Comparative analysis of filling quality and bond strength among different root-end filling materials in root-end cavities

International Journal of Adhesion & Adhesives 133 (2024) 103757

DOI: https://doi.org/10.1016/j.ijadhadh.2024.103757

Received: 8 May 2024 | Revised: 18 June 2024 | Accepted: 19 June 2024 | Available online: 2 July 2024

Karen Gisselle Garay Villamayor, Leonardo Moreira Teodosio, Iago Ramirez, Heitor Silva Prado, Helena Cristina de Assis, Manoel Damião de Sousa-Neto, Jardel Francisco Mazzi-Chaves, Fabiane Carneiro Lopes-Olhê*

Departament of Restorative Dentistry, Ribeirão Preto School of Dentistry, Universidade de São Paulo, 14040-904, Ribeirão Preto, São Paulo, Brazil

*Corresponding author: Fabiane Carneiro Lopes-Olhê — fabiane.lopes@usp.br / fabiane.c.lopes@gmail.com

Abstract

The aim of the study was to evaluate root-end filling materials (MTA Angelus, Bio-C Repair, Cimmo HD and Biodentine) in terms of filling ability and their bond strength to dentin. 40 maxillary incisors were prepared for simulated apical surgery. After sectioning 3 mm before the apical foramen and 6 mm in the cervical direction, the specimens were positioned at a 45° angle. Root-end cavities, 3 mm deep, were then created using an ultrasonic insert. The specimens were divided into four groups based on the material used (n = 10). Filling ability, bond strength, and failure modes were evaluated using microtomography, push-out test, and a stereomicroscope, respectively. Data were tested for normality (Shapiro-Wilk) and homogeneity (Levene) (P > 0.05). One-way ANOVA was used to analyze filling ability and bond strength data, for failure mode, the chi-square test was used at a 95% probability level. A lower percentage of gaps was observed in the root-end cavities filled with Bio-C Repair, Biodentine and MTA Angelus when compared to Cimmo HD, with no significant difference between them (P > 0.05). Regarding the bond strength, Biodentine (16.48 ± 3.92 MPa) and MTA Angelus (15.67 ± 3.07 MPa) showed higher values when compared to Bio-C Repair (11.18 ± 1.38 MPa), with no statistically significant difference between them (P > 0.05). Cimmo HD showed intermediate values (12.60 ± 2.61 MPa), with no statistically significant difference to MTA Angelus and Bio-C Repair (P < 0.05). The cavities filled with Biodentine showed a predominance of cohesive failures, while the other materials showed mixed failures (P < 0.05). Cimmo HD exhibited more gaps compared to other materials, with Biodentine and MTA Angelus showing the highest bond strength, with Cimmo HD showing an intermediate value.

Keywords: Apicoectomy; Microcomputed tomography; Tricalcium silicate.

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1. Introduction

The success of endodontic treatment relies on adequate case planning, disinfection, and instrumentation of the root canal system, followed by three-dimensional obturation of the root canal [1]. The complete elimination of microorganisms and their by-products within the root canal system and the prevention of re-infection are extremely important in the management of periapical pathology [2]. However, even after careful cleaning, shaping, disinfection and obturation, the probability of endodontic treatment failure remains, which may be related to bacterial persistence in the apical third of the canal, resulting persistent symptomatic periapical lesions [2]. In addition, potential iatrogenic occurrences during instrumentation, such as deviations, perforations, instrument fractures, as well as calcifications and anatomical variations such as isthmuses, lateral canals, accessory canals, and apical deltas, can negatively affect the cleaning and shaping of the root canal system, which can lead to treatment failures [3].

The first choice of therapy in cases where conventional endodontic treatment fails, or where periapical lesions do not respond to treatment, is non-surgical endodontic retreatment [4]. However, this approach may not repair the clinical condition due to the difficulties encountered during treatment, such as the complexity of the root canal system, inadequate instrumentation, and the presence of physical barriers, as well as genetic aspects related to the host [4,5]. When previous non-surgical retreatments have failed due to persistent intra- or extra-root infections without regression of the periradicular lesion, surgical intervention becomes the therapeutic option of choice [6].

The aim of apical surgery is to remove residual microorganisms from the periradicular region and the root canal system in the apical region, and to create a barrier at the apical end of the root with an inert material to enable repair of the periapical tissues [7]. The procedure includes exposing the apex of the affected root, surgically removing the pathological tissue, resecting the affected root end, preparing the root-end cavity and its filling [8]. Thus, the aim of apical surgery is not only to remove diseased periapical tissue and the root apex, but also to seal the root-end cavity with an appropriate root-end filling material [4,6,9].

