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2022, Number 1

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Rev Odont Mex 2022; 26 (1)

Clinical and antibacterial effect of Copaifera reticulata to support the treatment of periodontitis in type 2 diabetics

Ramos-Perfecto, Donald1; Castro Luna, Américo1; Moromi Nakata, Hilda1; Martínez Cadillo, Elba1; Arbañil Huaman, Hugo2; Gamarra Gonzales, Dante2; Chucos Ortiz, Rafael3; Villavicencio Gastelú, Jorge1; Dávila Paredes, Darío4

Language: English/Spanish [Versión en español]
References: 32
Page: 19-31
PDF size: 278.71 Kb.


ABSTRACT

Introduction: nowadays the use of natural products are an option in the treatment of various diseases, as could well be copaiba oleoresin, which presents properties that could be used as an adjuvant in the treatment of periodontitits. Objective: to determine the clinical and antibacterial effect of Copaifera reticulate (C.reticulata) "copaiba" as support for non-surgical periodontal therapy (NSPT) in the treatment of periodontitis in type 2 diabetic patients. Material and methods: 40 homologous zones with periodontitis were identified in the maxillary or mandibular hemiarchs of 20 type 2 diabetic patients, recording the clinical variables: probing depth (PD), clinical insertion level (CIL), bleeding on probing (BP) and gingival color (GC). Subgingival biofilm and blood samples were also collected for bacterial count and determination of glycosylated hemoglobin (HbA1c), respectively. Two homologous areas per patient were evaluated, forming a control group of 20 areas with periodontitis that received NSPT plus chlorhexidine and a study group of 20 areas with periodontitis that received NSPT plus C. reticulata. The obtained values were processed by the statistical tests of Wilcoxon and Fisher. Results: the PD had a difference of comparison between the control and study groups of the before and after of 2.0 ± 0.79 mm and 2.05 ± 0.89 mm, respectively. For the CIL, the values of the comparison difference between the control and study groups were 2.35 ± 0.93 mm and 2.05 ± 0.58 mm, respectively, thus no significant statistical differences were found in both indicators (p > 0.05). BP was reduced by 95% and 90% in the control and study group. Concerning bacterial count, it was reduced in both groups, therefore, it was observed that the study group had a lower number of colony-forming units (CFU) so no statistically significant differences were found (p > 0.05). Conclusions: C. reticulata as support for NSPT showed similar behavior to chlorhexidine, obtaining similar effects for both clinical and microbiological indicators.



ABBREVIATIONS:

  • BP = bleeding on probing.
  • CFU = colony-forming units.
  • CIL = clinical insertion level.
  • GC = gingival color.
  • HbA1c = glycosylated hemoglobin.
  • NSPT = non-surgical periodontal therapy.
  • PD = probing depth.
  • T2D = type 2 diabetes.



INTRODUCTION

Diabetes mellitus is a non-infectious disease that is part of metabolic disorders. It is mainly characterized by hyperglycemia, accompanied by a deficient production and/or action of insulin.1 Worldwide, 425 million people have diabetes,2 50% of whom are undiagnosed, and the prevalence has tripled between 2006 and 2017.1 Prevalence as the number of new cases continues to grow in the world, in the United States (USA) 30.3 million adults had diabetes in 2017, of which 23.1 million were diagnosed and 7.2 million did not know their diagnosis.1 In Peru, the prevalence of diabetes in adults is 6.8 to 7.2%, with differences according to regions: coast (8.2%), highlands (4.5%), and jungle (3.5%).3 Of the types of diabetes that can occur, the most frequent are: type 2 diabetes (T2D), type 1 diabetes, and gestational diabetes being T2D the one which occurs in more than 90% of the cases.

Diabetes mellitus is a great burden for the health care system in Peru, since it is a disease on the rise, generating mortality, morbidity, and disability in people. Its growing prevalence is demonstrated by the fact that two new cases per one hundred people are identified per year.4 In Peru, diabetes is the eighth leading cause of death, the sixth leading cause of blindness due to diabetic retinopathy, and the first cause of non-traumatic amputation of lower limbs. It is also a risk factor for the presentation of severe forms of periodontitis, which causes tooth loss.5

