Background

Post-extraction atrophy of the alveolar bone is a chronic, progressive, irreversible and cumulative process [1]. Severe mandibular atrophy includes Cawood — Howell class V and VI that implies complete loss of alveolar bone with atrophy of the underlying basal bone [2].

Dental implants (DI) significantly changed the concept of treatment of severe mandibular atrophy. However, their insertion is not always possible due to minimum residual native jaw. Many surgical techniques have been proposed to solve this problem. Some of them involve dental implantation without bone grafting, while others imply preliminary alveolar bone reconstruction [3–5].

In 1996, W. Bähr first reported reconstruction of the upper jaw for severe atrophy with a vascularized fibular autograft (VFA) [6]. Subsequently, many authors reported this method for reconstruction of severely atrophied upper jaw [7], mandible [8, 9], upper and lower jaws [5, 10–14], and even one-stage reconstruction of both jaws with one VFA [15].

The purpose of the study was to analyze the vascularized fibular autograft for reconstruction of alveolar part of the mandible with severe atrophy appreciating bone stability after dental implant insertion and prosthetic rehabilitation with implant-supported devices.

Material and methods

This study included 10 patients with complete loss of teeth and severe atrophy of the lower jaw (Cawood — Howell class V–VI) with favorable somatic status or compensated concomitant diseases and no contraindications for microsurgical reconstruction. The study was carried out in accordance with the recommendations of the Declaration of Helsinki and approved by the ethics committee of the National Medical Research Center of Dentistry and Maxillofacial Surgery. All patients signed an informed consent to participate in the study.

Preoperative examination of patients included analysis of anamnestic data, physical and laboratory survey to identify the risk factors for microsurgery.

Computed tomography (CT) (Aquilion PRIME, Toshiba Medical Systems, Japan) of head and legs with angiography and Doppler ultrasound (Mylab Twice, Esaote SpA, Italy) were performed to assess anatomy and hemodynamic capacity of arteries in recipient and donor zones. CT-based virtual planning of reconstructive surgery was performed in a special computer environment (Amira 5.4.5, Visage Imaging, Germany).

Surgery was performed under general anesthesia. Two surgical teams worked simultaneously in donor and recipient areas. Recipient bed was prepared via an incision along the residual ridge of the jaw extending from one retromolar space to another one. We formed vestibular and lingual muco-periosteal flaps and preserved submental and lower alveolar neurovascular bundles. The atrophied body of the lower jaw was completely skeletonized with preservation of muscle attachment to the mental spine. Recipient vessels were dissected through a 3–4 cm skin incision along the upper cervical fold in submandibular area.

Fibular autograft was elevated using a lateral approach with a 2–3 mm muscle cuff on its surfaces. Subsequent modeling was performed. For alveolar part reconstruction, we applied one wedge-shaped osteotomy with formation of two bone fragments of autograft. Acute angle obtained after V-shaped approximation of two fragments was sawed off. Thus, the frontal segment of the reconstructed alveolar part was formed.

Fibular autograft was transferred to the recipient bed after cutting off the vascular pedicle on the lower leg. Postoperative donor wound was sutured in layer-by-layer fashion with vacuum-assisted drainage. The autograft was fixed by screws and/or plates to the frontal part and rami of the lower jaw with a 3–4 mm diastasis between the autograft and lateral parts of the jaw. This diastasis was required to prevent traumatic compression of exposed mental or lower alveolar neurovascular bundles. The vascular pedicle passing along the vestibular surface of the reconstructed alveolar part was passed through a soft tissue tunnel into submandibular region and anastomosed with recipient vessels (Fig. 1). Postoperative wounds were sutured.

Fig. 1. Scheme of alveolar part reconstruction.

a — mental neuro-vascular bundle; b — fibula flap consisting of two bone fragments; c — fibula flap vascular pedicle; d — neck recipient vessels.

Dental implantation was carried out in 3–4 months after reconstructive surgery. Orthopedic rehabilitation was completed in 3–4 months after dental implantation.

CT-based morphological assessment of the atrophied and reconstructed mandible was carried out in a special software environment (RadiAnt DICOM Viewer 4.6.5, Medixant, Poland). All measurements were performed in multiplanar reformation and 3D reconstruction modes.