The use of bioactive materials to fill root-end cavities has shown advantages and high success rates [10]. These materials have moisture tolerance, good adaptation to cavity walls, good biocompatibility, and dimensional stability even after contamination with biological fluids, as well as stimulating the healing of periapical tissues [6,11]. Initially, mineral trioxide aggregate (MTA) was the hydraulic cement used in this context [9]. However, it has some disadvantages, such as being difficult to handle, a long setting time and low resistance to washout, which can result in microleakage, thus limiting its applications [11].

To overcome these limitations, a variety of hydraulic cements have been launched on the market, with different compositions and forms of presentation. Biodentine (Septodont, Saint-Maur-des-Fossés, France) is a hydraulic cement with good cytocompatibility, bioactivity and mineralizing capacity [12,13]. Although it is based on MTA technology, the absence of calcium aluminate and calcium sulphate in its composition preserves biocompatibility [14] and increases mechanical resistance [15]. Another alternative available on the market is Cimmo HD (Cimmo Soluções em Saúde, Pouso Alegre, MG, Brazil), a hydraulic cement differentiated by the inclusion of a pozzolanic compound in its formulation. This compound was included with the aim of, after reacting with calcium hydroxide and water, allowing the efficient flow of the pre-mixed substrate, maintaining an adequate consistency for handling, and reducing setting time, thus avoiding the use of chemical accelerators [16].

Regarding the different forms of presentation, the evolution of powder-liquid hydraulic cements resulted in the creation of pre-mixed hydraulic cements, such as Bio-C Repair (Angelus, Londrina, PR, Brazil). This cement stands out for its biocompatibility, which is comparable to that of MTA [17] and its presentation in the form of a ready-to-use paste, which requires less technical complexity and makes it more accessible to the professional [18], making it an interesting alternative for apical surgery procedures. The biggest challenge in endodontic surgery is to achieve persistent microbial containment in the root canal and prevent the entry of periapical fluids using a biomaterial with osteoinductive characteristics and the ability to stimulate the healing of periapical tissues [4,8].

The root-end filling must adhere strongly to the root canal dentin, ensuring the integrity of the interface between the filling material and the dentin, without the presence of gaps, to prevent microleakage and resist displacement forces, providing a long-lasting apical seal [8]. In this context, the push-out test proves to be an efficient method for assessing the ability of the root-end filling material to resist displacement forces, based on the principle of uniform and uniaxial distribution of stress between the filling material and the dentin during the test [19], as demonstrated in previous studies [20,21].

There are few studies evaluating the filling capacity of hydraulic cements in root-end cavities, especially in clinical situations where the operator does not have a direct view of the surgical area, and only one study [22] discusses this issue. Therefore, the aim of this study was to analyze the filling ability of MTA Angelus, Bio-C Repair, Biodentine and Cimmo HD in root-end cavities using micro-computed tomography, as well as the bond strength of these root-end filling materials to dentin. The null hypothesis tested is that there is no difference in the filling capacity and bond strength of the different hydraulic cements evaluated.

2. Materials and Methods

2.1. Sample Selection

After approval of the project by the Institutional Research Ethics Committee (approval report number 68715623.2.0000.5419), human upper incisors were obtained from the local tooth biobank, which were being kept in 0.1% thymol at 9°C for storage and preservation. They were then washed in running water for 24 h to eliminate residues. The sample size calculation was performed using SigmaPlot v.12.00 (Systat Software, San Jose, CA, USA) with the following parameters: a two-tailed test, a significance level of 5% (α = 0.05), a 95% confidence interval, 90% statistical power (β = 0.10), and an equal allocation ratio of 1:1 between the experimental groups. The standard deviation was derived from prior studies [23,24] indicating that at least 10 specimens were required for each group. The teeth were examined macroscopically and radiographed in the orthoradial and mesioradial directions using a digital sensor to select 40 teeth with a fully formed straight root with a minimum length of 12 mm, single canal, no calcifications, resorption or cracks and no previous endodontic treatment.

