Bone Regeneration and Soft Tissue Enhancement Around Zygomatic Implants: Retrospective Case Series

Purpose: To present a case series of zygomatic implants combined with bone regeneration and soft tissue enhancement techniques to reduce the risk of biological delayed complications such as maxillary sinusitis and soft tissue recession. Materials and methods: Zygomatic implants placed simultaneously with different bone regeneration techniques (buccal, palatal and buccal-palatal bone regeneration) and soft tissue enhancement techniques (pediculate and free connective tissue graft) were followed for at least 12 months. The following information was collected: patient age and sex, number of zygomatic implants, zygomatic implant success rate, zygomatic implant position according to classification of the Zygomatic Anatomy Guide Approach (ZAGA), sinus membrane perforation, type and outcome of the bone regeneration or the soft tissue enhancement technique, bone gain (width and length along the zygomatic implant) and keratinized buccal mucosa width, duration of follow-up, loading protocol (immediate or delayed) and biological complications (maxillary sinusitis and soft tissue recession). Results: Thirty-one zygomatic implants placed in 19 patients were included. All implants were successful and none of the implants presented biological complications. The bone regeneration technique was successful in 30 of 31 cases with a mean palatal bone width of 3 mm, buccal bone width of 2.65 mm, palatal bone length of 6.5 mm and buccal bone length of 8.3 mm. The success rate of soft tissue enhancement was 100% and it established at least 2 mm of keratinized buccal mucosa width in all implants. Conclusions: Within the limitations of the present study, bone regeneration and soft tissue enhancement techniques were useful to establish more favorable conditions of the peri-implant tissues around zygomatic implants. This could prevent biological complications such as maxillary sinusitis and soft tissue recessions. Prospective and randomized controlled clinical trials with longer follow-up periods are advisable.


Introduction
The original zygomatic implant placement technique was described by Branemark with a 97% of success rate in 81 treated patients [1]. The classical protocol introduced the placement of conventional implants in the maxillary anterior region in combination with posterior zygomatic implants through a palatal entrance and extensive sinus opening [1][2][3][4][5]. This method was proposed for the rehabilitation of atrophic maxillae (grade V and VI of Cawood-Howell classification [6]) without the use of Table 1. Patient selection criteria.

Inclusion Criteria Exclusion Criteria
Patient with indication for zygomatic implant treatment for atrophic maxillae (Cawood-Howell grade V and VI). Cases with less than 12 months of follow-up.
Zygomatic implants with simultaneous bone regeneration or enhancement of peri-implant soft tissue.
Incomplete medical history and incomplete radiographic examination.

Indication for Regenerative or Enhancement Method
Different techniques of bone regeneration and improvement of peri-implant soft tissues have been indicated depending on the emergence of the implant and the state of the alveolar process after implant placement ( Table 2). As a premise, it should be remembered that the coronal part of the implant has to obtain minimal peri-implant tissues [20][21][22]. gave their informed consent for inclusion before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the Ethics Committee of the University of Valencia (UV-INV_ETICA-1263997). The database of the Oral Surgery Unit (Department of Stomatology, Faculty of Medicine and Dentistry, University of Valencia, Spain) was consulted to collect the information.

Patient Selection and Operating Procedure
All patients were treated by the same oral surgeon (MPD) between June of 2016 and November of 2019. At the first appointment, a complete anamnesis, oral exploration and radiographic study (extraoral panoramic radiograph and cone bean computed tomography (CBCT) (Planmeca Promax ® 3D Max and 2D S3, Helsinki, Finland)) were made. The selection of the patients depending on criteria specified in Table 1.

Inclusion Criteria Exclusion Criteria
Patient with indication for zygomatic implant treatment for atrophic maxillae (Cawood-Howell grade V and VI).
Cases with less than 12 months of follow-up.
Zygomatic implants with simultaneous bone regeneration or enhancement of peri-implant soft tissue.
Incomplete medical history and incomplete radiographic examination.

Indication for Regenerative or Enhancement Method
Different techniques of bone regeneration and improvement of peri-implant soft tissues have been indicated depending on the emergence of the implant and the state of the alveolar process after implant placement ( Table 2). As a premise, it should be remembered that the coronal part of the implant has to obtain minimal peri-implant tissues [20][21][22]. Preserved. Non-existent.

