Root coverage with apical tunnel approach using propolis as a root conditioning agent: A case report with 2‐year follow‐up and review of the literature

Abstract Objectives One of the main challenges in performing root coverage is patient discomfort and donor site morbidity. This case report presents a minimally invasive apical tunnel surgical technique, with propolis for root conditioning, to correct gingival recession defects without harvesting donor grafts, flap elevation, or sutures. Propolis is a natural anti‐infective, anti‐inflammatory, and antioxidant agent. Material and Methods A 58‐year‐old woman with no significant medical history was presented for root coverage of her upper left canine and first premolar with recession type (RT)1A (+). Propolis was used as a root conditioning agent to promote soft tissue coverage via an apical tunnel approach. During the apical tunnel approach, a small apical hole was made 6 mm below the mucogingival junction, and the mucosa and associated attached gingiva was away from the tooth so the flap could be repositioned coronally. Collagen matrix was used as a soft tissue graft material. Results At the 2‐month, 6‐month, 8‐month, and 2‐year follow‐up, complete root coverage was achieved for both teeth. No bleeding on probing was noticed nor recurrent GRs at the treated sites. Conclusion Without incisions, donor site reflection, or flaps, the apical tunnel approach can be successfully used to cover the exposed roots. Additionally, propolis is a potential root conditioning agent during soft tissue graft procedure due to its anti‐inflammatory and antioxidant properties.


| INTRODUCTION
Periodontal plastic surgery is performed to address mucogingival defects. The apical movement of the gingival margin brought on by various diseases or illnesses and linked to clinical attachment loss is now known as gingival recessions (GRs) according to the 2018 World Workshop classification (Romandini et al., 2020). Numerous surgical techniques have been employed to correct GRs (Stefanini et al., 2023).
Despite the large number of research that has been conducted on this topic, the main challenges continue to be surgical considerations, time constraints, and patient discomfort. According to the American Academy of Periodontology, the mean root coverage of GRs varies from 67% to 86%, depending on the surgical approach and prognosis of the GR defect. Also, the position of the tooth within the arch, the thickness of the gingival biotype, and the existence or absence of keratinized tissue are considered challenging factors (Javaid et al., 2020).
Apical tunnel surgical (ATS) techniques, such as the pinhole approach, are a minimally invasive surgical procedure that reverses GRs without the need for donor grafts, flap elevation, or sutures (Beck, 2018;Chao, 2012). The alveolar mucosal tissue is punctured with a needle. Through this tiny opening, specialized tools are used to gently release the gingival tissues and move the gingiva to cover the exposed root surface. By doing this, all muscle and fibrous adhesions are broken up, allowing the flap to move freely and tension-free in the coronal direction (Chao, 2012).
Several biologics have been proposed to be used for root conditioning agents during the root coverage procedures (Ahangari et al., 2018). Propolis refers to a broad range of resinous materials that honeybees gather from plant parts, buds, and exudates (Martinotti & Ranzato, 2015). Propolis has been used in dentistry (Ahangari et al., 2018) due to its ability to condition the roots and to promote faster healing, as well as to act as an anti-infective, antiinflammatory, and antioxidative agent (Velazquez et al., 2007). It has been demonstrated that propolis is efficient against oral bacteria, pointing to its potential as an anti-periodontal pathogen, including Porphyromonas gingivalis, as well as an anti-cariogenic agent (Coutinho, 2012;Fard, 2022). Also, Galangin, genistein, quercetin, resveratrol, caffeic acid, and caffeic phenyl ester are active substances found in propolis that enhance its antiseptic, antibacterial, antifungal, antiviral, and immunomodulatory properties (Martinotti & Ranzato, 2015). Literature has also shown propolis is able to trigger an increase in extracellular matrix components during early wound repair thus lead to stimulation of the transforming growth factor-ß (TGF-ß) expression in promoting hemostasis and control inflammation (Martinotti & Ranzato, 2015).
Despite its feasibility, the ATS still lacks evidence regarding its long-term outcomes. Therefore, the aim of this case-report was to present a GR case that was successfully managed with ATS along T A B L E 1 The characteristics of the included studies in the literature review. The results of this review revealed a lack of sufficient evidence on the long-term outcomes of the apical tunnel surgical (ATS) technique.

| Clinical and periodontal examination
Initially, periodontal examination was performed. (Figure 1) presents the baseline clinical findings. The average plaque index was 0.9. The patient expressed that she manually cleaned her teeth using a horizontal motion brushing technique, twice daily without any auxiliary tools.

