Consistency of recommendations of clinical practice guidelines in periodontology: a systematic review

Abstract The aim of this systematic review was to evaluate the methodological quality and the consistency of recommendations of clinical practice guidelines (CPGs) in Periodontology. An electronic search was conducted in two databases, MEDLINE and EMBASE, eight CPGs databases, and home pages of scientific societies in Periodontology up to April 2022. Three reviewers independently assessed methodological quality using the AGREE II instrument. In addition, we evaluated the consistency of the recommendations. Eleven CPGs were included, and the topics developed focused on prevention, diagnosis, risk factors, surgical and non-surgical periodontal treatment, antimicrobial therapy, root coverage, and maintenance. We found that the AGREE domains 2 (Stakeholder involvement) and 5 (Applicability) obtained the lowest scores. Domains 1 (Scope and purpose), 3 (Rigor of development) and 4 (Clarity of presentation) obtained the highest scores among the evaluated CPGs. The clinical recommendations for treatment of periodontal diseases were mostly consistent. Overall, the quality of CPGs used in periodontics was high. There was consistency of recommendations in specific fields. These findings may help researchers to promote CPGs focused on different fields of periodontics that have not yet been developed. Furthermore, the clinician will be able to make better clinical decisions.


Introduction
Clinical practice guidelines (CPGs) are comprehensively developed statements designed to assist practitioners and patients make appropriate health care decisions for specific clinical circumstances. 1 The statements contain recommendations based on the best available evidence, e.g., systematic reviews (SR) and synthesis of the published medical literature.However, there may still be topics in dentistry for which no systematic reviews or meta-research are available. 2][5] Periodontal disease is the 11 th most prevalent disease in the world.It may lead to tooth loss and disability, it negatively affects chewing function, aesthetics, quality of life and is even associated with SARS-COV2 infection complications. 6,7Periodontology encompasses prevention, diagnosis, and treatment of diseases of tooth-supporting tissues, besides tissue regeneration and esthetics of these tissues. 8o date, some evidence-based guidelines are available in Periodontics, such as the American Dental Association (ADA) 9 guideline and the recently published European Federation of Periodontology (EFP) 10 guideline, both of which are based on the treatment of periodontal disease.It is important to identify and appraise other clinical practice guidelines produced so far in periodontics.The findings could be helpful in developing new public health policies by adapting existing guidelines or in generating new CPGs in specific fields of periodontics.
It is of paramount importance that CPGs are of sufficient quality to allow the implementation of clear and effective recommendations. 11Poor quality guidelines may compromise clinician's decisions and patient care.There are concerns in medicine and dentistry regarding the quality of CPGs.There is evidence that most CPGs do not adhere to the best methodological design. 12,13Furthermore, some countries adopt and/or adapt existing CPGs to their context, leading to a vast variability in CPG quality 14 .It would be expected that the recommendations would be consistent if the topics of these guidelines are similar, since they should follow the same methodological quality.
The Appraisal of Guidelines Research and Evaluation (AGREE II) tool is a validated instrument used to evaluate the methodological quality and transparency of clinical guidelines. 14,15Appropriate use of AGREE II will result in a correct elaboration of a CPG.
To the best of our knowledge, the methodological quality and the consistency of recommendations of consensus guidelines in periodontology have not been evaluated yet.Thus, the objective of this SR was to assess the methodological quality of CPGs in the field of Periodontology and the consistency of recommendations.A secondary objective was to evaluate the fields of periodontics that have developed CPGs.

Methodology
This systematic review was registered in the PROSPERO database under number CRD42021230566 and was written following the Prisma (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement. 16

Focused question
What is the methodological quality and the consistency of recommendations in CPGs of diagnosis, prevention, maintenance, and treatment of periodontal diseases and conditions?

Exclusion criteria
Proposals of guidelines, consensus statements, expert consensus, workshops, institutional protocols, surgical technique guidelines, and CPGs focusing on implants or peri-implant diseases.