Bone Regeneration
Peri-implant bone defects or thin buccal/palatal corticals were regenerated with a mixture of particulate synthetic bone graft (beta-phosphate tricalcium (KeraOs ®, Keramat, Spain)) with autogenous bone and resorbable collagen membranes (Creos Xenoprotect ®, Nobel Biocare, Sweden) fixed with surgical pins (Meisinger ®, Sanhigia, Spain). Management of the soft tissue without flap pressure was achieved through two-plane suturing (horizontal double and simple stitches). Bone regeneration was performed palatal, buccal or palatal and buccal. An example of buccal and palatal bone regeneration is illustrated in Figure 1.

Soft tissue enhancement
Total buccal emergence or more than half of the implant diameter outside the alveolar bone crest.

Bone Regeneration
Peri-implant bone defects or thin buccal/palatal corticals were regenerated with a mixture of particulate synthetic bone graft (beta-phosphate tricalcium (KeraOs ®, Keramat, Spain)) with autogenous bone and resorbable collagen membranes (Creos Xenoprotect ®, Nobel Biocare, Sweden) fixed with surgical pins (Meisinger ®, Sanhigia, Spain). Management of the soft tissue without flap pressure was achieved through two-plane suturing (horizontal double and simple stitches). Bone regeneration was performed palatal, buccal or palatal and buccal. An example of buccal and palatal bone regeneration is illustrated in Figure 1.

Bone Regeneration
Peri-implant bone defects or thin buccal/palatal corticals were regenerated with a mixture of particulate synthetic bone graft (beta-phosphate tricalcium (KeraOs ® , Keramat, Spain)) with autogenous bone and resorbable collagen membranes (Creos Xenoprotect ® , Nobel Biocare, Sweden) fixed with surgical pins (Meisinger ® , Sanhigia, Spain). Management of the soft tissue without flap pressure was achieved through two-plane suturing (horizontal double and simple stitches). Bone regeneration was performed palatal, buccal or palatal and buccal. An example of buccal and palatal bone regeneration is illustrated in Figure 1.

Bone Regeneration
Peri-implant bone defects or thin buccal/palatal corticals were regenerated with a mixture of particulate synthetic bone graft (beta-phosphate tricalcium (KeraOs ®, Keramat, Spain)) with autogenous bone and resorbable collagen membranes (Creos Xenoprotect ®, Nobel Biocare, Sweden) fixed with surgical pins (Meisinger ®, Sanhigia, Spain). Management of the soft tissue without flap pressure was achieved through two-plane suturing (horizontal double and simple stitches). Bone regeneration was performed palatal, buccal or palatal and buccal. An example of buccal and palatal bone regeneration is illustrated in Figure 1.

Buccal Soft Tissue Enhancement
Palatal rotated connective tissue flaps or free connective tissue grafts were performed to improve buccal soft tissues around the zygomatic implants. Palatal rotated flaps ( Figure 2) were fixed buccally to the zygomatic implants using resorbable sutures through small perforations created in the bone alveolar crest mesial and distal of the zygomatic implant. Free connective tissue grafts ( Figure 3) were collected from the palatal flap and fixed buccally around the coronal part of the zygomatic implants by two surgical pins.

Buccal Soft Tissue Enhancement
Palatal rotated connective tissue flaps or free connective tissue grafts were performed to improve buccal soft tissues around the zygomatic implants. Palatal rotated flaps ( Figure 2) were fixed buccally to the zygomatic implants using resorbable sutures through small perforations created in the bone alveolar crest mesial and distal of the zygomatic implant. Free connective tissue grafts ( Figure 3) were collected from the palatal flap and fixed buccally around the coronal part of the zygomatic implants by two surgical pins.

Immediate Loading
Immediate loading was performed when the zygomatic implants had primary stability (insertion torque at least 35 Ncm) and if demanded by the patient.

Follow-up
All patients were checked after two weeks (suture removal), at 6 months (second-stage surgery), at 8 months (prosthetic loading) and each year after prosthetic loading. A CBCT scan was performed to evaluate the bone regeneration and the health of the maxillary sinusitis at the 6 months. Protheses removal and prophylaxis were conducted every year.