Regarding periodontitis, it is considered the sixth most common complication in diabetics5 with bi-directionality in the origin and development of the disease with diabetes. Although periodontitis is indeed characterized by a dysbiosis at the periodontal sulcus level, where the presence of Gram-negative anaerobic bacteria has great relevance, it is also true that the host's susceptibility as well as systemic factors such as diabetes are factors for its origin. Thus, several studies have been able to confirm the association of periodontitis in diabetic patients, determining a higher prevalence of periodontal pockets, loss of clinical insertion, increased bleeding, and loss of teeth, among others.6-10

The treatment of periodontitis is based on the mechanical removal of subgingival biofilm, a biofilm composed mainly of bacterial flora, where the red and orange complexes mentioned by Socrasky11 are the most aggressive. Removal of this biofilm, reducing it to a minimum, is related to clinical improvements such as reduction of the periodontal pocket, attachment gain as well as reduction or absence of bleeding. In addition to this initial removal phase, several researchers have proposed the use of systemic or local antimicrobials to improve periodontal conditions.12-19 But these benefits not only occur in periodontitis but also in type 2 diabetic conditions, mainly by reduction of the level of glycosylated hemoglobin (HbA1c) in patients in a range of 1 to 2%.13,14,17,18

Regarding support products for the treatment of periodontitis, there are several antimicrobials used, but taking a more innovative view, natural products are a very good option. Whether in the form of an extract, essential oil, or oleoresin, they show antimicrobial active principles against periodontopathogenic bacteria, so products such as green tea,20 tara,21 and copaiba22 have been suggested as adjuvant treatments. Copaifera reticulata (C. reticulata) "copaiba" or also called palo de árbol oil, is a product extractable by perforation of a tree of the Copaifera genus. This oil or oleoresin has shown several pharmacological properties such as anti-inflammatory,23 healing,24 and antimicrobial,25 among others. Its antibacterial property may reduce the pathogenic bacterial flora that persists after mechanical removal of the biofilm, so it could be an option to support non-surgical periodontal therapy (NSPT). C. reticulata has sesquiterpenes in its composition, such as beta-caryophyllene, a chemical compound that is the main antibacterial active component.26 The antibacterial property of C. reticulata has been demonstrated in studies carried out by different researchers.22,27-31

Knowing the benefits of a natural product such as C. reticulata, as well as its easy handling and application, this study aimed to determine the clinical and antibacterial effect of C. reticulata "copaiba" as a support treatment for periodontitis in type 2 diabetic patients.



MATERIAL AND METHODS

The study was a prospective, comparative, split-mouth clinical trial. The participants were a group of 20 type-2 diabetic patients with periodontitis. They were recruited at the Diagnostic Service of the Faculty of Dentistry of the Universidad Nacional Mayor de San Marcos and at the Diabetic Foot Clinic of the Hospital Dos de Mayo, Lima, Peru. All the participants in the study had to meet the selection criteria. The inclusion criteria were: type 2 diabetic patients with periodontitis. As for the exclusion criteria, they were: a) Participants who had received periodontal or antimicrobial treatment 60 days before the start of the study. b) Edentulous patients or patients with absence of homologous teeth in different hemiarchs. c) Smokers. d) Patients with autoimmune disease. e) Patients under 18 years of age. f) Patients allergic to the substances to be evaluated, and g) Patients who did not sign the informed consent. The study was assessed and approved by the Ethics Committee of the San Fernando School of Medicine of the Universidad Nacional Mayor de San Marcos, with certificate number No. 0288 and project code No. 0369. Also, since participants were recruited from the Diabetic Foot Clinic of the Dos de Mayo Hospital, the hospital evaluated the research by its own ethics committee, approving it and giving it a registration number No. 004270.

From the selected group, the periodontium of homologous pieces present in different hemiarchs, either in the maxilla or the mandible presenting periodontitis, was evaluated. A total of 40 zones were assessed. They were distributed in a control group of 20 that received NSPT plus 0.12% chlorhexidine and a study group of 20 that received NSPT plus C. reticulata. Disease variables or indicators such as probing depth (PD), clinical insertion level (CIL), bleeding on probing (BP), and gingival color (GC) were registered at the beginning of the study, as well as the changes after performing the NSPT, supported by chlorhexidine in the control group and C. reticulata in the study group. Records of these indicators were obtained by the development of a periodontogram at baseline and two months after treatment. Subgingival biofilm samples were also taken at baseline and at two months to appraise changes in the bacterial flora after treatment.