We applied cephalometric method proposed by Tallgren A. to analyze the height of atrophied and reconstructed mandible, as well as vascularized fibular autograft [16]. We used the following reference points: md1 — intersection of bisector of gonial angle with retromolar triangle; md5 — the highest and posterior part of lower jaw symphysis; md6 — the highest point of lower jaw symphysis; md7 — the highest and anterior part of lower jaw symphysis; md1, md2, md3, md4, md5 — points at the same distance from each other in relation to mandibular plan marked by a line passing through the 2 lower points of the lower edge of the jaw (Fig. 2, a, b, c).

Fig. 2. Assessment of the height of atrophied (a) and reconstructed (b) mandible, as well as free fibula flap (c) using cephalometric method proposed by A. Tallgren, et al. [16].

All measurements were performed before surgery, immediately after reconstruction, in 3–4 months after reconstruction, and in 3–6 months after orthopedic rehabilitation. Depending on the structure of interest, we measured the height from the above-mentioned points on the upper edge of the native mandible or those projected onto the upper edge of VFA, along perpendiculars to mandibular plan to the lower edge of the native lower jaw or VFA (Fig. 2, a, b, c).

According to Wical K.E. and Swoope C.C. [17], the distance between the lower edge of the mandible and inferior edge of the mental foramen is one third of initial mandible height. Considering these data, we estimated the height of the reconstructed lower jaw at the various stages.

Volumetric CT-based assessment of VFA at the same stages of treatment was performed using semi-automatic segmentation in InVesalius 3.1 software environment (Renato Archer Information Technology Center, Brazil). Structures of interest were initially segmented from +226 to +3071 Hounsfield units with subsequent manual processing. Intraosseous regions of metal structures, such as DI, were included into the autograft volume, since these structures were equal to the volume of tissue lost during formation of holes for their implantation.

Success of dental implantation was assessed 12 and 18 months later in accordance with the criteria proposed by Albrektsson T. et al. [18]: 1) no persistent pain or local dysesthesia, 2) no peri-implant inflammation, 3) no implant mobility, 4) no continuous peri-implant radiolucency, 5) peri-implant bone resorption < 1.5 mm within the first year and < 0.2 mm in subsequent years.

Statistical analysis

Statistical analysis was performed using mean and standard deviation. Significance of differences was determined using Student’s t-test and Wilcoxon’s test. Differences were significant at p-value <0.05.

Results

There were 10 women aged 36–65 years (mean 50 years) with complete loss of teeth and severe atrophy of the lower jaw for the period 2017 to 2019. All patients underwent complex rehabilitation including microsurgical reconstruction of the alveolar part of the lower jaw with subsequent dental implantation and prosthetic rehabilitation with implant-supported devices.

The main complaint was instability of complete removable dentures and preferable fixed dentures for better fixation. The period of complete loss of mandibular teeth ranged from 9 to 28 years (mean 18 years). All patients used complete removable dentures throughout this period. The causes of tooth loss included periodontitis, parodontitis, and Langerhans cell histiocytosis.

Postoperative period after microsurgical reconstruction was uneventful. There were no postoperative complications in donor area, except for a few cases of transient edema of the lower leg and foot. Compression bandages were effective in these patients. Walking function was completely recovered in 4 months after fibular flap harvesting.

Height of the atrophied lower jaw before reconstruction was 12.40±2.20 mm, immediately after reconstruction — 21.20 ± 1.87 mm (significant augmentation by 8.80±1.71 mm, p<0.0001). In 3–6 months after onset of dental implant functional loading, height of the reconstructed mandible was decreased up to 20.04±1.84 mm. Thus, the total decrease was 1.16±0.22 mm or 5.48±1.05% (Fig. 3).

Fig. 3. Changes in mandibular body height at different stages of treatment.

I — before reconstruction; II — immediately after reconstruction; III — 3–4 months after reconstruction; IV — 3–6 months after prosthetic rehabilitation with implant-supported devices.

The height of VFA transplanted for correction severe lower jaw atrophy was 11.24±1.10 mm. In 3–6 months after orthopedic rehabilitation, VFA height was 10.25±1.11 mm, i.e. total vertical loss was 0.99±0.52 mm (8.79%). Thus, VFA preserved 91.21% of the primary height throughout the maximum follow-up period (14 months) after reconstruction (Table).

