ODOVTOS-International Journal of Dental Sciences

ODOVTOS
LITERATURE REVIEW DOI: 10.15517/IJDS.2022.48547

Received:
9-VII-2021
Use and Effectiveness of Propolis on Chronic Periodontitis:
Accepted:
a Systematic Review
10-IX-2021

Published Online: Uso y efectividad del propóleo en periodontitis crónica:

1-X-2021
una revisión sistemática

Irma A. Fraire-Reyes DDS¹; César Gaitán-Fonseca DDs, MSc, PhD²;

Óscar Cepeda-Argüelles DDs, MSc, PhD³; Vicente Esparza-Villalpando DDS, MSc, PhD⁴;
Luis Aguilera-Galavíz BSc, MSc, PhD⁵; Carlos Bermúdez-Jiménez DDS, MSc, PhD⁶

1.Maestría en Ciencias Biomédicas, Área de Ciencias de la Salud, Universidad Autónoma de

Zacatecas “Francisco García Salinas”, Zacatecas, Zac., México.
https://orcid.org/0000-0003-3456-8676
2. Unidad Académica de Odontología, Universidad Autónoma de Zacatecas “Francisco García Salinas”,
Zacatecas, Zac., México. https://orcid.org/0000-0001-6452-2578
3. Unidad Académica de Odontología, Universidad Autónoma de Zacatecas “Francisco García Salinas”,
Zacatecas, Zac., México. https://orcid.org/0000-0003-1853-9461
4. Facultad de Estomatología, Universidad Autónoma de San Luis Potosí, San Luis Potosí, S.L.P.,
México. https://orcid.org/0000-0002-2047-3388
5. Unidad Académica de Odontología, Universidad Autónoma de Zacatecas “Francisco García Salinas”,
Zacatecas, Zac., México. https://orcid.org/0000-0002-1513-4971
6. Unidad Académica de Odontología, Universidad Autónoma de Zacatecas “Francisco García Salinas”,
Zacatecas, Zac., México. https://orcid.org/0000-0001-7503-350X

Correspondence to: Dr. Carlos Bermúdez-Jiménez - [email protected]

ABSTRACT: The aim of this study was to determine the effect of propolis on non-
surgical periodontal therapy in patients with chronic periodontitis (CP) as it appears in
the recent literature. Propolis is a natural and biocompatible resinous substance that
has shown, by means of several scientific studies, to possess medicinal properties
such as antimicrobial, healing, anesthetic, anti-inflammatory, and analgesic, among
others. There are several studies that have reported the use of propolis as a non-
surgical treatment of CP, its comparison with other antimicrobials, and the improvement
of clinical and microbiological parameters with scaling and root planing (SRP). A
bibliographic search was conducted in the PubMed, Google Scholar, Web of Science,
and Science Direct databases up to 2021. The results showed that there are very few
reports focused on clinical studies; however, according to the analyzed data, propolis
could be a good adjuvant for the treatment of patients with chronic periodontitis
compared to the conventional treatment (SRP).

FRAIRE-REYES I.A., GAITÁN-FONSECA C., CEPEDA-ARGÜELLES O., ESPARZA-VILLALPANDO V., AGUILERA-GALAVÍZ L., BERMÚDEZ-JIMÉNEZ C.,
2022: Use and Effectiveness of Propolis on Chronic Periodontitis: a Systematic Review.-ODOVTOS-Int. J. Dental Sc., 24-1 (January-April): 32-43.
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 Fraire-Reyes et al: Use and Effectiveness of Propolis on Chronic Periodontitis: a Systematic Review

KEYWORDS: Propolis; Periodontal disease; Periodontitis; Dentistry; Antibacterial;

Antimicrobial.