Data Gathering
The following information was collected in all cases: patient age and sex, number of zygomatic implants, sinus membrane perforation, zygomatic implant position according to ZAGA classification [16], zygomatic implant success, type and success rate of the bone regeneration or of the soft tissue enhancement technique, bone gain (width and length along the zygomatic implant) or keratinized buccal mucosa width, duration of follow-up, loading protocol (immediate or delayed) and biological complications (maxillary sinusitis and soft tissue recession).
The evaluation of maxillary sinusitis and soft tissue recession was made by radiological study and clinical exploration. For maxillary sinusitis diagnosis, the CBCT images were evaluated at 6 months to discard maxillary sinus occupation and the clinical exploration assessed possible symptoms and signs at each follow-up visit such as: Facial pain or pressure, facial congestion or fullness, nasal obstruction, purulent discharge, hyposmia or anosmia, purulence on examination and fever [28]. For soft tissue recession, a clinical visual exploration was performed, and defects were measured through a periodontal probe.

Immediate Loading
Immediate loading was performed when the zygomatic implants had primary stability (insertion torque at least 35 Ncm) and if demanded by the patient.

Follow-up
All patients were checked after two weeks (suture removal), at 6 months (second-stage surgery), at 8 months (prosthetic loading) and each year after prosthetic loading. A CBCT scan was performed to evaluate the bone regeneration and the health of the maxillary sinusitis at the 6 months. Protheses removal and prophylaxis were conducted every year.

Data Gathering
The following information was collected in all cases: patient age and sex, number of zygomatic implants, sinus membrane perforation, zygomatic implant position according to ZAGA classification [16], zygomatic implant success, type and success rate of the bone regeneration or of the soft tissue enhancement technique, bone gain (width and length along the zygomatic implant) or keratinized buccal mucosa width, duration of follow-up, loading protocol (immediate or delayed) and biological complications (maxillary sinusitis and soft tissue recession).
The evaluation of maxillary sinusitis and soft tissue recession was made by radiological study and clinical exploration. For maxillary sinusitis diagnosis, the CBCT images were evaluated at 6 months to discard maxillary sinus occupation and the clinical exploration assessed possible symptoms and signs at each follow-up visit such as: Facial pain or pressure, facial congestion or fullness, nasal obstruction, purulent discharge, hyposmia or anosmia, purulence on examination and fever [28]. For soft tissue recession, a clinical visual exploration was performed, and defects were measured through a periodontal probe.

Immediate Loading
Immediate loading was performed when the zygomatic implants had primary stability (insertion torque at least 35 Ncm) and if demanded by the patient.

Follow-up
All patients were checked after two weeks (suture removal), at 6 months (second-stage surgery), at 8 months (prosthetic loading) and each year after prosthetic loading. A CBCT scan was performed to evaluate the bone regeneration and the health of the maxillary sinusitis at the 6 months. Protheses removal and prophylaxis were conducted every year.

Data Gathering
The following information was collected in all cases: patient age and sex, number of zygomatic implants, sinus membrane perforation, zygomatic implant position according to ZAGA classification [16], zygomatic implant success, type and success rate of the bone regeneration or of the soft tissue enhancement technique, bone gain (width and length along the zygomatic implant) or keratinized buccal mucosa width, duration of follow-up, loading protocol (immediate or delayed) and biological complications (maxillary sinusitis and soft tissue recession).
The evaluation of maxillary sinusitis and soft tissue recession was made by radiological study and clinical exploration. For maxillary sinusitis diagnosis, the CBCT images were evaluated at 6 months to discard maxillary sinus occupation and the clinical exploration assessed possible symptoms and signs at each follow-up visit such as: Facial pain or pressure, facial congestion or fullness, nasal obstruction, purulent discharge, hyposmia or anosmia, purulence on examination and fever [28].
For soft tissue recession, a clinical visual exploration was performed, and defects were measured through a periodontal probe.
Bone regeneration success in cases with immediate loading was evaluated by CBCT images at 6 months. This evaluation was performed during the second-stage surgery in cases without immediate loading. Soft tissue enhancement success was based on the presence or absence of necrosis during the next two weeks after the implant placement.
Bone gain was measured in the CBCT images at 6 months in two directions: through a perpendicular buccal and palatal lines to the implant axis (width) [24] and through a parallel buccal and palatal lines to the implant axis at level of coronal part of the implant (length) (Figure 4). Keratinized buccal mucosa width was measured at 3 months in cases with immediate loading and at the removal of second-surgery suture in cases without immediate loading (< or > 2 mm of keratinized buccal mucosa width).
Materials 2020, 13, 1577 7 of 12 the removal of second-surgery suture in cases without immediate loading (< or > 2 mm of keratinized buccal mucosa width).