Table. FFF height at different stages of treatment

Stage of treatment	Mean, mm	Standard deviation, mm	Changes in comparison with previous stage, mm	Standard deviation, mm	p-value	Significance
I	11,24	1,10	—	—	—	—
II	10,76	1,04	–0,48 (–4,26%)	0,52	8,54E-03	*
III	10,25	1,11	–0,51 (–4,53%)	0,21	1,62E-05	***
Total	—	—	–0,99 (–8,79%)	0,52	0,000281	**

Note. * — p<0.05 (significance >95%); ** — p<0.001; *** — p<0.0001. I – immediately after reconstruction; II – 3–4 months after reconstruction; III — 3–6 months after implant-supported prosthetic rehabilitation.

Analysis of VFA height decrease at various stages revealed no significant differences in vertical bone resorption (p=0.79). The process appeared to be linear (0.16 mm per a month).

We estimated initial lower jaw height in accordance with a formula proposed by Wical K.E. and Swoope C.C. In our patients, this value was 21.17±3.76 mm. Immediately after reconstruction, we restored lower jaw height up to 21.20±1.87 mm. Thus, the difference between the mandible height after reconstruction and the calculated value was 0.03±3.17 mm (0.14%, p=1). In 3–6 months after orthopedic rehabilitation, mandible height was 20.04±1.84 mm, i.e. height loos was equal to 1.14±3.05 mm (5.38%, p=0.16).

According to semi-automatic CT data segmentation, initial VFA volume was 9.42±1.71 cm³. In 3–6 months after orthopedic rehabilitation, VFA volume was 8.96±1.61 cm³ (insignificant change by 0.46±1.14 cm³, p=0.24). Interestingly, VFA enlargement was observed in 2 out of 10 cases by 1.22 (12.8%) and 1.71 cm³ (22%), respectively. These measurements were obtained after DI functional loading. This fact is also clearly seen in one of the patients during othopantomography (Fig. 4).

Fig. 4. Orthopantomography immediately after reconstruction (a) and in 4 months after functional loading on dental implants (b).

Revealing free fibula flap enlargement with closure of diastasis by bone tissue apposition (arrows).

In total, 46 dental implants (OsseoSpeed, Astra Tech Implant System, USA) were inserted in 4 months after reconstruction. Their diameter was 3.5–4.0 mm, length — 9–13 mm. In 9 out of 10 cases, 6 dental implants were inserted on the reconstructed jaw (3 implants in each VFA fragment). Only in one case, we used 4 dental implants (2 for one VFA fragment) due to smaller mandible. This was a patient with Langerhans cell histiocytosis and concomitant growth hormone deficiency. The implantation success rate determined by the criteria of Albrektsson T. et al. was 100% in 14 months after the procedure.

In 11 months after reconstruction, rehabilitation was completed by implantation of complete acrylic orthopedic structures with a metal frame with screw fixation on the dental implant and restoration of 12–14 teeth of the lower jaw in all patients.

All patients were satisfied with aesthetic and functional result after complex rehabilitation and returned to a long-forgotten normal diet.

There were no cases of claw hallux or dorsiflexion. No gait disturbance was noted in 6 and 12 months after flap harvesting. All patients were free in their daily activities and did not need help or support.

A 65-year-old female with a total loss of teeth in the lower jaw for 28 years is shown in Fig. 5 and 6.

Fig. 5. Clinical case. 65-year-old patient with total loss of lower jaw teeth lasting 28 years.

a — patient’s intraoral view with complete removable dentures at admission; b — exposure of intraosseus part of 4 dental implants previously inserted in the frontal segment due to severe bone resorption; c — CT imaging of severe mandibular body atrophy with resorption of periimplantar bone; d — virtual planning of reconstructive surgery; e — mandibular body skeletization with preservation of muscle attachment to the mental spine (arrow); f — pedicled free fibula flap; g — postoperative CT; h — dental implantation virtual modeling; i — dental implants inserted in the reconstructed mandible; j — fixed healing abutments; k — control orthopantomography; l — final prosthetic rehabilitation with implant-supported devices.

Fig. 6. Facial appearance of 65-year-old patient (with complete loss of lower jaw teeth) before (a) and after (b) complex rehabilitation.

Discussion

No physiological stress in relation to edentulous jaw results its resorption. Pressure on the bone by conventional removable denture and period of teeth loss are the factors accelerating this process. It is known that severe lower jaw atrophy is more common in females [19]. We observed the same fact, all our patients were females.

Two out of 10 our patients had bilateral extramandibular course of inferior alveolar nerve (throughout 1.70 and 1.78 cm in one case, 1.32 and 1.21 cm in other case on the right and left, respectively) due to resorption of the upper wall of the mandibular canal.

