodological quality assessment tool, QUADAS-2, which is specific for evaluate the risk of bias and applicability of primary diagnostic accuracy studies. Therefore, the review will obviously only include studies with such characteristics, which did not necessarily aim to estimate the prevalence of periodontal disease in pregnant women. Therefore, although the 4 studies that were included are cross-sectional type, they do not present representativeness to illustrate prevalence. A specific systematic review for studies on the prevalence of periodontal disease in pregnant women would certainly find another set of articles. It seems clear that the authors, upon realizing that it would not be possible to carry out the meta-analysis with the accuracy results, decided to seize the opportunity and use the same database to do so with a focus on prevalence. However, I think this strategy is not appropriate and can lead to some misguided conclusions. Among them, the one that states that a “high heterogeneity in the prevalence of periodontitis was observed amongst the included studies” (line 332). It is impossible to state that because, as I highlighted previously, the 4 studies included are not representative of the prevalence of periodontal disease in pregnant women. For the same reason, it is not also possible to state that “the summary measurement of periodontitis prevalence was 39.47% [95% Confidence Interval (95%CI): 9.34%-69.6%]” (line 193). Therefore, I think that the second objective proposed for the study (lines 68 to 69) is not possible to be achieved. I can see two Attachments Attachment Submitted filename: Responses to Reviewers - 04 05 2024.docx https://doi.org/10.1371/journal.pone.0304758.r002
9 May 2024 Decision Letter - Erika Barbara Abreu Fonseca Thomaz, Editor PONE-D-23-35573R1Systematic Review to Evaluate Accuracy Studies of the Diagnostic Criteria for Periodontitis in Pregnant WomenPLOS ONE Dear Dr. Gomes-Filho, 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. After carefully reading this new version, I consider that the decisions made by the authors made the manuscript more appropriate. I only have a small observation regarding the two new paragraphs inserted at the end of the Introduction, as mentioned below. Please submit your revised manuscript by Jun 23 2024 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'. We look forward to receiving your revised manuscript. Kind regards, Erika Barbara Abreu Fonseca Thomaz, Ph.D Academic Editor PLOS ONE Journal Requirements: 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. Additional Editor Comments: Dear authors, Please, I recommend that you remove the names of the authors of the sentence. Leave only the numerical references. This will make the text cleaner and easier for the reader to understand. The various "commas", "semicolons" and "and" throughout the sentence make the text very confusing. I also suggest that the last paragraph of the Introduction (consisting of just 1 sentence of 2 lines) be joined to the previous paragraph, as follows: "Different criteria used for diagnosing periodontitis in pregnant women have been reported (8-15). Which of these is the best criterion to diagnose periodontitis in pregnant women has not been agreed upon; however, they are important to estimate the frequency of maternal periodontitis and, thus, evaluate the effectiveness of preventive or therapeutic procedures and to determine individual risk (16,17). This systematic review evaluated the accuracy of the criteria for diagnosing periodontitis in pregnant women." [Note: HTML markup is below. Please do not edit.] [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. https://doi.org/10.1371/journal.pone.0304758.r003
Revision 2
10 May 2024 Author Response Dear Erika Barbara Abreu Fonseca Thomaz, Ph.D Academic Editor PLOS ONE Provided below are the responses to the reviewers’ comments to the manuscript, “Systematic Review to Evaluate Accuracy Studies of the Diagnostic Criteria for Periodontitis in Pregnant Women” (PONE-D-23-35573R1). Journal Requirements: 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. Response: The reference list was reviewed, as suggested. ADDITIONAL EDITOR COMMENTS Dear authors, After carefully reading this new version, I consider that the decisions made by the authors made the manuscript more appropriate. I only have a small observation regarding the two new paragraphs inserted at the end of the Introduction, as mentioned below. Please, I recommend that you remove the names of the authors of the sentence. Leave only the numerical references. This will make the text cleaner and easier for the reader to understand. The various "commas", "semicolons" and "and" throughout the sentence make the text very confusing. I also suggest that the last paragraph of the Introduction (consisting of just 1 sentence of 2 lines) be joined to the previous paragraph, as follows: "Different criteria used for diagnosing periodontitis in pregnant women have been reported (8-15). Which of these is the best criterion to diagnose periodontitis in pregnant women has not been agreed upon; however, they are important to estimate the frequency of maternal periodontitis and, thus, evaluate the effectiveness of preventive or therapeutic procedures and to determine individual risk (16,17). This systematic review evaluated the accuracy of the criteria for diagnosing periodontitis in pregnant women." Response: As recommended, the two last paragraphs at the end of the Introduction section were rewritten, as follows: “INTRODUCTION … Different criteria used for diagnosing periodontitis in pregnant women have been reported (8-15). Which of these is the best criterion to diagnose periodontitis in pregnant women has not been agreed upon; however, they are important to estimate the frequency of maternal periodontitis and, thus, evaluate the effectiveness of preventive or therapeutic procedures and to determine individual risk (16,17). This systematic review evaluated the accuracy of the criteria for diagnosing periodontitis in pregnant women.” Attachments Attachment Submitted filename: Responses to Reviewers - 10 05 2024.docx https://doi.org/10.1371/journal.pone.0304758.r004
20 May 2024 Decision Letter - Erika Barbara Abreu Fonseca Thomaz, Editor Systematic Review to Evaluate Accuracy Studies of the Diagnostic Criteria for Periodontitis in Pregnant Women PONE-D-23-35573R2 Dear Dr. Gomes-Filho, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, 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, Erika Barbara Abreu Fonseca Thomaz, Ph.D Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0304758.r005
Formally Accepted
9 Jun 2024 Acceptance Letter - Erika Barbara Abreu Fonseca Thomaz, Editor PONE-D-23-35573R2 PLOS ONE Dear Dr. Gomes-Filho, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, 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 customercare@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. Erika Barbara Abreu Fonseca Thomaz Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0304758.r006

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