Search strategy
An electronic search was conducted in two databases: the National Library of Medicine (MEDLINE via PubMed) a nd EMBASE (via Ovid).The search strategy included the following combinations of key words that included "All Fields" and "MeSH Terms": (( ((((((((((((((((((periodontitis) OR (periodontal diseases)) OR ("periodontal examination")) OR (probing)) OR (periodontal index)) OR (clinical attachment loss)) OR (clinical attachment level)) OR (periodontal regeneration)) OR (guided tissue regeneration)) OR (root coverage)) OR (Gingivitis)) OR (subgingival curettage)) OR (root planning)) OR (periodontal surgery)) OR (gingivectomy)) OR (gingivoplasty)) OR (gingival diseases)) OR (Periodontium)) OR (Periodontics)) OR (Periodontology)) AND (((("clinical practice guidelines") OR (CPG)) OR ("clinical guidelines"))).The following CPGs websites were also screened up to April 2022: National Institute for Clinical Excellence (NICE), Scottish Intercollegiate Network (SIGN), The New Zealand Guidelines Group, Institute for Health Technology Assessment (Instituto de Evaluación de Tecnología en Salud), Library of Clinical Practice Guides of the National Health System (Biblioteca de Guías de Práctica Clínica del Sistema Nacional de Salud), American Dental Association Center for Evidence-Based Dentistry (ADA), American College of Physicians Clinical Practice Guidelines, Guidelines International Network, National Guideline Clearinghouse.Also, an electronic screening of the grey literature was conducted in the Grey Literature Report and OpenGrey databases, as well as in websites of periodontics scientific societies, identified through FIPP, EFP and AAP, to detect potentially eligible titles.

Selection of CPGs
Two reviewers (TA, NC) conducted a three-stage selection independently and in duplicate (Figure).
The reviewers screened titles and abstracts of search results according to selection criteria.Potential articles and those with insufficient data to make a clear decision, were analyzed in full for the eligibility criteria.Disagreement between the above reviewers was resolved by discussion and consultation with a third author (MAA).The reasons for exclusion at this or later stages were recorded (Table 1).

Assessment of the consistency of recommendations
To d e t e r m i n e t h e c o n s i s t e n c y o f t h e recommendations, two independent reviewers (ALP, LMF) extracted the recommendations from the guidelines related to the diagnosis, prevention, and treatment of periodontal disease.The evaluation was made in the direction and strength of the recommendation.If all the recommendations are for, against, or insufficient, there is consistency.If one recommendation is for and another is against, then there is inconsistency in the direction of the recommendation.When there are several for and several against, the threshold for consistency is that 80% of the recommendations must agree in the direction of the recommendation. 18ssessment of consistency strength is only done if there is consistency in direction.If all the recommendations are strong or weak, then there is consistency in strength.If we have a strong recommendation and a weak recommendation, we say that there is inconsistency in the strength of the recommendation.Insufficient recommendations are considered weak. 18e compared CPGs addressing the same topic to assess the direction of recommendations in guidelines.It was registered as for if the source recommended a diagnostic criterion or a certain treatment; against, if the source explicitly did not recommend the use of a diagnostic criterion or a certain treatment; insufficient, if the source did not specify the topic described, and not reported if the source did not mention that topic.
The recommendation was categorized as strong if the source was rated at the highest level according to the tool used to evaluate the level of recommendation of each CPG, if it was based on the highest level of evidence, or if it used a definitive language that implied the highest level of obligation or expectation to follow the recommendation.The recommendation was considered weak if the source rated the recommendation below the highest level of recommendation, level of evidence, or used nondefinitive language that implied a lower degree of obligation or expectation to follow the recommendation, and different if it was not clear enough to suggest whether the recommendation was strong or weak or if there was not a sufficient level of evidence to make an accurate recommendation. 18

Quality assessment
We used the AGREE II tool to evaluate the methodological quality, accuracy, and reliability of guidelines. 14MAA conducted a pilot test for training and calibration with a sample of randomly selected studies to ensure the accuracy and consistency of data extraction and evaluation.The level of agreement between reviewers was calculated using Cohen's kappa coefficient and interpreted according to Landis and Koch scale. 19hree calibrated authors (TA, NC, and LMF) independently applied the AGREE II tool in triplicate in a standardized format containing the 23 items covering six domains.Items are rated using a seven-point scale ranging from 'strongly disagree' to 'strongly agree', representing the assessor's confidence in whether the guidelines meet the quality of reporting and AGREE II criteria.Between rounds of data evaluation, assessors discussed the outcomes comprehensively to improve the homogeneity of assessment.

Unclear methodology
The overall quality was considered high if CPGs scored 60% in at least three of six AGREE II domains, including Domain 3, moderate if three AGREE II domains scored 60%, except Domain 3, and low if CPGs scored 60% in two or more domains and 50% in Domain 3. 17

Data analysis
We conducted a descriptive analysis to describe the basic features of the data in the included guidelines.The consistency in direction and strength of recommendations related to the prevention, diagnosis and treatment in periodontics were compared and analyzed.Finally, the current prevention/ diagnosis and treatment recommendations for periodontics were summarized and the consistency of recommendations on various diagnostic and therapeutic options were examined.Consistency of recommendations was evaluated through the coincidences of recommendations in the evaluated CPGs.