RESUMEN: El objetivo de este estudio fue determinar el efecto del propóleo sobre la
terapia periodontal no quirúrgica en pacientes con periodontitis crónica (PC) en la
literatura reciente. El propóleo es una sustancia resinosa natural y biocompatible que
ha sido demostrado a través de varios estudios científicos que posee propiedades
medicinales como antimicrobianas, cicatrizantes, anestésicas, antiinflamatorias,
analgésicas, entre otras. Existen varios estudios que han reportado el uso del propóleo
como tratamiento no quirúrgico de la PC y su comparación con otros antimicrobianos
y la mejora de los parámetros clínicos y microbiológicos con el raspado y alisado
radicular (SRP). Se realizó una búsqueda bibliográfica en las bases de datos directas
de PubMed, Google Scholar, Web of Science y Science hasta el 2021. Los resultados
muestran que existen muy pocos reportes enfocados a estudios clínicos, sin embargo,
según los datos analizados, el propóleo podría ser un buen adyuvante para el
tratamiento de pacientes con periodontitis crónica en comparación con el tratamiento
convencional (SRP).

PALABRAS CLAVE: Propóleo; Enfermedad periodontal; Periodontitis; Odontología;

Antibacteriano; Antimicrobiano.

INTRODUCTION dicyclic, and derived monoterpenes), and by phenolic

compounds (cinnamic acid, p-coumaric acid,
Propolis is a viscous, resinous, aromatic caffeic acid, ferulic acid, and derived acids (6).
substance that has different colors ranging between There are various types of propolis, depending
brownish-green and coffee, depending on its on the plant species from which they are
origin and age. It is hard and brittle on contact obtained but, in particular, 50-60% of propolis is
with cold and when ihot, it becomes soft and composed of resins and balms (including phenolic
sticky and is also known as bee glue (1). It is compounds), 30-40% of waxes and fatty acids,
obtained from the branches of resinous trees 5-10% of essential oils, 5% of pollen, and about
and from the leaves of certain plants (2). The 5% of other substances including amino acids,
main source of propolis is Salicaceae (poplar micronutrients, and vitamins (thiamin, riboflavin,
and willow trees), whose chemical composition pyridoxine, vitamin C, and vitamin E) (7,8). Propolis
is very complex; about 19 components have been extracts have an application in treating diseases
classified, with some of these substances belonging due its anti-inflammatory (9), antioxidant (10),
to the flavonoid group, isovanieline, resins, etc. antibacterial (11), antifungal (12), antiulcer (13),
All of these are characterized by their biological anticancer (14), and immunomodulatory properties
activity (3-5). The antibacterial activity of propolis is (15). The therapeutic application of propolis that has
mainly conferred by flavonoids (flavones, flavonols, been most studied is its antibacterial action, which
flavanones, flavanonol, chalcones, dihydrochalcones, is made up of flavonoids, the main component of
isoflavones, isodihydroflavones, flavanos, isoflavans, propolis, by enhancing the antibacterial, antiviral,
and neoflavonoids) and terpenoids (acyclic, monocyclic, and anti-inflammatory effect (16).

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 ODOVTOS-International Journal of Dental Sciences

APPLICATIONS OF PROPOLIS IN DENTISTRY PROPOLIS IN PERIODONTAL DISEASES

In dentistry, propolis is known as a promising In the treatment of periodontal diseases, propolis