Obtainment of the oleoresin from Copaifera reticulata. C. reticulata was obtained by drilling the trunk of trees of the Copaifera genus and the species reticulata, which was taxonomically identified by taking as a sample a tree leaf and taking it to be analyzed in the Amazonian Herbarium of the National University of the Peruvian Amazon (UNAP), located in Iquitos-Loreto-Peru. The sample of oleoresin used in this study was obtained in the district of Santiago de Estrecho, in the province of Putumayo, on the border with Colombia. Also, the areas of Remanso and Punchana are places where this tree grows and develops naturally. Once C. reticulata, was identified, it was deposited in amber glass containers and taken to a conventional sterilization process by autoclave. Afterward, it was ready for its application as a support treatment for periodontitis.

Development and evaluation of periodontal therapy in type 2 diabetic patients. Before the diagnosis and registration of periodontal lesions in the patient, the dental staff was calibrated in the recognition of periodontitis indicators, periodontal charting, and sampling of subgingival biofilm. This was done in order to try to make measurements as reliable as possible. In relation to periodontal therapy, the forty identified zones with periodontitis were divided into two groups of 20 homologous zones, in different hemiarchs. Initially, the following indicators were recorded: PD, CIL, BP, and GC, in a card designed for the study.

Once the initial data were obtained, NSPT was performed. NSPT included scaling and root planing of the identified areas in both the control and study groups. This procedure was performed with Gracey periodontal scalers and curettes (Hu-Friedy, USA). Once this procedure was finished, the treatment was supported in the control group with 0.12% chlorhexidine and in the study group with C. reticulata. The amount of the support product was 10 µL taken to the periodontal sulcus utilizing a micro brush (Micro-applicators, China) of 1.5 mm diameter. The application of the products was performed in the first, second, third, and fourth weeks, and two months after NSPT. Changes in some of the indicators of periodontitis, as well as dental plaque control by the patient, were also evaluated visually during these weeks.

To assess the patient's diabetes control condition, two blood samples were taken, one at the beginning and one at the end of the study, to determine the patient's glycosylated hemoglobin (HbA1c), the reference test to determine the patient's diabetes status.

Development and assessment of the microbiological study of periodontal pockets in type 2 diabetic patients. Periodontal pockets were identified in homologous teeth with periodontitis, 20 in the control group and 20 in the study group. These samples were taken at two moments: at the beginning and the end of the study. For this procedure, first, relative isolation of the selected area for sampling was performed and the supragingival plaque was removed from the tooth with periodontitis. Afterward, two No. 40 paper cones were placed in the periodontal sulcus for a time frame of 40 to 60 s. Once the time was over, the paper cones were removed and brought into a BHI (brain-heart infusion) transport medium. Then they were taken to the laboratory for processing. In the laboratory, dilutions of the sample were made at 10-1, 10-2, and 10-3, from this last dilution 100 μL were taken for sowing in Schaedler agar medium or 5% blood agar supplemented with vitamin K and hemin. This medium was incubated at 37 oC under anaerobic conditions for 7 days. After this time, a colony-forming unit (CFU) count was performed for both the control and study groups. This sampling and CFU counting procedure were performed at the beginning and end of the study in both groups.

Statistical analysis. The results were analyzed by the SPSS statistical program version 21. Clinical and microbiological variables were evaluated, comparing the before and after of each group as well as the mean differences of the quantitative variables. The Wilcoxon test was applied for all the variables except Gum Color in which the McNemar χ2 test was applied.

The qualitative variables, bleeding on probing and gum color, were dichotomized to facilitate the differential analysis between the control and study groups using Fisher's exact test. All tests were performed at a significance level of 0.05 (p < 0.05).



RESULTS

In general, it was possible to determine the supportive effect of C. reticulata on NSPT by demonstrating improvements in the studied clinical and microbiological aspects. Among the general characteristics of the sample, it was identified that 55% were male, with an average age of 62 years, and had been suffering from diabetes between 8 to 9 years. Sixty percent had severe periodontitis and 40% had moderate periodontitis. Something that stands out about these patients' HbA1c is its average since at the beginning of the study the mean was 7.3% and at the end of the study, it was 6.2%. These data and others concerning the patients are detailed in Table 1. After the study phase in which the NSPT support products were applied, the clinical and microbiological variables were compared.