Data collection
In the initial search, a total of 2376 records were found in the electronic and manual searches.After removing duplicates and screening titles and abstracts, 25 remained for full-text assessment (Figure).Eleven CPGs were finally included in this systematic review.The reviewers showed an almost perfect level of agreement (k = 0.92).The most common reasons for exclusion were guidelines based on consensus meeting, expert consensus, and workshops without the explicit definition of CPGs.
The excluded papers and reasons for exclusion are listed in Table 1.
Eligible CPGs were published from 2011 to 2020, and six were developed in Europe, one in North America, two in Latin America, and two in Asia.Most CPGs were funded by dental scientific societies.Two included non-dental scientific societies in their work team. 20,21The following topics were covered: diagnosis, associated factors, surgical and nonsurgical periodontal treatment, antimicrobial therapy, unitary root coverage, and supportive periodontal therapy (Table 2).
Four different tools were used to assess the level of evidence and grade of recommendation: Scottish Intercollegiate Guidelines Network (SIGN), [22][23][24] Shekelle y cols, 20 American Dental Association (ADA), 9 and Association of the Scientific Medical Societies in Germany (AWMF). 10,21,25ecommendations concerning analysis of medical and dental risk factors, basic periodontal exam (BPE), and oral hygiene instruction (OHI) for prevention and diagnosis of periodontal disease were consistent in direction, but were inconsistent in strength (Table 3).For the analysis of nonsurgical and surgical periodontal treatment, the recommendations were consistent in direction, but inconsistent in strength.The analysis demonstrated that consistency for photodynamic therapy was against the recommendation, while for regenerative surgery, the consistency was in the direction of recommendation.Recommendations for adjunctive antibiotic therapy were inconsistent in direction, as four CPGs recommended adjunctive antibiotics for the treatment of periodontitis 9,[20][21][22] but four other CPGs did not recommend 10,[24][25][26] (Table 4).
We could not evaluate the consistency of the recommendations regarding the diagnosis with periapical or panoramic radiographs, root coverage, and complete oral disinfection therapy since these issues were evaluated by only one guideline.

Quality assessment
According to recommendations, all CPGs scored adequately in at least three of six domains including domain 3 (rigor of development), thus obtaining an overall high-quality score.Domains 1 (Scope and purpose), 3 (Rigor of development), and 4 (Clarity of presentation) obtained the highest score and domain 5 (Applicability) obtained the lowest score (Table 5).

