Oral health in Brazil: What were the dental procedures performed in Primary Health Care?

This cross-sectional study aims to describe the primary dental care procedures performed by Oral Health Teams (OHTs), adhering to the third cycle of the "National Program for Improving Access and Quality of Primary Care" (PMAQ-AB) in Brazil. A descriptive analysis was performed through 26 dental procedures, including spontaneous, preventive, restorative/prosthetic and surgical procedures, and actions of cancer monitoring. Each conducted procedure assigned a score to the OHT, the final score being the sum of the number of procedures performed by the OHTs. These scores were then compared among the geographic regions of the country. Most OHTs perform basic dental procedures, such as supragingival scaling, root planning and coronal polishing (98.1%), composite filling (99.0%), and permanent tooth extraction (98.6%). The frequency related to dental prosthesis and monitoring of oral cancer decreased. Only 12.9% of the OHTs carries out biopsies, 30.9% monitor patients undergoing biopsy, 15.1% carry out impression for prostheses, and 13.6% carry out prostheses' installation. The scores reveal that OHT's performed, on average, 19.45 (±3.16) dental procedures. The OHTs in the South, Southeast, and Northeast had a higher number of primary dental procedures, while the teams in the North and Midwest performed, on average, fewer procedures. The Brazilian regions with the highest dental need have the lowest number of dental procedures. It is necessary to increase the range of procedures offered by OHT and reduce regional inequalities, adapting to the needs of the population in order to achieve comprehensive oral health.

Introduction

Primary Health Care (PHC) in Brazil is considered the entry point for the user of the Brazilian National Health System (SUS in Portuguese). The evaluation of this level is strategic to identifying the persistent fragilities that hinder its organization and operation towards the desired resolubility for the service [1].

To reorganize oral health actions in primary health care, the Brazilian Ministry of Health proposed the inclusion of Oral Health Teams (OHT) in the Family Health Strategy (FSH). FHS is the starting point for the application of the principles of PHC in Brazilian oral health. The result was the expansion of access to dental care in Brazil, [2,3] with improved dental facilities in the units and a better qualification of professionals [4]. In Brazil, there are currently 27,564 OHTs distributed throughout 5,032 municipalities [5].

The expansion of access to oral health has revealed the need to evaluate services in order to improve the quality of care provided to the population. Issues related to the quality of management and team practices assumed a more relevant position while it reduced the concern only with the expansion of services [6].

In 2011, the Brazilian Ministry of Health (MofH) launched the National Program for Improving Access and Quality of Primary Care (PMAQ-AB in Portuguese) [7]. The PMAQ-AB has the aim to increase access and improve the quality of health care, providing a national, regional, and local quality standard. This program is the largest health service evaluation program ever instituted in the country [8].

The PMAQ-AB is organized in three phases; adhesion and agreement, certification and re-agreement, and one strategic transverse axis of development [9], forming continuous evaluation cycles. In 2018, the 3rd cycle was finished. A significant increase was observed in the participation of OHTs over the years in PMAQ-AB. In the 1st (2011–2012), 2nd (2013–2014), and 3rd (2017–2018) cycles, the number of OHTs assessed were 12,403; 18,114, and 25,090, respectively.

After three cycles of PMAQ-AB, and approximately seven years of evaluation of dental services, studies have evaluated the procedures performed at PHC by OHTs. Reis et al. [10] and Neves et al. [11], using data from the 1st cycle, showed that most OHTs performed emergency, preventive, restorative and surgical procedures; however, for oral cancer and prosthetic procedures, a failure was found in both supply and execution. In the 2nd cycle, an improvement was observed in the external evaluation instrument with a greater number of variables related to the structure and work process [12]. However, Mendes et al. [13] revealed that failures related to the prevention and detection of oral cancer and the manufacture of prostheses still persisted. The evaluation of the 3rd cycle may indicate if there were advances in the provision of PHC procedures in oral health and changes in the performance of the OHTs, providing data for the improvement and development of services.

Brazil has a territory with a continental dimension and is divided into five regions: South, Southeast, Midwest, Northeast and North. This territorial extension leads to geographical socioeconomic inequalities with impact on health services and consequently on the population´s health [14].