For the patients in the control group, PD went from 4.25 ± 0.44 to 2.25 ± 0.85 and the initial CIL of 5.90 ± 2.08 was reduced to 3.55 ± 2.24. Bleeding was assessed using the Papilla Hemorrhage Index as described by Saxer and Muhlemann. Initially, grades 1, 2, 3, and 4 were registered, and at the end of the study, grade 1, which is the representation of a bleeding point when probing the papilla. Regarding GC, in the beginning, all the areas showed a red color that changed to a coral pink color in 95% of the sample after the study. Concerning the microbiological aspect, the CFU count was 146.30 (± 108.64) × 103 at the beginning and 48.0 (± 57.62) × 103 at the end. Both the clinical and microbiological values had a significant statistical difference with a p-value < 0.001, except for GC (Table 2).

With regard to the study group, the results indicated that PD decreased from 4.5 ± 0.69 at baseline to 2.45 ± 1.19 at the end of the study. The CIL was 6.70 ± 3.34 at baseline and 4.55 ± 3.36 mm at the end of the study. Bleeding was identified in grades 1, 2, and 3. In the end, grade 1 was obtained in two patients. GC was red in all patients and at the end of the study, it changed to a coral-pink color in 90% of the cases. Regarding the CFU bacterial count, this had a mean of (146.55 ± 145.08) × 103 at the beginning, and at the end of the study, it was recorded at (35.50 ± 31.24) × 103. The studied variables had a p value < 0.001, except for GC (Table 3).

When comparing the results of the differences between the variables of the control and study groups at the end of the investigation, it was determined that the PD was 2.0 ± 0.79 for the control group and 2.05 ± 0.89 mm for the study group. As for CIL, the control group had 2.35 ± 0.93 mm and in the study 2.15 ± 0.58 mm, with no statistically significant differences (p > 0.05). In relation to bleeding, in the control group, it was controlled in 95% and in the study group in 90%, thus the differences between them were considered statistically non-significant (p > 0.05). GC changed from red to coral pink in 95% of the control group and 90% of the study group, so it was considered statistically non-significant p > 0.05. As for the microbiological variable, the CFU had a value of (98.3 ± 88.54) × 103 in the control group and (111.05 ± 137.07) × 103 for the study group, showing no statistically significant differences p = 0.456 (Table 4).



DISCUSSION

Copaifera reticulata oleoresin has been shown to have a variety of properties, among them that of being a good antimicrobial. This characteristic is supported by researchers such as Oliveira dos Santos and collaborators,27 Mendonca and collaborators,25 Pieri and collaborators,29 among others, who have demonstrated its activity against Gram-positive and Gram-negative microorganisms as well as yeast forms, thus supporting its possible use as an adjuvant to NSPT, promoting improvements in clinical variables or parameters such as PD, CIL, Bleeding, GC. Changes in the microbial flora present in the altered gingival sulcus have also been suggested.

Concerning PD, this clinical parameter had a reduction in both the control and study groups of 2.0 ± 0.93 mm and 2.05 ± 0.89 mm, respectively. These values were similar to those mentioned by Famarzi and collaborators,14 who used NSPT supported with 1.5% chlorhexidine gel, achieving a reduction of 1.93 ± 0.33 mm in PD in the group that received this product. Likewise, Tsobgny and collaborators,18 performed their study with the same technique supported with 10% iodopovidone. PD was reduced by 1.1 ± 0.4 mm. Duarte and collaborators,19 used amoxicillin and metronidazole systemically as an adjuvant, achieving a reduction of 1.11 mm of PD in the study group. These studies support some extra benefits when using an antimicrobial as support. There are also reports such as the one by Palka and collaborators32 that do not use antimicrobial support for NSPT, obtaining less PD reduction in their results: they achieved an average BP reduction of 0.9 mm in the study group.

In relation to CIL, at the end of the study, an insertion gain of 2.35 ± 0.93 mm and 2.15 ± 0.58 mm was obtained in the control and study groups, respectively. These values are similar to those obtained by Tsobgny et al,18 who, using 10% iodopovidone irrigant to support NSPT, obtained a gain of 1.3 ± 0.5 mm. Likewise, Famarzi and collaborators,14 employing 1.5% chlorhexidine gel, obtained a CIN gain of 0.87 ± 0.1 mm. Duarte and collaborators,19 supported their therapy with systemic antibiotics and obtained a CIL gain of 0.86 mm in the study group. These two researchers obtained values below 1 mm, unlike the results hereby shown regarding this parameter. Rovai and collaborators,15 reported values above the ones obtained in the present study in their systematic review on the local use of antimicrobial agents as support for NSPT, where they mention Martorelli, who used 10% doxycycline gel as support for NSPT and achieved a CIL gain of 3.2 ± 0.4 mm in periodontitis in diabetic patients. Likewise, very low values of CIN gain were obtained by Goel and collaborators,17 when performing NSPT only in type 2 diabetic patients with periodontitis. They achieved a CIL gain of 0.3 mm, a figure well below all the aforementioned studies.