compound mainly in the treatment of tooth decay has demonstrated antibacterial, anti-inflammatory,
and periodontitis; it is used in various presentations anesthetic, and healing activity in certain lesions
such as toothpastes and mouthwashes (17). The such as chronic ulcers or periodontitis (26).
oral cavity is an environment in which there are Some studies claim the action of propolis against
around 700 different species of microorganisms supragingival plaque by its stimulating tissue
that live in symbiosis, these known as the normal recovery and the local immune response (18). As
microbiota of the mouth. Because there are an anti-inflammatory, it inhibits the synthesis of
changes in the oral environment or under host prostaglandins and helps the immune system by
conditions, some bacteria tend to colonize and give promoting phagocytosis and stimulating cellular
rise to various oral pathologies mostly related with immunity (27). Periodontal propolis has been
inflammation and infection (18). The use of propolis utilized in various presentations, such as patches
in dentistry has been studied for a long time; that continuously release propolis into the affected
there are several studies mentioning that propolis gingiva, promoting tissue recovery (28). As an
extract can inhibit the growth of Gram-positive and irrigator prior to periodontal treatment, good results
Gram-negative bacteria, comparing its efficacy were observed, and these results were even noted
with some antibacterial drugs such as Ampicillin in the treatment of the herpes simplex virus in a
and Tetracycline, or even with antiseptics such solution presentation, slowing the progression of
as 0.12% Chlorhexidine (19,20). Regarding the skin changes at the beginning of the disease (26).
prevention of oral diseases, propolis has been
employed for its anticariogenic potential and the Chronic periodontitis (CP) is the most common
reduction of the accumulation of dentobacterial periodontal disease. It is defined as an infectious
plaque. Several studies affirm that the presence inflammation that compromises the supporting
of propolis significantly reduces cavities in rats by tissues of the tooth, causing loss of insertion and
inhibiting the synthesis of glucans and blocking alveolar bone. Its asymptomatic behavior prevents
the action of glucosyltransferase (21). Momen- the disease from being diagnosed in early stages;
Beitollahi et al. mentioned that propolis decreases thus, the clinical manifestations are more severe
the growth of the most prevalent oral pathogens (29). It is initiated by bacteria present in the
that include Streptococcus mutans, Candida biofilm; however, the specific immune response
albicans, and Actinobacillus commitans (22). In and inflammation play an important role in the
addition, propolis has been successfully used in the development of the disease (30). The assessment
treatment of dental pulp regeneration as a direct of periodontal status should be performed by a
coating in accidental exposure (23). Meakawa clinical evaluation of the inflammation of periodontal
et al. reported that the propolis extract was tissues (31). To assess these clinical parameters,
effective against the microorganisms C. albicans, an index system with several scores was designed,
Enterococcus faecalis, and Escherichia coli (24). including the gingival index (GI) (32), the dental
However, Koo et al. note that the true mechanism plaque index (PI) (33), bleeding after probing
of antimicrobial action of propolis appears to be (BP) (34), and the periodontal index (PI) (35). The
complex and is not yet fully understood (25). treatment for CP is undoubtedly scaling and root

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 Fraire-Reyes et al: Use and Effectiveness of Propolis on Chronic Periodontitis: a Systematic Review

planing (SRP), since it allows for the elimination clinical trials (ASE), with cohort or cases and
of microorganisms that give rise to inflammation controls were considered; (3) patients considered
and tissue damage. However, it has been observed had chronic periodontitis diagnosed with an intraoral
that adjuvant treatment with antiseptics permits examination, with nonadjacent teeth with periodontal
better results in the clinical and microbiological bag; (4) propolis management in any presentation;
parameters of the patients with this condition (5) comparison with any other antimicrobial agent,
without neglecting bacterial resistance, which is and (6) response, including improvement in clinical
a worldwide problem and in which the majority and microbiological parameters. Then, the full texts
of CP pathogens present genes for resistance to of the possible eligible articles were evaluated
the most widely employed antibiotics (36,37). The considering the following exclusion criteria: (1)
most widely used adjuvant treatment in patients patients with gingivitis; (2) in-vitro studies; (3) in-vivo
with periodontitis is Chlorhexidine but, in recent studies (mouse, rat, rabbit, dog, etc.); (4) patients
years, propolis has been investigated to a greater requiring endoperiodontal treatment; and (5) patients
extent in presentations such as gel and toothpaste with peri-implantation disease. Duplicate revisions
as natural products, which offer even better results were deleted in the different databases; thus, a total
than Chlorhexidine (38-40). Therefore, the aim of of 75 articles were obtained, which were analyzed
this study was to determine the effect of propolis on by title and abstract, their being useful in only 18
non-surgical periodontal therapy in patients with CP bibliographies. Of these, four were discarded due to
as it appears in the recent literature as an adjuvant their failing the eligibility criteria (one on gingivitis,
for the improvement of its clinical parameters. another with a focus on immunodetection, and two
on plaque control). In the final analysis, 12 articles
MATERIALS AND METHODS were evaluated for qualitative data collection and
seven for quantitative data collection (Figure 1).
The PRISMA Statement checklist for
preferred reporting items for systematic reviews RESULTS
and meta-analyzes (41) was used to conduct this
systematic review. This review was registered in According to the bibliographic review,
the International Prospective Register of Systemic seven articles related to the use of propolis as an
Reviews in Health and Social Care (PROSPERO) adjuvant of periodontal treatment were compared
under protocol number CRD42020191473. in study subjects with chronic periodontitis with an
approximate age ranging from 25-63 years; the
SEARCH STRATEGY AND STUDY SELECTION variables are described in Table 1. Some authors
describe their methodology by dividing their study
An extensive search of the literature was population into three groups: a control group; a
conducted using the electronic databases in PubMed, comparative group, and a group without adjuvant
Google Scholar, Web of Science, and Science Direct. treatment. Gebara et al. considered 20 patients
The keyword strings employed were the following: for their study, with three non-adjacent teeth
“Propolis AND periodontal disease”; “Propolis AND with periodontal pocket. Each of these sites was
red complex”; “Propolis AND periodontal surgery", assigned to a group as follows; group A irrigated
and "Propolis AND scaling and root planing", with hydroalcoholic extract of propolis twice
finding a total of 15,238 articles relating to the weekly for 2 weeks; group B irrigated with placebo
subject. All of the articles included in this review in the same manner as the first group, and group
were based on the following criteria: (1) time C, which did not include additional treatment.
interval ranging from 2013-2021; (2) randomized The analysis of clinical and microbiological