The present study aims to describe the procedures of primary dental health care performed by OHTs that adhered to the 3rd cycle of the PMAQ-AB among Brazilian regions. The null hypothesis of this study is that there is no difference in the PHC procedures performed by OHT’s among the five Brazilian regions.

Methods

This study was approved by the Research Ethics Committee of Universidade Federal de Minas Gerais (UFMG), logged under protocol number 02396512.8.0000.5149. No participant was identified at any stage of this study, as it dealt with secondary and public data of the Brazilian MofH. This is a cross-sectional descriptive study that used secondary data from the third cycle of the PMAQ-AB, related to the procedures performed by OHTs that complied with the program.

In the 3rd cycle of PMAQ-AB, which occurred between 2017 and 2018, 25,090 OHTs were assessed. Of these, 2,097 (8.4%) were disqualified by the PMAQ-AB evaluation criteria, as they did not follow the program’s recommendations, such as an adequate oral health surveillance system and the presence of the dentist and dental equipment in the PHC unit, resulting in a sample of 22,993 OHTs.

The data were collected during the external evaluation phase, which is characterized by a visit of program evaluators to the PHC units. An instrument, developed for this purpose by MofH in partnership with Brazilian teaching and research institutions, was used to interview the dental professionals and was applied by a trained team. At the time of the interview, the documents were verified to check the quality standards established according to norms, protocols, principles, and guidelines for the organization of actions and practices. The answers were recorded on tablets, using a program developed for PMAQ-AB. After data collection, the partner institutions performed the data validation and sent the results to the MofH’s central database.

For this study, data were obtained from the interview conducted with the OHT and verification of documents in the PHC, through Module VI—Oral Health Professional Interview; section VI.7 - Organization of team’s agenda and actions offered and section VI.11 - oral cancer care. Questions about 26 procedures performed by OHTs, mostly dichotomous (yes/no), were evaluated. The questions included response to spontaneous demand (subsection VI.7.4); preventive, restorative, surgical and procedures related to the manufacture and installation of dental prostheses (subsection VI.7.5); and actions of cancer monitoring (subsections VI.11.1, VI.11.2, VI.11.3, VI.11.6, VI.11.6/1, VI.11.7, VI.11.9).

Each procedure performed attributed a score to each OHT, with the final score being the sum of the quantity of procedures performed by each OHT (from 0 to 26 points). For example, if an OHT score was 18, it meant that this OHT carries out 18 of the 26 procedures evaluated. After this, the OHTs were divided into five geographic regions (North, Northeast, Midwest, South, and Southeast) in Brazil, and the score for each region was calculated.

The data were analyzed descriptively, by frequency, using the Statistical Package for Social Sciences (SPSS), version 25.0 (IBM SPSS Statistics for Windows, Armonk, NY).

Results

The descriptive analysis showed that 98% of OHTs guarantee the scheduling of appointments and the spontaneous meeting of demand. Table 1 shows the organization of the spontaneous demand and the frequency of 26 primary dental care procedures performed by the OHTs, including preventive, restorative/prosthetic, surgical and actions of cancer monitoring. Most of OHTs perform basic procedures, such as supragingival scaling, root planning, and coronal polishing (98.1%); composite fillings (99.0%), and permanent tooth extractions (98.6%). However, it was observed that the frequency decreased when asked about procedures related to dental prostheses. Only 15.1% of the OHTs perform impressions for prostheses and 13.6% conduct prostheses’ installations. With regard to actions for cancer prevention, most of the OHTs perform actions to prevent and diagnose oral cancer (94.9%), including medical advice on tobacco use (93.2%) as well as on alcohol and other drugs (91.7%). This percentage decreased slightly when ask about the active search for potentially precancerous lesions and cases in the population (80.5%). In addition, most OHTs did not perform biopsies (12.0%) and did not monitor patients undergoing biopsy to evaluate the results of the examination (30.9%).

Table 1

Basic dental procedures performed by oral health teams, Brazil, 2017–2018.