Bleeding was almost completely controlled, being absent in both the control and study groups at 95 and 90%, respectively. Similar results were obtained by Tsobgny and collaborators,18 who, using 10% iodopovidone as an adjuvant in NSPT, were able to reduce the bleeding rate to 4.2 ± 4.7%. Likewise, Duarte and collaborators,19 obtained bleeding control with a final percentage of 10.6 ± 5.7%. About the GC, a color change to coral pink was observed in both the control and study groups at 95 and 90%, respectively. This is a variable scarcely compared in research but of great clinical importance. There are no previous studies with which to compare this parameter.

Regarding the antibacterial effect of the applied products for NSPT support, it was possible to quantify the CFU count before and after treatment, both in the control and study groups, obtaining a difference in the mean CFU, for the control group of 98.3 (± 88.54) × 103 and the study group of 111.05 (± 137.07) × 103. These results might suggest a greater reduction in the study group, which received C. reticulata plus NSPT. Similar results were obtained by Tamashiro and collaborators12 who evaluated the subgingival bacterial flora and periodontal indicators of the disease in type 2 diabetics, after performing NSPT supported by the use of antibiotics. After an evaluation period of 2 years, they found that the study group had a low proportion of red complex bacteria 5.5%, and the control group that did not receive antimicrobials exhibited a value of 12%.

An indicator of the metabolic control of diabetes considered in several studies with diabetic patients is the HbA1c test since it allows one to know the control (or lack of it) of the condition. This value ideally should be below 7% so that procedures that can reduce this percentage will help the metabolic control of the disease. This investigation performed NSPT supported with local antimicrobial products, demonstrating a recovery of periodontal health indicators, but also, possibly an improvement of the HbA1c value: the total of diabetics at the beginning of the study had a mean HbA1c of 7.3 ± 1.4% and at the end of the study this value was 6.2 ± 0.9%, thus the value of HbA1c was reduced by 1.1%, this finding might support the bidirectional nature of the diabetes-periodontitis disease, whereby positively manipulating one of the illnesses, a benefit may be obtained in the other; in this research, the periodontal disease condition was improved, and hence, there was an improvement in the diabetes control condition. These results are similar to those reported by Cuaresma and collaborators.13 They showed a reduction in HbA1c by an average of 0.8%, although slightly higher values were obtained by Tsobgny and collaborators,18 who used chlorhexidine as NSPT support in type 2 diabetic patients with periodontitis, reducing HbA1c by 3.0 ± 2.4%.

Smaller results of HbA1c reduction were reported by Preshaw et al.,6 in their review of diabetes as a risk factor for periodontitis, stating that NSPT would be related to a reduction of approximately 0.4% in HbA1c. Following this line Saenz et al.,10 in their expert review, state that NSPT improves glycaemic control in type 2 diabetic patients, resulting in a decrease in HbA1c in the range of 0.27 to 0.48%.



CONCLUSIONS

According to the methodology developed in this study, it was possible to determine the clinical and antibacterial effect of C. reticulata as support to NSPT which is considered the "gold standard" for the treatment of periodontitis, as well as chlorhexidine (the most used support chemical agent for this disease) that served as control. It can be concluded that the results observed in all periodontal and microbiological indicators demonstrated improvements thus restoring periodontal health in 100% of type 2 diabetic patients with periodontitis. The possible use of copaiba as an adjuvant to NSPT is hereby recommended, although studies with a larger number of cases might strengthen this suggestion.


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AFFILIATIONS

1 Docente de la Facultad de Odontología de la Universidad Nacional Mayor de San Marcos, Lima, Perú.

2 Médico-Endocrinólogo del Servicio de Endocrinología del Hospital Dos de Mayo, Lima, Perú.

3 Licenciado en Enfermería del Servicio de Endocrinología del Hospital Dos de Mayo, Lima, Perú.

4 Ingeniero Forestal Asistente del Herbario Amazonense de la Universidad Nacional de la Amazonia Peruana, Loreto, Perú.



Conflicto de intereses: los autores declaran no tener ningún conflicto de intereses.



CORRESPONDENCE

Donald Ramos-Perfecto. E-mail: dramosp@unmsm.edu.pe




Received: Junio 2020. Accepted: Mayo 2021.

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