2.2. Sample Preparation

The crowns of the teeth were sectioned perpendicular to their long axis in the buccal-lingual direction at the cemento-enamel junction. The specimens were positioned on acrylic plates, with the longitudinal axis parallel to the surface of the plates and fixed with hot glue. The plates were individually attached to the Isomet 1000 cutting machine (Buehler, Lake Forest, IL, USA) and the cuts were made with a 0.5 mm thick diamond blade (South Bay Technology, San Clement, CA, USA) weighing 75 g, at a constant speed of 350 rpm, under constant refrigeration.

The experimental procedures were carried out by a single expert using a DM Plus IB surgical microscope (Opto Eletrônica, São Carlos, Brazil) with 2x to 12× magnification. After removing the crown, the root canal was irrigated with 5 ml of 1% NaOCl and passively explored using a #15 stainless-steel K-file until reaching the apical foramen, determining the actual tooth length. Then, 1.0 mm was subtracted to establish the working length (WL). Biomechanical preparation of the root canals was performed using Reciproc R50 over the entire WL. The file was used passively with pecking movements, cleaned with gauze every 3 advances, and irrigated with 5 ml of 1% NaOCl throughout the entire process. Canals were suctioned and dried with absorbent paper points (Reciproc, VDW GmbH, Munich, Germany).

2.3. Making the Specimens

The specimens were made by adapting the method proposed previously [22]. The roots were transversely sectioned at two points: 3 mm below the apex and, parallel to the first point, 6 mm towards the cervical using a 0.5 mm thick diamond blade attached to an Isomet 1000 cutting machine. The specimens obtained were individually centered in aluminum rings (16 × 4 mm), which were filled with wax. The specimens were positioned at an angle of 45° to the horizontal plane in a stainless-steel device developed specifically for this test.

The root-end cavity was made using a P1M ultrasonic insert (Helse Ultrasonic, Santa Rosa de Viterbo, SP, Brazil) coupled to an ultrasound device (Advance 1, Microdont, São Paulo, SP, Brazil), programmed at 30% power under constant refrigeration. The insert was used for 20 s, until all its active part penetrated the root-end cavity, corresponding to 3 mm, thus standardizing the cavity at 3 mm in height and 1.5 mm in diameter. Subsequently, the root-end cavities were irrigated with 2 mL of saline solution using a syringe and NaviTip tips (Ultradent Products Inc., South Jordan, UT, USA).

2.4. Initial Micro-Computed Tomography (micro-CT)

To analyze the quality of the filling, micro-CT was carried out on the specimens. The slices were removed from the wax and scanned individually using a SkyScan 1174 v.2 microtomograph (Bruker-microCT, Kontich, Belgium) from the Endodontics Research Laboratory at FORP-USP. Each specimen was fixed with the cervical side of the root canal facing upwards on the microtomography's turntable.

Images were acquired according to the following parameters: 180° rotation, 1° rotation step, 26.7 μm isotropic voxel size and 0.5 mm aluminum filter, totaling an average scanning time of 40 min for each sample. The two-dimensional projections were archived in Tagged Image File (TIFF) format and used for three-dimensional reconstruction using NRecon v.1.6.6.0 software, with a "Ring artefact reduction" value of 5, "Beam hardening" of 40%, "Contrast histogram" between 0.001 and 0.15 and "Smoothing" of 3. The reconstructions were saved in Bitmap (BMP) format.

2.5. Filling of the Root-End Cavities

The hydraulic cements used in this study are listed in Table 1.

The specimens were reinserted into the aluminum rings with wax and then randomly divided into four groups using a random number generator (https://www.random.org/lists) [25]. Each group (n = 10) was assigned a different cement: MTA Angelus, Bio-C Repair, Biodentine, and Cimmo HD. The hydraulic cements were handled according to the manufacturer's instructions. Prior to inserting the cement, an R50 main gutta-percha cone (VDW GmbH, Munich, Germany) was inserted in the cervical-apical direction and locked at the root canal's limit with the root-end cavity, simulating the obturation [22].

The cavities were filled with the cements according to each manufacturer's instructions, which were gradually inserted into the root-end cavity. After insertion, the cements were compacted with a manual micro compactor (MPolachini, São Paulo, SP, Brazil) to completely fill the root-end cavity. The specimens were wrapped in gauze and stored at 37°C and 90% relative humidity for three times the time needed for the hydraulic cements to harden. After this period, the gutta-percha cone was removed.

Table 1. Hydraulic cements used in this study according to composition and manufacturer.