Variables	Yes (%)
Response to spontaneous demand
Urgency care (drainage of abscess, suture of trauma injuries, access to dental pulp, pulpotomy, treatment of alveolitis, initial treatment of traumatized tooth)	22,298 (97.0)
Prescription of medicines	22,360 (97.2)
Medical advice	22,253 (96.8)
Preventive and periodontal procedures
Fluoride application	22,651 (98.5)
Ionomer sealant application	20,102 (87.4)
Supragingival scaling, root planning, and coronal polishing	22,566 (98.1)
Subgingival scaling, root planning, and coronal polishing	20,117 (87.5)
Restorative/Prosthetic procedures
Composite filling	22,767 (99.0)
Amalgam filling	18,450 (80.2)
Ionomer filling	22,310 (97.0)
Impression for prostheses	3,471 (15.1)
Prostheses installation	3,114 (13.6)
Prostheses cementation	5,785 (25.2)
Surgical procedures
Deciduous tooth extraction	22,812 (99.2)
Permanent tooth extraction	22,680 (98.6)
Ulotomy/ulectomy	18,803 (81.8)
Cancer monitoring
Does the OHT carry out actions to prevent and diagnose oral cancer?	21,817 (94.9)
Medical advice on tobacco use	21,439 (93.2)
Medical advice on the use of alcohol and other drugs	21,076 (91.7)
Medical advice on the prevention of exposure to solar radiation	19,929 (86.7)
Active search for potentially precancerous lesions and cases in the population	18,498 (80.5)
Systematic examination of oral mucosa	20,468 (89.0)
Does the OHT perform biopsies to diagnose oral cancer?	2,769 (12.0)
Does the OHT have a record of patients with suspected oral cancer who were biopsied or referred to the referral service?	7,831 (34.1)
Does the OHT have a document that proves this?	6,891 (30.0)
Does the OHT monitor patients undergoing biopsy to evaluate the results of the examination?	7,109 (30.9)
After the user’s reference for treatment, does the OHT follow up and monitor the continuity of care?	14,645 (63.7)

Table 2 shows the scores of basic procedures that OHT’s performed, which was, on average, 19.45 (±3.16) dental procedures (0–26 procedures). Regarding the average number of procedures performed according to the Brazilian regions, it was observed that the OHTs in the South, Southeast, and Northeast had a higher number of primary dental procedures, while the teams in the North and Midwest, on average, performed fewer procedures.

Table 2

Scores of dental procedures performed by OHTs in Brazilian geographic regions, Brazil, 2017–2018.

Brazilian Regions	OHT	%	Mean	Minimum	Maximum	Median
North	1,916	7.6	16.91	2	25	18
Northeast	11,132	44.4	19.46	0	26	20
Midwest	2,026	8.1	18.8	2	26	19
Southeast	6,751	26.9	20.16	0	26	20
South	3,265	13.0	19.84	3	26	20

Discussion

The descriptive analysis revealed that most OHTs perform basic dental procedures, as recommended by the MofH, including emergency, preventive, restorative and surgical procedures. Regarding dental prostheses, few teams perform impressions, installations, and cementation of dental prostheses at the PHC. Although most teams perform actions to prevent and diagnose oral cancer, few teams perform biopsies of suspected cases, keep adequate records, or monitor patients undergoing biopsy to evaluate the results of the examination. In addition, the results revealed differences between Brazilian regions in relation to the procedures performed by the teams, invalidating the null hypothesis.

Despite changes in data collection methodology in the 3rd cycle, our findings are similar to previous 1st cycle [10,11] and 2nd cycle [13,15,16] studies. The highest perform of basic oral health procedures by OHTs, like emergency, preventive, restorative and surgical procedures, can be explained by the improvement in the infrastructure of dental offices and working conditions, and higher qualification of professionals due to the increase in investments in oral health, provided by the National Oral Health Policy [17]. The work process of oral health care is affected by legislation of the country [18], and access to care is influenced by the social determinants of health [19]. The delivery of health promotion strategies at the population level has shown a great impact on reducing the prevalence of oral diseases [19,20]. Health systems that strength preventive and tooth-preserving strategies, inclusive of adults, progress faster and perform better in respect of effectiveness and efficiency [20]. Over the past several decades, Netherlands passed by changes in the funding of oral health care aiming to reduce the need for curative treatment and more emphasis on prevention of dental diseases. These changes improved oral health, especially, Dutch adults [18]. Although progress has been made in the offer and organization of services, access has been expanded and oral health actions have been qualified, considering that, 17 years after the launch of the National Oral Health Policy, there are still difficulties to implement basic premises, such as completeness and access to secondary care and reduction of regional inequalities [21]. So, more political actions are needed to reduce inequalities, to promote health [19], and to improve the work process of OHTs.