Results
Thirty-one zygomatic implants (13 Branemark System Zygoma ® zygomatic implants (Nobel Biocare T.H, Sweden) and 18 Smooth IPX-Tilted System ® zygomatic implants (Galimplant S.L, Sarria, Spain) were placed in 19 patients. The mean age was 61.7 years (54-73) and the gender proportion was 15.4% males and 84.6% females. Sinus membrane perforation during the surgery occurred in all cases. Immediate loading was performed in 41.9% of the total cases. The mean duration of follow-up was 20.1 months (range 12-41). Implant success rate was 100% and there were no biological complications.
Bone regeneration was performed around 16 zygomatic implants (Table 3). According to the ZAGA classification, 81.2% of the zygomatic implants with simultaneous bone regeneration were classified as ZAGA 1. Only one buccal regeneration failure among the total bone regenerations without implant failure was identified, due to presence of an infected fistula. The infected area was opened, the bone graft was curettage and retired, and irrigation with digluconate of chlorhexidine 0.12% was performed. The mean bone gain at 6 months showed that all successful cases obtained more than 2 mm of buccal and palatal bone width and length.

Results
Thirty-one zygomatic implants (13 Branemark System Zygoma ® zygomatic implants (Nobel Biocare T.H, Sweden) and 18 Smooth IPX-Tilted System ® zygomatic implants (Galimplant S.L, Sarria, Spain) were placed in 19 patients. The mean age was 61.7 years (54-73) and the gender proportion was 15.4% males and 84.6% females. Sinus membrane perforation during the surgery occurred in all cases. Immediate loading was performed in 41.9% of the total cases. The mean duration of follow-up was 20.1 months (range 12-41). Implant success rate was 100% and there were no biological complications.
Bone regeneration was performed around 16 zygomatic implants (Table 3). According to the ZAGA classification, 81.2% of the zygomatic implants with simultaneous bone regeneration were classified as ZAGA 1. Only one buccal regeneration failure among the total bone regenerations without implant failure was identified, due to presence of an infected fistula. The infected area was opened, the bone graft was curettage and retired, and irrigation with digluconate of chlorhexidine 0.12% was performed. The mean bone gain at 6 months showed that all successful cases obtained more than 2 mm of buccal and palatal bone width and length.
Soft tissue regeneration around zygomatic implants (Table 4) was performed in 15 implants. According to the ZAGA classification, 80% of the zygomatic implants with simultaneous soft tissue enhancement procedure were classified as ZAGA 1. No cases of soft tissue necrosis were recorded. The keratinized buccal mucosa width obtained was > 2 mm in all zygomatic implants.