2.6. Filling Ability Analysis

The specimens were again removed from the wax and subjected to new micro-CT and image reconstruction using the same parameters as in the initial scan. The images from the final scan were aligned with those from the initial scan using the "3D registration" tool in Data Viewer v.1.5.1.2 software (Bruker-microCT, Kontich, Belgium). The post-obturation images were processed and analyzed using CTAn v.1.18.8.0 software (Bruker-microCT, Kontich, Belgium). The region of interest (ROI) was defined as the area of the root-end cavities: for the "Top" the most apical cut was selected, and for the "Botton" the cut corresponding to the next 3 mm coronal. Volumetric data were generated for subsequent 3D imaging.

The volume of the region of interest was calculated using CTAn v.1.18.8.0 software. The percentage of filling was determined by subtracting the initial volume (empty root-end cavities) from the final volume (filled root-end cavities). The results were converted into percentages based on the initial volume and stored in an Excel spreadsheet.

2.7. Bond Strength Analysis

The same specimens were subjected to the push-out test on the Instrom 2519-106 universal testing machine (Instrom, Canton, Massachusetts, USA), equipped with a load cell coupled to the oscillating system, at a speed of 1.0 mm/min. The specimens were fixed with the apical side of the root canal facing upwards and centered in stainless steel metal bases attached to the bottom of the universal testing machine, with a 2 mm diameter hole in its central portion. The specimens were aligned with the shaft used to compress the cement (diameter 1 mm, length 5 mm), ensuring that the shaft was centered under the root canal material and did not encounter the dentin. The testing machine was driven at a constant speed of 1.0 mm/min until maximum tension was reached.

Fig. 1. Schematic drawing of the push-out test simulation, with the arrow pointing in the direction of the shaft movement. A: push-out shaft; B: root-end filling material; C: root; D: wax; E: aluminum ring.

The force (F) required for displacement was measured in Newtons (N). To calculate the bond strength, the resulting force was converted into tension (σ), in Megapascals (MPa), by dividing the force value by the area of adhesion of the luting material (SL) in mm². The formula used was: σ = F/SL, and the approximate calculation of the area (SL) was: SL = πDg + (πD²/4 − πd²/4), where "D" refers to the average radius of the root-end cavity in mm, "d" the average radius of the root canal in mm, and "g" the relative height of the root-end cavity in mm. The relative height (g) of the slices was measured using a digital caliper (Digimess Instrumentos de Precisão Ltda, São Paulo, SP, Brazil) and the radii using a Leica M165C stereomicroscope (Leica Mycrosystems, Wetzlar, Hessen, Germany) with LAS v4.4 software. The bond strength (BS) was calculated in MPa as BS = F/SL.

2.8. Failure Mode Analysis

After the bond strength test, the slices were evaluated for the type of failure mode under a Leica M165C stereomicroscope, using LAS v4.4 software, at 25× magnification. The failures observed were classified into: a) adhesive to dentin: when the root-end filling material dislodged from the dentin; b) cohesive to dentin: when there was a fracture in the dentin; and c) mixed: when the root-end filling material dislodged from the dentin and there was a fracture in the dentin.

2.9. Statistical Analysis

For the analysis of filling ability and bond strength, the data was expressed as mean values and standard deviations and statistically analyzed for normality using the Shapiro-Wilk test (P > 0.05), and homogeneity of variance using the Levene test (P > 0.05). One-way ANOVA was used to evaluate the influence of the type of root-end filling material on the bond strength values and percentage of filling. Tukey's post-test was used for multiple comparisons between the groups. The chi-square test was used to assess the association between the type of failure and the type of cement after the bond strength test (P = 0.05). All statistical analyses were carried out using Jamovi software v.1.6.23 (The Jamovi Project, Sydney, Australia), with the probability level set at 95%.

3. Results

A lower percentage of gaps was observed in the root-end cavities filled with Bio-C Repair, Biodentine and MTA Angelus cements when compared to the root-end cavities filled with Cimmo HD cement (P < 0.05), with no significant difference between them (P > 0.05) (Table 2).

Fig. 2. Representative 3D image of the filling material gaps in the specimens. A: frontal view; B: gutta percha-sealer interface; C: apical view.

Regarding the bond strength of the materials, Biodentine and MTA Angelus cements showed higher bond strength values when compared to Bio-C Repair, with no statistically significant difference between them (P > 0.05). Cimmo HD showed intermediate bond strength values, with no statistically significant difference to MTA Angelus and Bio-C Repair (P < 0.05). Regarding the mode of failure, the chi-square test showed that there was a statistically significant higher prevalence of cohesive failures for root-end cavities filled with Biodentine and mixed failures for those filled with MTA Angelus, Cimmo HD and Bio-C Repair (P < 0.05) (Table 3).