Our results showed that most OHTs provide spontaneous demand care, together with emergency care, prescription of medication, or specialized guidance. Despite the advances in oral health services in recent years [17], the population still has a repressed demand for dental treatment, which leads to the search for emergency care [22]. Considering the current moment of the COVID-19 pandemic, when most routine dental care is not available, an increase in repressed demand is expected, causing more patients to seek out emergency dental care [23]. In this sense, it is expected that OHTs will be able to meet the demand, since they claim to be performing these types of procedures. In this sense, the emergency dental care must be performed with a minimal use of slow and high-speed handpieces in order to avoid aerosols, prioritizing the use of manual instruments. In addition, the team must also have all personal protective equipment ’s recommended and indicated by the relevant health authorities [24], demonstrating the importance of also having a well-structured service in terms of instruments and inputs.

Regarding preventive and periodontal procedures, it was observed that OHTs perform subgingival scaling less frequently. It is important to stress that this procedure, together with the correct diagnosis and oral hygiene instructions, is recommended as a periodontal preventive treatment, which is able to solve most demands, thus avoiding referral to secondary care [25].

It is important to note that the prevalence of tooth loss, which leads to the need for prosthetic rehabilitation, is still high in Brazil [26]. The findings on the manufacture and installation of dental prostheses show the failure in this process, although OHTs are required to offer this type of service. Reis et al. [10] Mendes et al. [13] and Cunha et al. [15] analyzing data of 1st and 2nd cycles of PMAQ-AB, also reveal failures in the procedures related to the offer and manufacture of dental prostheses. This demonstrates that there was no significant progress in this period. Prosthesis procedures require infrastructure and qualified labor for the service. The availability and distribution of regional prosthesis laboratories has not followed the epidemiological need of the population, and the growth of prosthesis production has been discrete in recent years [16]. This failure reveals a gap in the completeness of care, as it does not provide the complete treatment necessary to meet the user needs [21]. Besides that, the organizational factors and human resources has an essential role of in the provision of dental prosthesis in primary dental care in Brazil. The OHTs that are more likely to perform dental prostheses have professionals admitted through public examinations and involved in permanent education, with a more organized work process and that receive more support from municipal management [27].

Regarding oral cancer actions, the results reveal that, although oral cancer OHTs report procedures for prevention and early detection, few teams perform lesion biopsies. Results similar were founded by Galante et al. [28] using data of second cycle of PMAQ-AB. The presence of the dentist in primary care, had a positive impact on campaign actions, follow-up, referral to specialists, and registration of suspected cases of oral cancer However, actions to perform lesion biopsies are done on secondary care. This is a worrisome fact due to the high mortality rate of the disease [29]. The active search for lesions, visual examination for oral cancers during regular dental consultations, and biopsy of suspected lesions may be able to reduce mortality from oral cancer [30], mainly when these actions are directed toward alcohol and tobacco users, since these are the main risk factors for oral cancer, which is linked to more than 80% of the cases [31]. Early diagnosis is crucial for patient survival, since survival rates for oral cancer are associated with the stage of the tumor in diagnosis, as well as the availability and quality of treatment provided [32]. In addition, the knowledge and experience of health professionals also plays a key role; monitoring post-treatment patients prevents recurrence and improves patients’ quality of life [33], since the treatment of an oral cancer does not necessarily mean a cure. Nevertheless, our results revealed that OHTs do not continuously monitor oral cancer cases. Due to its structure and organization, the PHC is an excellent strategy for screening oral cancer cases. The access of community agents to patients’ homes can help in early detection and follow-up of suspected and confirmed cases [10]. Therefore, it is important to qualify professionals and encourage campaigns for systematic examinations of oral mucosa as a way to qualify the diagnosis of potentially malignant lesions in a more frequent manner than that reported in our findings.

