A Retrospective Study of Clinical and Radiologic Outcomes of 69 Consecutive Maxillary Sinus Augmentations Associated with Functional Endoscopic Sinus Surgery Antonello Falco, PhD, DDS1/Cinzia Amoroso, MD2/Marco Berardini, DDS1/Lanfranco D’Archivio, MD3 Purpose: The aim of this clinical investigation was to evaluate the clinical and radiologic outcomes of a singlestep surgical procedure that includes functional endoscopic sinus surgery (FESS) and maxillary sinus elevation by the lateral window approach in patients with reversible contraindications to sinus elevation. Materials and Methods: Thirty-eight patients with insufficient bone height in the posterior maxilla caused by pneumatization of the sinus and with reversible ear-nose-throat (ENT) contraindications to sinus elevation were recruited for this investigation between January 2010 and January 2012. All patients were treated in a single session under general anesthesia for a total of 69 consecutive sinus augmentations. FESS was performed by an ENT specialist, and an oral surgeon carried out sinus elevation through the lateral window approach. Particulate xenograft was used beneath the sinus membrane. Intraoperative and postoperative complications (eg, membrane tears, rhinosinusitis, graft infection or loss) were reported. Nasal endoscopies were performed at 7, 14, and 30 days and 3 months after treatment. After a healing period of 6 months, 137 implants were inserted. Computed tomography scans were performed after 6 months and 1 year. Results: Intraoperative membrane perforation occurred in only one case. No implant failures were recorded during the follow-up period. Radiologic and clinical findings showed the resolution of ENT disease and good bone graft integration after 1 year. A relapse of mucosal thickening observed in some patients did not influence the graft healing. Conclusion: Preliminary rhinosinusal evaluation by an ENT specialist and computed tomography of the ostiomeatal complex are necessary in patients needing maxillary sinus elevation. A single-step approach to FESS and sinus elevation is a predictable technique to manage patients with ENT reversible contraindications to sinus elevation. Int J Oral Maxillofac Implants 2015;30:633–638. doi: 10.11607/jomi.3757 Key words: bone graft, chronic hyperplastic sinusitis, dental implants, functional endoscopic sinus surgery, maxillary sinus elevation, sinus membrane
T
he maxillary alveolar process undergoes irreversible bone resorption after tooth loss, which leads to both horizontal and vertical bone atrophy. The increased pneumatization of the maxillary sinus and atrophy of the alveolar bone consequent to this hard tissue resorption significantly reduce the amount of bone available for dental implant placement.1,2 Different surgical techniques have been developed to this effect to allow
1Private
Practice, Pescara, Italy. Physician, ENT and Maxillofacial Surgery Department, Lanciano Hospital, Chieti, Italy. 3Head, ENT and Maxillofacial Surgery Department, Lanciano Hospital, Chieti, Italy. 2 Attending
Correspondence to: Dr Marco Berardini, Via Galilei 8, 65122 Pescara (Italy). Fax: +390-85-7933050. Email: [email protected] ©2015 by Quintessence Publishing Co Inc.