Table 2. Mean and standard deviation of the percentage of gaps present in each root-end filling material evaluated (n = 10).

*Equal letters indicate statistical similarity between the lines, different letters indicate statistical difference between the lines.

Table 3. Mean and standard deviation of bond strength of hydraulic cements to dentin and percentage of failure mode (n = 10).

*Equal letters indicate statistical similarity between the lines, different letters indicate statistical difference between the lines. MPa = Megapascal.

4. Discussion

To achieve effective three-dimensional sealing of the root-end cavity, the hydraulic cements need to have good sealing capacity, dimensional stability, biocompatibility, and bactericidal and bacteriostatic properties [4], thus providing greater predictability in preventing contamination and infiltration of microorganisms and fluids from the periradicular region into the dentin, favoring treatment prognosis [8]. Hydraulic cements are widely used for filling root-end cavities due to their good biocompatibility, excellent sealing capacity, inhibition of pathogenic microorganisms and ability to promote healing of periapical tissues [13,26]. However, this material can have disadvantages such as being difficult to handle and manipulate [13]. As a result, new hydraulic cements with different compositions and forms of presentation have appeared on the market to facilitate the handling and insertion of the sealing material.

The use of the device to create an angulation of 45° and thus simulate the approximate angulation of the root during apical surgery was proposed previously [22] and used in this study. Performing the filling using an angled specimen, rather than on a flat surface, allows us to get closer to the complexity of filling the root-end cavity during apical surgery, which is an important factor for better analysis of the quality of the filling and the bond strength of hydraulic cements. The filling ability of the different root-end filling materials was analyzed using micro-CT. This method allows the volume of the filling material and the gaps to be quantified, as well as providing three-dimensional visualization of the filling of the root-end cavities and differentiating between sealing materials, gaps, and dentin [27], and is an advantageous method because it allows repetition and is non-destructive.

The push-out test was used to assess the bond strength of the root-end filling materials. This method is considered reliable, despite being subject to variables, as it measures sheer bond strength, where fracture occurs exclusively parallel to the cement-dentin interface [19,28]. The application of the push-out and failure mode tests is important for analyzing the bond strength of hydraulic cements in root-end cavities, particularly in situations where the integrity of the seal is crucial to the success of endodontic treatments [22,29].

In the method used as the basis for the test [22], the compressive force was applied in the crown-apex direction. However, it was very difficult to carry out the test without the metal rod touching the inner walls of the root canal. In view of this, it was decided to compress the sealing material in the apex-crown direction, due to the parallelism observed between the walls of the root-end cavities and the endodontically instrumented portion and the more detailed visualization of the interface between material and dentin, following the methodology used in a previous study [21]. High bond strength values of root-end filling materials can be beneficial in preserving the integrity of the cement-root dentin interface, achieved through micromechanical retention or the frictional resistance of these cements to the dentin wall [30].

The null hypothesis of this study was ruled out, as there was a statistically significant difference between the root-end filling materials tested in terms of both the percentage of gaps and bond strength. All the groups had gaps, but Biodentine, Bio-C Repair and MTA Angelus had fewer gaps when compared to Cimmo HD, with no statistically significant difference between them. Hydraulic cements are mainly composed of calcium silicates, which, as well as being biocompatible [31] and having osteoinductive capacity [32], have expansive and apatite-forming capacity, which fills the dentin-cement interface, improving sealing and making it easier to fill root-end cavities [33].

This was the first study to evaluate the ability of root-end cavity filling with Cimmo HD cement and its bond strength to root dentin. In this study, the root-end cavities filled with Cimmo HD had a higher percentage of gaps, which is probably related to the shorter setting time compared to the other materials evaluated. The setting time of Cimmo HD is only 5 min, while Biodentine is 12 min and Bio-C Repair and MTA Angelus 15 min, making the working time of Cimmo HD shorter, which may have negatively impacted the compaction of the material in the root-end cavity, resulting in the formation of more gaps.