| Treatment considerations and surgical procedure
According to AAP World Workshop classification, teeth #11 & #12 were classified as RT1 A (+) (Cortellini & Bissada, 2018). The patient declined to receive an autogenous soft tissue graft. Thus, the ATS technique was indicated for her to cover the exposed root surfaces.
The phase I treatment was performed before the surgical phase. The ATS was employed by utilizing propolis as a root conditioning agent to enhance clinical outcomes and healing. Figure 1e-j depicts the surgical steps. After the surgery, the post-op instructions were given, additionally, she was asked to apply a propolis paste twice daily for the first week. After 10 days following the surgery, chlorohexidine mouthwash was prescribed to avoid any physical disruption. After 4 weeks, the patient was told to brush in vertical strokes. F I G U R E 1 Probing depth (PD) was 1 mm in the midfacial region for both teeth without any bleeding on probing (a, b). The recession height was 4 mm in tooth #11 (a) and 2 mm in tooth #12 (b), and the width of keratinized tissue (WKT) was 2 mm for both teeth (a-c). A preoperative periapical radiograph was taken, the affected teeth showed no signs of interproximal radiographic bone loss as well as no interproximal attachment loss (d). Only a slight amount of gingival inflammation was seen, along with rolled marginal gingiva and blunted interdental papillae. First, scaling and root planing was performed to prepare the teeth for phase II treatment (e). Local anesthetic infiltration was performed and applied propolis paste using a cotton pellet to condition the roots for 3 min (f). Then pierced an apical hole of 4 mm above the mucogingival junction (MGJ) apical to the recession defect (g). The gingiva then pushed downward until it is coronal to cementoenamel junction, using a curved Orban's knife and tunneling tools to loosen gingival tissues. Full-thickness splitting was accomplished, resulting in free mobile gingiva (h, i). To help and hold the gingiva in its coronal position, one-piece of CenoMembrane, an allograft collagen matrix (size: 10 × 10 mm, thickness: 0.6-0.9 mm, CenoBiologics Ltd-Tissue Engineering, United Kingdom) was divided into small strips and placed through the hole to the interdental papillae, as illustrated in (j). To keep the gingiva in its new position, gentle digital pressure was applied for 3 min. Propolis was then reapplied to the gingiva for an additional 3 min. The 2 months (k), 6 months (l), 8 months (m), and 2 years (n) follow-ups showing complete root coverage. The pocket depth was 2 mm for both teeth #11 and #12 during all follow-up visits (k-n). WKT of both affected teeth increased to 3 mm and remained the same during all follow-ups (k-n). Post-op peri-apical X-ray taken at the 2 years follow-up showed no bone level change when compared to baseline (o).

| DISCUSSION
In this report, we demonstrated that a successful root coverage was achieved and maintained for 2-year after ATS. In this case, propolis was used as a root conditioning agent. To the best of our knowledge, this is one of the first case reports that used this combination to manage the GR defect.
The advantages of this minimally invasive surgical procedure comprise coverage of the exposed roots without the need for an incision, a donor site, with providing rapid esthetic outcomes, and taking less chair-time, and covering multiple GRs. Propolis has been utilized in several other periodontal procedures with improved clinical outcomes (enhanced wound healing and reduced inflammation) (Filho & Carvalho, 1990;Nakao et al., 2020;Zohery et al., 2018). Hence, it is our intent to apply propolis to condition the exposed root surface because it is a natural anti-infective and antioxidant agent so it can minimize inflammation as well as speed up the healing process. Our observations confirm this finding, since no surgical bleeding or inflammation was observed. This may be related to the anti-inflammatory properties of propolis, which inhibits lipoxygenase and cyclooxygenase enzymes, prevention of the conversion of arachidonic acid to prostaglandins and leukotrienes (Kuropatnicki et al., 2013), as well as the stimulation of expression of TGF-ß (Martinotti & Ranzato, 2015), that aids in hemostasis during wound healing.
Due to the minimally invasive nature of this technique, without separation of underlying tissue, less bleeding, improved access and visibility, and surgical time was experienced. This also explains why we did not note any complications during healing nor the formation of scars, which has further confirmed the biological and esthetic benefits of ATS approach (Anuroopa, 2018).
In both teeth #11 & #12, our findings showed an increase in gingival volume and thickness. These findings also supported others, who concluded that ATS could increase tissue volume and produce predictive results if the baseline tissue thickness is at least 0.8-1 mm.
Additionally, there was an improvement in thickness and width of keratinized tissue (WKT) in both teeth from the baseline to 8 months and remained stable at 2 years. This observation agreed with many of the previous findings (Anuroopa, 2018;Kuropatnicki et al., 2013;Nakao et al., 2020;Stefanini et al., 2023). Also, the rationale for using the collagen matrix in this technique was to maintain the level of gingival margin (Barootchi et al., 2022), as well as to modify the gingival phenotype (Barootchi et al., 2020). Moreover, collagen matrix is a noncross-linked, resorbable, and intended to promote angiogenesis and tissue integration (Barootchi et al., 2020), which all agree with our long-term results.
Nonetheless, the ATS also has some challenges such as technique sensitivity and the need for specialized instruments to elevate the flap without exposing the inner tissue, which raises the risk of flap proliferation. In addition to these, there is still a lack of quality research on the efficacy of this technique being supported by randomized controlled trials compared to other techniques. Therefore, despite the long-term feasibility of ATS that is shown in this case, the readers should be cautious about the limitations of the casereport nature of this study. Lastly, the results of the literature review regarding implementing ATS in root coverage procedures indicated a substantial gap in the higher level of evidence articles. Thus, it is suggested for future research to experiment on this technique and its feasibility within controlled trials with larger sample sizes.

| SUMMARY
The ATS technique is a method that shows promising results for treating GRs. The use of propolis paste for this technique should be taken into consideration for root cleansing and improved healing.
However, future randomized controlled trials are needed to validate the current findings.

AUTHOR CONTRIBUTIONS
None.