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 ODOVTOS-International Journal of Dental Sciences

parameters was analyzed after 6 months, yielding used toothpaste with aloe vera, and the second
a promising and more effective result in the used toothpaste with propolis, with clinical and
group irrigated with propolis (42). Coutinho et microbiological parameters by polymerase chain
al. included the same number of patients with reaction (PCR). At the beginning of the study and at
the same characteristics and divided them into the end of 3 months, the results were statistically
the same three groups; analysis of clinical and significant for propolis both on plaque and in clinical
microbiological parameters was performed after 2 and microbiological parameters (39). El-Sharkawy
months with positive results in the propolis group et al. studied a population with chronic periodontitis
(43). Shalaby et al. evaluated 45 subjects with stage and type 2 diabetes mellitus (DM2), for 6 months.
II or stage III periodontitis with grade B, who were The analysis was divided into the placebo group
included in the study, according to the 2017 World and the propolis group; these patients were
Workshop Classification of Periodontal Disease administered SRP and a 400-mg tablet according
(44). Each subject was randomly assigned to a to the group to which they belonged. The results
study group as follows: group 1 with 15 subjects included changes in hemoglobin and in fasting
who only received SRP; group 2 with 15 subjects plasma glucose and, as secondary parameters, a
who received SRP accompanied by daily dietary decrease in periodontal clinical parameters. The
supplementation with omega 3 for 6 months, results render it noteworthy that a treatment for
and group 3 with 15 patients who received SRP 6 months with a daily dose of 400 mg of propolis
with daily propolis supplementation for 6 months. improves hemoglobin and glucose levels in plasma,
Statistical analysis revealed that both propolis and as well as improving clinical parameters in chronic
omega 3 are significant and that they decrease periodontitis in this type of patient (48). De Andrade
periodontal disease and improve the level of clinical et al. used two groups for the analysis of a 20%
insertion at 6 months (45). Therefore, Shalaby et propolis hydroalcoholic extract as an adjuvant to
al. suggest dietary supplementation with propolis periodontal treatment, the two groups denominated
or omega 3 as an adjuvant of periodontal therapy the control group and the test group. There were
(46). Sanghani et al. analyzed 20 patients with a 14 patients in the test group, in whom 65 teeth
minimum of two deep periodontal pockets. Sites received SRP and irrigation with propolis extract.
were randomly assigned to the control group In the and finally in the control group, there were
who received only SRP, and to the test group who 52 teeth that received SRP and a saline irrigation.
received SRP and propolis. Clinical parameters Clinical parameters were analyzed on days 0, 45,
were evaluated, and subgingival plaque samples 75, and 90. The results indicated that the use of
were taken on 15 days per month. These results propolis as an adjuvant of periodontal treatment
revealed better clinical and microbiological results is more effective than the use of water-saline
at sites treated with propolis (47). Kumar et al. irrigation, placebo, and omega 3 (49). The clinical
also analyzed 40 patients in two groups with CP, parameters discussed in the previously mentioned
separated into group A and group B; the first group articles are summarized in Table 2.

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 Fraire-Reyes et al: Use and Effectiveness of Propolis on Chronic Periodontitis: a Systematic Review

Figure 1. Flowchart of the research in the literature.