In the present study, Biodentine showed higher bond strength values compared to Cimmo HD and Bio-C Repair. Biodentine has a high capacity for biomineralization [34], with calcium depositions forming cement tags at the dentin-cement interface, thereby promoting material adhesion to the dentin surface [35]. Both Biodentine and MTA Angelus have similar compositions; however, Biodentine's liquid contains calcium chloride, a water-soluble compound acting as an accelerator [36], reducing setting time and decreasing the probability of contamination and infiltration [37], thereby enhancing material adhesion to the dentin wall. These characteristics may also account for the cohesive failure mode observed in the Biodentine-treated group, as seen in previous studies [20,21,29], as it not only promotes significant adhesion but also induces linear expansion [33]. This expansion generates localized residual stresses, which may lead to cracks, increasing susceptibility to cohesive failure [21].

Angelus MTA showed higher bond strength values when compared to Bio-C Repair, but no statistically significant difference when compared to Biodentine and Cimmo HD. MTA was one of the first hydraulic cements to be used to fill root-end cavities [13]. The tricalcium oxide component of MTA reacts with the tissue fluid and forms calcium hydroxide, leading to the formation of biomineralized tissue with a hardening capacity, favoring marginal adaptation and sealing, generating retentive properties [26].

The root-end cavities filled with Bio-C Repair showed the lowest bond strength values when compared to Biodentine and MTA Angelus. This result can be attributed to the composition of Bio-C Repair, a pre-mixed cement that contains a lower concentration of calcium ions when compared to MTA and Biodentine [38], which can compromise the cement's adhesion to root dentin. Another associated factor may be its longer setting time [33], which is common in hydraulic pre-mixed cements [39]. Together, these conditions may contribute to a reduction in the bond strength of Bio-C Repair.

A mixed failure pattern was observed in the groups filled with MTA Angelus, Cimmo HD and Bio-C Repair, in contrast to previous studies in which adhesive [30] and cohesive [21] failures predominated in hydraulic cements. The greater solubility of hydraulic cements compared to other types of endodontic cements may be associated with this type of failure, since solubility can result in a reduction in the adhesive strength of the material to the dentin surface [40]. In addition, the heterogeneous particle size of hydraulic cements can make it difficult for them to penetrate the dentinal tubules uniformly, favoring their displacement [29].

The results presented in this study should be interpreted considering their limitations. We have attempted to reproduce clinical conditions as accurately as possible. However, due to the bond strength test, the root canals were not filled and a cone corresponding to the apical diameter was used. Another limitation may be related to the shape of the cavity, which, due to the use of specific inserts for this type of procedure, causes greater parallelism of the cavity walls. An additional aspect to consider is the variation in the setting expansion of the cements tested [41]. Future studies are crucial to improve application techniques and formulations of sealing materials, enhancing adhesion, and minimizing failures.

5. Conclusion

Based on the results, all the hydraulic cements studied showed gaps in the root cavities, with Cimmo HD standing out for having the largest amount. About bond strength, Biodentine and MTA Angelus showed higher values than the other materials. It was observed that the materials showed a mixed failure mode, except for Biodentine, which showed cohesive failures. Therefore, with the limitations of this study, it is suggested that Biodentine and MTA Angelus were considered the best options for filling root-end cavities, although more studies are needed to better understand the behavior of hydraulic cements in these cavities.

How to Cite

Garay Villamayor KG, Teodosio LM, Ramirez I, Prado HS, de Assis HC, de Sousa-Neto MD, Mazzi-Chaves JF, Lopes-Olhê FC. Comparative analysis of filling quality and bond strength among different root-end filling materials in root-end cavities. Int J Adhes Adhes. 2024;133:103757.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

CRediT Authorship Contribution Statement

Karen Gisselle Garay Villamayor: Conceptualization, Methodology, Writing - Original Draft, Investigation and Data Curation. Leonardo Moreira Teodosio: Formal analysis, Data Curation, Review, Editing and Project administration. Iago Ramirez: Validation, Methodology. Heitor Silva Prado: Validation, Methodology. Helena Cristina de Assis: Data Curation, Review, Editing, Validation, and Project administration. Manoel Damião de Sousa-Neto: Supervision and Resources. Jardel Francisco Mazzi-Chaves: Data Curation, Visualization and Resources. Fabiane Carneiro Lopes-Olhê: Writing – Review, Editing and Project administration.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data Availability

Data will be made available on request.

Acknowledgments

The authors are grateful to Coordination for the Improvement of Higher Education Personnel (CAPES) for financial support, Research Ethics Committee (REBEC) for the study review and approval. The authors deny any conflicts of interest related to this study. The data that support the findings of this study are available on request from the corresponding author.

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