Regarding the scores obtained in this study, better rates were observed in the Southeast and South regions, followed by the Northeast region. The North region presented the worst results, showing important differences between the regions. This difference can be explained by the level of development of these regions. Despite the growth of the Municipal Human Development Index (HDI), which has proven to be more accelerated in recent years in Brazil, with improvement in the indices of all regions, the North and Northeast still have the lowest HDI in the country. The highest HDI is recorded in the Southeast region (0.766), followed by the Midwest (0.757) and South (0.754) regions [34]. From 2004, with National Oral Health Policy, an increase in the oral health incentive was observed for municipalities with lower HDIs. This policy benefited the North and Northeast regions, with increased access and improved infrastructure. However, the impact of this policy on service use was not enough, since the proportion of procedures is still higher among regions with higher HDIs [28,35].

In recent years, Brazil has expanded oral health service coverage and there have been changes in the epidemiological profile of oral diseases, but efforts are still needed to reduce inequalities in access to services, in improved and qualified care, as well as in the use epidemiology for planning oral health actions [11,19]. The Northeast region has a higher number of OHTs in the country, while the North region presents the worst HDI of the country and the lowest number of OHTs. However, this number does not reflect a higher score of dental procedures performed by OHTs when compared to the Southeast and South regions.

Therefore, the results showed that only the number of OHTs does not necessarily translate into better care for the population. Other factors, such as different socio-demographic conditions, repressed demand for dental treatment, and the organization of the dental service may interfere in the offer of the service to the population.

This study’s results are limited due to the use of a secondary database, based on dentist reports, and by the fact that PMAQ-AB is a pay-for-performance program. Nevertheless, the need to improve and expand the supply of prostheses and actions related to the early diagnosis and monitoring of oral cancer is evident. Despite these limitations, our study is based on national data, from the largest PHC evaluation program ever conducted in Brazil in its third cycle [8], which reinforces the relevance of our results.

It is necessary to increase the range of procedures offered by OHTs and reduce regional inequalities, adapting them to the needs of the population in order to achieve comprehensive oral health care. Health assessments can provide an overview that allows one to trace ways to boost access to oral health.

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11 Aug 2021

PONE-D-21-14792

Oral health in Brazil: what were the dental procedures performed in Primary Health Care?

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Reviewer #1: The data were very old (2017-2018) and These data in present study is not contemporary, so these results don't reflect the current oral health requirements in Brazil.

Material method

Explain 5 macro region, mention which city in five region.

Reviewer #2: Thank you for submitting you manuscript.

The manuscript presents good data about Brazilian national public program for oral health services. Public health professionals can use these valuable data in countries where they provide dental public health services.

Manuscript is organized and present sound interpretation of data, but needs some language editing and review to avoid confusion and make it more clear and readable. Especially for some terminologies that have been translated to English terms.

Here are some examples (in bold and underline):

69 three phases: accession and contractualisation, certification and recontratualisation, and a transversal strategic axis of development

78 OHTs performed individual preventive, restorative, and surgical procedures and

emergencies; however

132 performed by the OHTs, including preventive, restorative, surgical, and prosthetic

133 procedures and cancer monitoring.

142 and cases in the community (80.5%). In addition, most OHTs did not realize biopsies

Also in Discussion:

The great accomplishment of basic oral health procedures by OHTs can be explained by the improvement in the infrastructure of dental offices, improvement in working conditions and higher qualification of professionals due to the increase in investments in oral health, provided by the National Oral Health Policy [16].

Comment: if you can elaborate more and exaplain what do you mean by the great accomplishment? Is it improvement in provided services compared to the 2nd cycle? Maybe mention some data from 2nd cycle to make it clear.

In this sense, the emergency dental care must be performed with a minimal use of high

speed handpieces in order to avoid aerosols resulting from the use of manual instruments.

Comment : you mean headpiece instrument?

**********

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24 Sep 2021

We would like to thank the reviewers for the excellent suggestions in order to improve our paper. The responses of each comment are listed below. All edition and revisions made are highlighted by red in the new file.

Reviewer #1:

The data were very old (2017-2018) and these data in present study is not contemporary, so these results don't reflect the current oral health requirements in Brazil.

Response: The National Program for Improving Access and Quality of Primary Health Care (PMAQ-AB) is the largest health service evaluation program instituted in Brazil. The program ended in 2018 after three evaluation cycles. This study is based on national data, from the largest PHC evaluation program ever conducted in Brazil. These data refer to the last cycle of the PMAQ. Until this moment, there is no health service evaluation program under development in the country. So, nowadays, these are the data available that represents Brazilian national public program for oral health services, which reinforces the relevance of these results.