Discussion
According to the literature, zygomatic implant therapy achieves survival rates between 92.3% and 100% [29]. Biological complications, such as maxillary sinusitis and soft tissue problems, have been reported [29].
Maxillary sinusitis is probably the most common biological complication with an incidence of up to 23.3% of all patients treated with zygomatic implants [30]. The coronal part of the implant is surrounded by an extremely atrophic alveolar bone crest, so marginal bone loss may easily result in an oroantral communication and consequent sinus infection [20,[31][32][33]. As this study describes, transforming the atrophic bone crest related to the coronal part of the implant through bone or soft tissue enhancement techniques seems to be a logical strategy for avoiding such problems.
Chow et al. [23] described a simultaneous sinus lift for reducing oroantral communications and subsequent maxillary sinus infections in zygomatic implants. This technique preserved the integrity of the sinus mucosa and the implants were surrounded by bone during their intrasinusal trajectory. According to Chow et al. [23] no patients suffered maxillary sinusitis over 6 to 24 months of follow-up. In the present study, the implant length surrounded by bone was only centered around the coronal part in contrast with the implant completely covered in Chow's technique. This postoperative bone-to-implant contact seems to be also enough to prevent maxillary sinusitis.
Hinze et al. [24] with Chow's technique described an increase in peri-implant bone around the coronal part of the implant (buccal bone 1.4 ± 0.5 mm and palatal bone 4.3 ± 0.4 mm) at 6 months. The results of this study showed similar bone gained width (buccal bone 2.65 mm and palatal bone 3 mm) at 6 months. The new bone regeneration approaches suggest new bone formation around zygomatic implants at the coronal level, as with other published procedures from CBCT images [24].
Some zygomatic implants needed palatal bone regeneration because the coronal part of the implant had been placed in a palatal position with respect to the residual bone crest. This regeneration method was derived from palatal-positioned conventional implants in atrophic maxillae grade IV [6]. Palatal positioned implants are anchored in the palatal cortical bone with 2 to 5 exposed implant threads in their palatal surface. Peñarrocha-Diago et al. [34] placed 330 palatal positioned implants with simultaneous palatal bone regeneration in 69 severely resorbed edentulous maxillae that were rehabilitated with total fixed prostheses. The success rate of palatal positioned implants was 97.8% with a follow-up of 2 years and the peri-implant soft and bone tissue showed same values as well-centered implants in non-atrophic zones [35]. The palatal regeneration technique was successful in the 7 zygomatic implants in which it was used, with a gained bone width and length of 3 and 6.5 mm, respectively. Some zygomatic implants needed buccal bone regeneration because the coronal part of the implant had a bone dehiscence, and more than the half of the implant was inside the bone alveolar crest. Wessing et al. [36] described that conventional implant survival was similar in simultaneous and deferred implant placements in guided bone regeneration with particulate graft materials and resorbable collagen membranes. Jung et al. [37] showed buccal bone width gain between 2-3 mm through CBCT measurements, such as the results of this study (2.65 mm).
The peri-implant mucosa around zygomatic implants may also present complications such as buccal dehiscence, with the exposure of implant threads in the oral cavity. Thus, the soft tissue enhancement technique may prove crucial in extramaxillary zygomatic implants because the coronal part stays lateral of the alveolar bone crest [15,18,19].
The extramaxillary approaches have yielded high success rates, with the prevention of maxillary sinusitis. Aparicio et al. [38] reported a 100% survival rate and no cases of maxillary sinusitis in 20 patients with 63 extramaxillary zygomatic implants with a follow-up between 12 and 24 months. The extrasinus technique was introduced by the authors to avoid sinus complications and bulky prostheses in the presence of pronounced maxillary wall concavities. Implant paths started with a "tunnel" osteotomy thorough the alveolar remain from the palatal side of the crest. Soft tissue problems were not observed, nor even imagined the possibility to occur, and subsequently they were not reported. However, the recession of buccal mucosa may be presented, and infective and aesthetic problems may be produced when treating not so concave or more atrophied anatomies [18,19].
As a solution to these soft tissue complications, Guennal et al. [25] dissected the buccal fat pad in 25 patients treated with 62 zygomatic implants and no buccal recessions were produced. Aparicio et al. [26] proposed the ZAGA "Scarf Graft" to gain width of keratinized mucosa around zygomatic implants through pediculate connective tissue flap. In the present study, pediculate connective tissue flaps (ZAGA Scarf graft [26]) or free connective tissue grafts were executed. More than 2 mm of keratinized buccal mucosa were present in all zygomatic implants. This minimum value of 2 mm of keratinized buccal mucosa seems to be preventive with respect to the marginal bone loss in conventional implants [21]. Soft tissue grafting procedures showed successful results obtained in conventional implants regarding to less rate of bleeding and marginal bone loss [39].
The potential advantage of these bone and soft tissue enhancement methods is to optimize peri-implant tissues surrounding of the coronal part of the zygomatic implant. This allows regeneration of the atrophic maxillary bone crest and the prevention of biological complications around zygomatic implants.
There are some limitations to this study: The study design was a retrospective case series (low scientific level) with a short follow-up and a small sample, the immediate loading protocol was sometimes subjected to the patient's demand and not only to the insertion torque value, and the measurement of the keratinized buccal mucosa was another aspect to improve because it was measured as a dichotomous value (major or minor than 2 mm). Therefore, prospective-controlled studies with sample size calculations, and longer follow-up times are necessary to prove if regenerative bone and soft tissue procedures reduce the occurrence of biological complications.

Conclusions
Within the limitations of the present study, bone regeneration and soft tissue enhancement techniques were useful to establish favorable conditions of the peri-implant tissues around zygomatic implants. This could prevent biological complications such as maxillary sinusitis and soft tissue recessions. Prospective and randomized controlled trials with a longer follow-up period are advisable.