implant-supported rehabilitation of the atrophied maxilla, including ridge augmentation through inlay bone grafts, Le Fort I osteotomy with bone graft interposition, maxillary sinus elevation, and onlay bone graft.3,4 Maxillary sinus grafting through elevation of the sinus membrane was first described by Tatum in 1977 and published by Boyne and James in 1980.5 This surgical technique allows vertical bone augmentation in the posterior maxilla via the formation of new bone between the sinus membrane and the maxillary sinus floor. Titanium dental implants could be inserted during the same surgical step or after a healing period of 6 to 9 months. The procedure is predictable, and published implant success and survival rates are higher than 90%.6–9 Different graft materials have been used to support bone regeneration beneath the maxillary sinus membrane: autogenous bone,10,11 demineralized allograft,12,13 freeze-fried bone allograft, alloplast,14,15 resorbable and nonresorbable hydroxyapatite,16 and xenografts.17 The International Journal of Oral & Maxillofacial Implants 633
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Falco et al
Although high success rates have been reported for this surgical technique, intraoperative or postoperative complications to sinus elevation surgery could have several negative effects on sinus homeostasis. Obstruction of the ostium of the sinus and secondary rhinosinusitis, periosteal inflammation, inhibition of ciliary mucosa,18–20 graft bacterial infection, membrane perforations, and penetration of graft material into the maxillary sinus21,22 are among the complications that may lead to graft and implant failure. Bacterial infection of a graft could spread to the orbit and endanger the patient’s life. It has been reported that patients with sinus membranes with circumferential thickness > 5 mm who are subjected to sinus elevation have a substantial risk of obstruction of the ostiomeatal unit and subsequent sinusitis.23 Reversible ear-nose-throat (ENT) contraindications to sinus elevation are represented by anatomical alterations of the region (ostium obstruction, sinus membrane hypertrophy), infectious-inflammatory processes (acute or chronic), sinus mucocele, and benign neoplasms of the rhinosinus area. Preoperative evaluation of the patient by an ENT specialist is thus necessary to identify these nasosinusal diseases. Accurate identification of those reversible contraindications to the sinus elevation procedure through evaluations (including nasal endoscopy) by an otorhinolaryngologist is essential.24 The patient, in case of ENT diseases, should be first treated by an ENT specialist and, in a subsequent surgical session, by the oral surgeon for maxillary sinus elevation. This will result in two surgical steps, with considerable discomfort for the patient. A one-step surgical procedure that includes maxillary sinus floor elevation in association with functional endoscopic sinus surgery (FESS) has been presented.25,26 This surgical treatment demonstrated good results in some patients with reversible contraindications to sinus elevation. It seemed appropriate to perform a clinical investigation of 69 treated maxillary sinuses to determine whether this surgical approach can be proposed as a predictable option to treat minor reversible contraindications to maxillary sinus floor elevation and perform bone augmentation at the same time. The aim of the present study was to evaluate the clinical and radiologic results of sinus elevation done through the lateral approach simultaneous with FESS in patients with reversible ENT contraindications.
MATERIALS AND METHODS Thirty-eight patients (total of 69 sinuses) with ages ranging from 36 to 59 years (mean age, 48 years) were recruited between January 2010 and January 2012 at Lanciano Hospital ENT and Maxillofacial Surgery
Department (Chieti, Italy). All patients were investigated with nasal endoscopy associated with panoramic radiographs and with maxillofacial computed tomography (CT) scans. The inclusion criteria were insufficient bone height (< 5 mm) in the posterior maxilla to receive dental implants associated with inflammatory diseases and anatomical alterations in the rhinosinusal region (eg, chronic hyperplastic sinusitis, mucocele, ostium obstruction, anatomical alterations of the nasal septum). The majority of cases involved asymptomatic hyperplastic chronic inflammatory disease of the maxillary sinuses. In some patients, this condition was bilateral. In 4 cases, a unilateral maxillary mucocele was found and removed. Sinusitis was treated with a functional correction of the nasal septum and radiodecongestion of the inferior turbinates in 5 patients, whereas in the other 33 cases, surgery on the ostiomeatal complex was sufficient to widen the ostium to support sinus ventilation. The patients were treated under general anesthesia in a single surgical session involving an ENT surgeon (who performed the FESS) and an oral surgeon who performed the sinus elevation via the lateral approach. The standard protocol involved intravenous anesthesia (remifentanil infusion) with orotracheal intubation. The patient was positioned at 30 to 40 degrees with the head up to facilitate venous return from the head and neck. The aim of FESS is to restore proper ventilation to the sinuses by widening the meatal ostium and removing any obstruction to sinus drainage. It is performed with different endoscopes assisted by video (for the maxillary sinus, these are angled by 30 to 45 degrees) and sharp, angled surgical tools. The endoscopic approach included, depending on the clinical circumstances, inferior uncinectomy, mucocele removal, septoplasty, or partial middle turbinectomy. Sinus elevation was performed by creating a lateral trapezoidal flap with a horizontal incision on the edentulous ridge and vertical incisions at least 1 cm from the edge of the mesial and distal antrostomy. The bony window was created with a 3-mm diamond bur at high speed under abundant irrigation with cold sterile saline solution. The window shape was ellipsoidal, with the horizontal longest margin parallel to the crestal margin. It was removed or eroded and the sinus membrane was elevated using periosteal instruments with rounded edges and different lengths, sizes, and angles. Bio-Oss xenograft (Geistlich) was inserted after membrane elevation. The biomaterial particles were 1 to 2 mm in size. The graft material was compacted to stabilize it between the bone walls and the sinus membrane. Hermetic and passive sutures were applied. Postoperative medical treatment included nasal emollient oil in the nasal cavity and oral chlorhexidine
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Falco et al
Fig 1a Meatus middle opening. Pus is present. Fig 1b Internal view of the maxillary sinus through the middle meatus. Fig 1c Suction of the suppuration using an endoscopic aspirator from the right sinus. Fig 1d Middle right antrotomy. Fig 1e Sinus elevation by the lateral approach. The bone window was created with a 3-mm diamond bur, and the membrane was elevated by periosteal instruments.