Table 1. Study design.

Author Extract type Groups Sample Control Age Dose Time of the P value
(Reference) size group (range) presentation study
Gebara (34) Hydroalcoholic 3 20 Placebo 25-57 Solution 6 months <0.05
Coutinho (24) Hydroalcoholic 20% 3 20 Ethanol 14% 25-57 Solution 2 months -
Sanghani (31) LDD 2 20 NS 25-50 Local agent 1 month <0.01
Kumar (25) - 2 40 Aloe Vera 35-55 Toothpaste 3 months -
El-Sharkawy (23) - 2 50 Placebo 38-63 Tablet 6 months -
De Andrade (26) Hydroalcoholic 20% 2 18 Saline ≥ 30 Solution 6 months -
Solution
Shalaby (30) - 3 45 Omega 3 35-55 Capsule 6 months <0.01
NS=not shown.

Table 2. Clinical parameters in propolis treatment.

Author PI PI GI GI BP BP PD PD CAL CAL

(Reference) (Baseline) (Outcome) (Baseline) (Outcome) (Baseline) (Outcome) (Baseline) (Outcome) (Baseline) (Outcome)
Gebara (34) - - - - 57% 43% 93% 64% - -
Coutinho - - - - 0% 70% 0% 80% - -
(24)
Sanghani - - 2.04 ± 0.26 0.96 ± 0.09 2.99 ± 0.32 1.08 ± 0.23 5.35 ± 0.67 3.60 ± 0.68 3.35 ± 0.67 1.60 ± 0.68
(31)
Kumar (25) 1.87 ± 0.48 1.29 ± 0.27 3.08 ± 0.63 1.95 ± 0.23 2.83 ± 0.35 1.26 ± 0.25 5.57 ± 0.82 3.63 ± 0.67 4,57 ± 0,94 3.00 ± 0.95
El-Sharkawy - - - - - - 6.60% 1.90% 4.50% 7.80%
(23)
De Andrade 1.50 ± 0.94 0.95 ± 0.80 0.94 ± 0.84 1.10 ± 0.93 - - 5,75 ± 1,17 5.63 ± 0.84 - -
(26)
Shalaby (30) 2.00 ± 0.46 0.63 ± 0.25 - - 1.98 ± 0.55 0.53 ± 0.26 5,67 ± 0,68 3,01 ± 1,01 20 ± 0.93 2.86 ± 0.68

PI=Periodontal Index; GI=Gingival Index; BP=Bleeding on Probing; PD=Periodontal Depth; CAL=Clinical Attachment Level.

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 ODOVTOS-International Journal of Dental Sciences