Material method

Explain 5 macro region, mention which city in five region.

Response: Thanks for the observations. We agree with the reviewer and the explanation about the Brazilian regions was included in Introduction section (7th paragraph, 84 line; The differences between the regions are discussed from 230 Line in Discussion.

Reviewer #2:

Thank you for submitting you manuscript. The manuscript presents good data about Brazilian national public program for oral health services. Public health professionals can use these valuable data in countries where they provide dental public health services.

Manuscript is organized and present sound interpretation of data, but needs some language editing and review to avoid confusion and make it more clear and readable. Especially for some terminologies that have been translated to English terms.

Here are some examples (in bold and underline):

69 three phases: accession and contractualisation, certification and recontratualisation, and a transversal strategic axis of development

Response: Thanks for the observations. We agree with the reviewer. The text was rewritten and the change was made to “The PMAQ-AB is organized in three phases; adhesion and agreement, certification and re-agreement, and one strategic transverse axis of development...”

78 OHTs performed individual preventive, restorative, and surgical procedures and emergencies; however

Response: Thanks for the observations. We agree with the reviewer. The text was rewritten and the change was made to “OHTs performed emergency, preventive, restorative and surgical procedures; however…”

132 performed by the OHTs, including preventive, restorative, surgical, and prosthetic 133 procedures and cancer monitoring.

Response: Thanks for the observations. We agree with the reviewer. The text was rewritten and the change was made to “performed by the OHTs, including preventive, restorative/prosthetic, surgical and actions of cancer monitoring.”

142 and cases in the community (80.5%). In addition, most OHTs did not realize biopsies

Response: Thanks for the observations. We agree with the reviewer. The text was rewritten and the change was made to “and cases in the population (80.5%). In addition, most OHTs did not perform biopsies”

Also in Discussion:

The great accomplishment of basic oral health procedures by OHTs can be explained by the improvement in the infrastructure of dental offices, improvement in working conditions and higher qualification of professionals due to the increase in investments in oral health, provided by the National Oral Health Policy [16].

Comment: if you can elaborate more and exaplain what do you mean by the great accomplishment? Is it improvement in provided services compared to the 2nd cycle? Maybe mention some data from 2nd cycle to make it clear

Response: Thanks for the observations and the opportunity to clarify this point. The better performance of OHTs, in basic procedures, is due to a greater investment in oral health, after the National Oral Health Policy. The text was rewritten: “The highest perform of basic oral health procedures by OHTs, like emergency, preventive, restorative and surgical procedures, can be explained by the improvement in the infrastructure of dental offices and working conditions, and higher qualification of professionals due to the increase in investments in oral health, provided by the National Oral Health Policy [17].”

In this sense, the emergency dental care must be performed with a minimal use of high speed handpieces in order to avoid aerosols resulting from the use of manual instruments. Comment: you mean headpiece instrument?

Response: Thanks for the observations and the opportunity to clarify this point. The text was rewritten:” In this sense, the emergency dental care must be performed with a minimal use of slow and high-speed handpieces in order to avoid aerosols, prioritizing the use of manual instruments.”

Submitted filename: Response to reviewers.docx

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11 Nov 2021

Oral health in Brazil: what were the dental procedures performed in Primary Health Care?

PLOS ONE

Dear Dr. Martins,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Dec 26 2021 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,

Gaetano Isola, 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:

Please revise in accordance to reviewer's 3 comments before any further assessment of the manuscript.

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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 #2: All comments have been addressed

Reviewer #3: 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 #2: Yes

Reviewer #3: Yes

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

Reviewer #2: Yes

Reviewer #3: I Don't Know

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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 #2: Yes

Reviewer #3: 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 #2: Yes

Reviewer #3: 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 #2: (No Response)

Reviewer #3: This is a very interesting article.

I would suggest the authors to search if other similar articles were performed in other countries.

In my opinion the materials and methods chapter has to be better explained.

Please also in the discussion chapter try to find more recent published articles.

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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 #2: Yes: Ziyad Allahem

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.