Currently, dental implantation is a valuable treatment option for patients with tooth loss, since this method reduces bone loss and even stimulates bone de novo via apposition after functional loading [20]. However, height of 10 mm and width of 5 mm are minimal bone dimensions required for successful implantation in case of lower jaw [21].

Lower jaw fracture in patients with atrophy is a formidable complication associated with dental implantation. This event is followed by severe consequences and difficult treatment. False joint and osteomyelitis occur in 48% of cases [22].

Currently, there are various treatment methods for these patients with less biological and economic cost including insertion of short implants (<7 mm) [23, 24] and All-on-4 concept [25]. The last one implies insertion of all 4 dental implants between the mental holes of the lower jaw with a minimum dimensions of 4 × 10 mm (two mesial in vertical position and two distal in posteriorly inclined position). However, these methods do not ensure lower jaw reconstruction and focus on circumvention of anatomical structures. All this leads to some compromises, i.e. the use of taller dentures to achieve the occlusal plane and consoles for posterior teeth restoration.

It is known that vascularized bone autografts are widely used for facial skull defects and deformities. VFA is preferred for reconstructive microsurgery in patients with extensive and combined maxillofacial defects [26–28].

Jaw reconstruction in patients with severe atrophy may be also performed with vascularized bone autografts. Resorption of these grafts is more linear compared to avascular bone autografts [29].

According to various data, VFA resorption makes up 2–17% [29–31]. We observed mean vertical VFA resorption of 0.99 mm with preservation of 91.21% of initial height in 14 months after transplantation. Thus, we obtained similar data.

VFA is the least susceptible to resorption and retain up to 95% of its original volume in 2 years after transplantation [32]. In our study, VFA preserved 95.11% of own initial volume in 14 months after transplantation.

The phenomenon of VFA “hypertrophy” is usually described in the literature after reconstruction of upper and lower extremities. Incidence of this event is 37–90% [33, 34]. However, VFA hypertrophy is rarely reported in maxillofacial surgery. Some authors consider mechanical stress to be the main cause of this process [34]. Others explain VFA hypertrophy after mandibular reconstruction by subperiosteal apposition of a new bone [29].

Makiguchi T. et al. [30] reported VFA height increase in 21% of cases after mandibular reconstructions. The authors found the number of osteotomies and female sex as predictors of fast resorption of the autograft. Delayed dental implantation reduced resorption. Pressure exerted by the tongue, lips, upper teeth and food is transmitted by VFA via dental implants and can contribute to development of bone tissue de novo.

Considering semiautomatic CT data segmentation, we found VFA enlargement by 12.8% and 22% in 4 months after the onset of dental implant functional loading in 2 out of 10 patients. We attribute these cases to periosteal type of “hypertrophy” of vascularized bone autograft in accordance with the classification proposed by De Boer H.H. [34]. Good consolidation of VFA with native mandible was accompanied by closure of diastasis between these structures (Fig. 4).

Previously, the authors left the partially exposed fascia [8], muscle cuff [15] or periosteum [13] of autograft in the oral cavity during lower jaw reconstruction for severe atrophy. Subsequent prolonged (6–8 weeks) healing resulted keratinized mucous membrane. We preferred primary closure of postoperative wound in the oral cavity with suturing the vestibular and lingual mucoperiosteal flaps. This approach eliminates the need for long-term follow-up and subsequent correction of soft tissues. Moreover, displacement and suturing the mobilized mucoperiosteal flaps over the reconstructed jaw create the effect of soft tissue lifting of the lower third of the face.

Earlier methods included fibular autograft modeling with dissection of 3 bone fragments for reconstruction of the alveolar part of the lower jaw [9, 11, 12, 15]. In our opinion, 2 bone fragments are sufficient for this purpose. Application of 1 osteotomy reduces surgery time and minimizes the incidence of possible complications.

Conclusion

VFA ensures reconstruction of the alveolar part of the lower jaw throughout the entire length with subsequent DI and implant-supported prosthetic rehabilitation. Despite the difficult technique, this approach is followed by predictable functional and aesthetic outcomes in certain cases of severe atrophy of the lower jaw, such as extramandibular course of inferior alveolar nerve, previous radiotherapy and unsuccessful bone grafting or implantation. VFA enlargement after transplantation is considered as functional adaptation in response to biomechanical loading on the bone through the dental implants under neoanatomical conditions.

The authors declare no conflicts of interest.