DISCUSSION et al., who worked with a total of 20 patients with a

minimum of two periodontal pockets administered
Current scientific evidence shows us that the SRP treatment in a periodontal pocket, and in
propolis is a good adjuvant in the non-pharmacological the other, SRP and propolis as a local adjuvant,
therapy of chronic periodontitis (CP). In the present reporting the majority of the clinical parameters
review, seven clinical trials were analyzed; in all except for the dental plaque index (PI). This latter
of these, the patients presented a diagnosis of treatment was more favorable than that without
chronic periodontitis (CP), in which the main the adjuvant (47). De Andrade et al. worked with
clinical characteristic was periodontal pockets 16 individuals; a certain number of teeth in the
with a depth of ≥5mm. In the majority of studies, treatment group were treated with SRP in addition
the experimental process was carried out during to propolis irrigation, while another number of
a period of 6 months, which is the time period teeth were treated in the control group with SRP
stipulated, according to the scientific literature, in addition to saline irrigation. The authors found
during which there are better results after clinical better results in the experimental group treated
treatment with adjuvants in CP (50). The presentation with propolis. However, the authors did not report
of the experimental agent was used locally as an the majority of the clinical parameters, except for
irrigator (38,40,51), such as toothpaste (39), and bleeding after probing (BP) and clinical attachment
the former was also tested as an oral systemic level (CAL); thus, the conclusions of their study
agent (tablets/capsules), exhibiting promising cannot be decisive in determining whether
results in both patients with DM2 and in those propolis could be an effective treatment, or an
with CP (37) and in patients without systemic even better one, than that of the control group (40).
alterations (45). Several authors in this review The most recent study (Shalaby et al.) was one
reported that the propolis extract utilized in their of the most complete reports in terms of clinical
experiments was the hydroalcoholic extract at 20% parameters, in which only the gingival index (GI)
(40,42,43), since it has been observed that this is was not reported, however, this analysis concludes
the best method for extracting the highest amount that both omega and propolis are adequately
of polyphenols, in that these compounds are those significant for the decrease of chronic periodontis
that confer antimicrobial properties on the propolis (CP) (43). The clinical parameters reported in
(52). However, authors such as Shalaby et al. and Table 2 demonstrate improvements with the use
El-Sharkawy et al., who employed propolis in of propolis in all patients regardless of the control
tablets as a vehicle, did not report what type of group used, inferring that the physicochemical
extract was used for its preparation (45,48). The characteristics of propolis have a favorable effect
latter is a disadvantage because it is not known on CP. In the report by Gebara et al., the authors
whether the effect is due to the hydroalcoholic mention a 14% decrease in periodontal bleeding
preparation or to the phenols of propolis. Similarly, as a result; they also report a 29% decrease
Sanghani et al. and Kumar et al. did not report in the periodontal pocket and a decrease of
the methodology they utilized in the realization Porphyromonas gingivalis and yeast colonies
of their irrigation agent and toothpaste, which (42). These decreases in clinical parameters
does not allow for a better analysis of its results led us to suppose that adjuvant treatment with
(39,47). The age range used by the authors propolis induces changes in the pathophysiology
in this research was very similar, in that they of periodontal disease, in that the reductions are
included adults aged approximately 25-60 years. quite significant. In the same way, Coutinho et al.
Researchers who employed two groups (control found similar results with the propolis extract as an
group and experimental group) included Sanghani adjuvant to periodontal treatment; this was more

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 Fraire-Reyes et al: Use and Effectiveness of Propolis on Chronic Periodontitis: a Systematic Review

effective than SRP according to the evaluation of depending on geographical location, harvesting
clinical and microbiological parameters (43). In season, and method of extraction. Therefore, it is
another article (Sharkawy et al.), it was evidenced important to investigate a standardization method
that there were improvements in treatment with to determine a universal dose in the treatment of,
propolis in individuals with DM2 and with chronic for example, chronic periodontitis.
periodontitis, obtaining satisfactory results in
both hemoglobin levels and glycemic control, as DISCLOSURE STATEMENT
well as in the depth of the periodontal pocket,
with a reduction of 4.7% and an increase in The authors declare no conflict of interest.
CAL of 3.3% (48). The studies reviewed in this
work demonstrated that the study of propolis as ACKNOWLEDGEMENTS
an adjunct in periodontal disease is currently
in progress. Propolis as an organic compound The fund for this study were provided by
does not present cytotoxicity in bone marrow PROFEXCE-UAZ 2020.
mesenchymal stromal cells (BMMSC) (53), tumor
cell lines (54), and human dermal fibroblasts AUTHOR CONTRIBUTION STATEMENT
(HFFF2) (55), among others. However, none of the
reviewed articles reported conducting tests for Conceptualization and Design: I.A.F., C.G and C.B.
cytotoxicity, which would be important to perform Literature Review: I.A.F and C.B.
specifically in oral cell lines. The search for an Methodology and Validation: L.A, C.G. and C.B.
ideal vehicle for propolis continues to comprise Formal Analysis: I.A.F, C.G., L.A. and C.B.
one of the main issues in this regard since, in the Investigation and Data Collection: I.A.F and C.B.
oral cavity, this presentation must be suitable for Resources: L.A. and C.B.
the application of propolis in the oral tissues. Data Analysis and Interpretation: I.A.F. and C.B.
Writing-Original Draft Preparation: I.A.F.
CONCLUSIONS Writing-Review & Editing: I.A.F., C.G., O.C., L.A
and C.B.
The previously mentioned articles conclude Supervision: C.G., O.C., V.E., L.A and C.B.
that propolis is a good adjuvant for the treatment Project Administration: C.G., L.A. and C.B.
of patients with chronic periodontitis compared to Funding Acquisition: C.G., L.A. and C.B.
the conventional treatment (SRP), saline solution,
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