Discusion
In this study, we found 11 clinical practice guidelines, which suggests a lack of worldwide guidelines in a specialty as broad as periodontics.According to the AGREE II instrument, the guidelines produced by multiple institutions and academic organizations were of high quality.
We found guidelines from different continents.We observed a trend for more publications of original guidelines in high-income countries, while in lowincome countries (e.g., Perú and India), CPGs were adapted from other guidelines.A possible explanation for this could be the absence of organizations involved in guidelines elaboration, less support and funding from government agencies for guideline development in low-income countries, and the lower likelihood that guidelines will be published in indexed journals. 12Another reason for adaptations is that most high-quality CPGs are developed for highincome countries with different resources for clinical practice than low-income countries.Difficulties and limitations of adaptation processes include a) lack of knowledge for organizing and planning the resources and time needed for the whole process and b) lack of methodological expertise.Considering the above reasons, CPG adaptation is an alternative in low-income countries.
Although it seems that the overall quality of guidelines has improved over the past decades, 27 whereas the report of the type and involvement of stakeholders seem to be especially poor.The report on stakeholder participation in the design, development, and implementation of CPG demonstrates transparency and endures that an agreed and/or published stakeholder participation plan has been followed, and explains and justifies any changes made to the stakeholder participation plan as a result of adaptive management. 11For example, for the development of a CPG about  importance in providing proper guidance for clinical treatments.
The constant scientific advance makes it imperative that CPGs are updated.This critical issue has been recently addressed by the living systematic reviews, where evidence is continuously updated and incorporated as soon as available in the literature through a process of continuous surveillance. 28,29The validity of each recommendation and of the CPG is determined by the methodological quality and the  transparency of its development and by the "living evidence" on which it is based.As suggested by Martínez Garcia et al., 30 waiting more than three years to review a guideline may be too long because the recommendations may already be outdated by the time of guideline publication.Based on this, we suggest that the CPGs included in this study should be updated in a period of less than five years.
The objective of a CPG is to provide evidence-based recommendations that help clinical decision-making.In this study, we found many useful recommendations for the management of periodontal patients.This SR recommends the following clinical protocol when examining a new patient based on the diagnostic criteria: a) Identifying all patients suspected of having periodontitis; b) Confirming the diagnosis of periodontitis; c) Staging the periodontitis case; and d) Grading the periodontitis case. 31egarding non-surgical periodontal treatment, there was consistency in the recommendations, which can be summarized in: a) Professional instructions for good oral hygiene should be provided to reduce plaque and gingivitis; b) Re-enforcement of oral hygiene instructions may provide additional benefits; c) Manual or electric tooth brushing are recommended as a primary means of reducing plaque and gingivitis; d) When gingival inflammation is present, the use of interdental brushes should be professionally taught to patients; e) Professional mechanical plaque removal is recommended, which consist of interventions aimed at removing supragingival plaque and calculus and plaqueretentive factors; and 6) Risk factors such as smoking and diabetes should be controlled. 32,33hen non-surgical periodontal treatment does not have a favorable response, the next step, according to consistent recommendations, can be summarized as: 1) Access flap periodontal surgery; 2) Resective periodontal surgery, and 3) Regenerative periodontal surgery 32,33 .
To our knowledge, the consistency of the CPG recommendations in dentistry has not been previously described.It is interesting to note that, unlike clinical guidelines in medicine, 18,34,35 the recommendations of clinical guidelines on periodontology were consistent in direction.The main controversy and the only inconsistency was in the use of adjuvant antibiotic therapy for the treatment of periodontal disease.This could be due to the wide range of drugs and doses used in periodontics.In addition, this lack of coherence may be mostly due to the different definitions of periodontal disease used by each guide, different publication dates, different methods of selection and interpretation of the evidence, and different preferences and indications.
In periodontal research, researchers have used different definitions for periodontal disease.For standardization purposes, the periodontal diagnosis should be recorded following the latest classification of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. 36In the current classification system, periodontal health is defined as the absence of inflammation and absence of attachment and bone loss from previous periodontitis.A case of clinical gingivitis is defined as the presence of gingival inflammation as assessed by bleeding on probing at ≥10% of the sites and absence of detectable attachment loss due to previous periodontitis.A periodontitis case is defined as loss of periodontal tissue support, which is defined as the presence of bone loss or interproximal loss of clinical attachment measured by radiographic examination. 10We recommend that guidelines update their recommendations according to the new classification of periodontal diseases 36 to avoid confusion when interpreting the recommendations.
Although there was a general consistency in direction, CPGs lack consistency in the strength of recommendations.This may be related to the lack of high-quality scientific evidence on some topics in periodontology, especially in primary studies reported in different systematic reviews, which are often used as sources of information to issue recommendations. 37espite the different CPGs in periodontology, there may be barriers to their application in all populations.Many potential factors may limit the adoption of evidence, including CPGs, into clinical practice, such as knowledge and awareness of the guidelines, individual/professional barriers, cognitive factors, attitudes and social barriers, and organizational and economic context (e.g., culture of the network, leadership, financial arrangements, capacity, and resources). 38imitations of this systematic review include potential selection bias, since there is no specific registration center for guidelines in dentistry that could help us perform a more comprehensive search.Only CPGs published in journals and online databases were included.Furthermore, CPGs published in the form of books or government documents were not analyzed.This could limit the comprehensiveness of grey literature search.Likewise, it was not possible to make comparisons between guideline recommendations due to the different instruments used to grade the recommendations.We strongly believe that CPGs should be developed using validated methodology (the use of GRADE is recommended) and updated regularly.
This study was the first attempt to assess the methodological quality of CPGs on periodontics using the AGREE II tool.Only 11 guidelines met the inclusion criteria and were included.Considering the high prevalence of periodontitis and the different topics covered by periodontics, the number of guidelines that were eventually included in this study was lower than expected.This systematic review demonstrated that the AGREE II tool can serve as an adequate reference for the development of CPGs on Periodontics.The knowledge on the quality and applicability of CPGs may help clinicians make the right clinical decisions.

Conclusion
The quality of CPGs in periodontics was high.Furthermore, there was consistency in recommendations for the diagnosis and treatment of periodontal diseases.Developers of future CPGs should fully disclose the involvement of stakeholders and standardize the clinical diagnosis criteria according to the current classification system.

Table 1 .
Excluded articles and respective reasons.

Table 2 .
Characteristics of the included CPGs.

Table 3 .
Consistency analysis of prevention and diagnosis recommendations of periodontics guidelines.
*NR: not reported; SIGN: Scottish Intercollegiate Guidelines Network; Shekelle, Modified Shekelle scale; ADA: American Dental Association; AWMF: Association of the Scientific Medical Societies in Germany .

Table 4 .
Consistency analysis of periodontal treatment recommendations of periodontic guidelines.

Table 5 .
AGREE II results.