a
b
c
d
Fig 1f Preoperative CT scan showing pro- Fig 1g Control CT scan after 6 nounced hyperplasia of the sinus membrane. months showing graft healing and resolution of sinus membrane hyperplasia.
e
Fig 1h Control CT scan after 1 year of implant load. The ostiomeatal complex is open, and the graft shows good integration.
Fig 2a Patient no. 4, preoperative CT scan. The patient showed unilateral chronic sinusitis caused by blocked ventilation of the sinus. Fig 2b Patient no. 4, 6 months postoperative. The patient shows resolution of the chronic sinusitis. No complications occurred during the graft integration period. a
spray on the wound, broad-spectrum antibiotics (amoxicillin 1 g 1 pill twice daily by mouth for 7 days), and corticosteroids (Deflazacort 30 mg 1 pill twice daily for 5 days). Nasal packing with Merocel (Medtronic) was performed after the surgery in three patients and was removed on the second day. The patients were instructed to use saline solution for nasal rinse (twice daily for the following 10 days) and nasal drops of Nafazolina nitrate (7.5 mg) and Tirotricina (3 mg twice daily for 10 days). In all cases, a mask-type refrigerant (Hilotherm) was placed. Medical examinations and nasal endoscopies were performed at 7 days, 14 days, 30 days, and 3 months after sinus surgery. Dental implants (Biomet 3i, n = 137) were inserted according to the prosthetic plan after 6 months of healing. The implant sites were prepared using traditional burs without the use of osteotomes
b
because of the high density of the regenerated tissue. Insertion torque was above 45 Ncm for all implants placed. At 6 months and 1 year after sinus surgery, all patients were investigated with panoramic radiographs and CT scans. All patients were followed for at least 1 year. The parameters evaluated were intraoperative complications, postoperative complications, clinical and radiologic resolution of ENT disease, radiologic graft integration, and implant survival rate.
RESULTS Images from two treated patients are shown in Figs 1 and 2. In one case the sinus membrane was perforated intraoperatively; it was treated by application of a resorbable membrane (Bio-Gide, Geistlich). The International Journal of Oral & Maxillofacial Implants 635
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Falco et al
Table 1 Patient Data Patient Unilateral or no. bilateral surgery Age (y)
ENT disease
FESS surgical treatment
Complications
1
Unilateral
40
Chronic hyperplastic sinusitis
OMC surgery
None
2
Bilateral
58
Chronic hyperplastic sinusitis
OMC surgery
Graft site swelling
3
Unilateral
34
Sinusitis and nasal septum alteration
Nasal septum functional correction
None
4
Bilateral
56
Chronic hyperplastic sinusitis
OMC surgery
None
5
Bilateral
45
Chronic hyperplastic sinusitis
OMC surgery
None
6
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
7
Bilateral
36
Chronic hyperplastic sinusitis
OMC surgery
None
8
Bilateral
49
Sinusitis and chronic hyperplastic sinusitis
OMC surgery
Membrane perforation, graft site swelling
9
Bilateral
47
Chronic hyperplastic sinusitis
OMC surgery
None
10
Unilateral
48
Sinus mucocele
Mucocele removal/OMC surgery
None
11
Unilateral
40
Sinus mucocele
Mucocele removal/OMC surgery
None
12
Bilateral
51
Chronic hyperplastic sinusitis
OMC surgery
None
13
Bilateral
53
Chronic hyperplastic sinusitis
14
Bilateral
47
Sinusitis and nasal septum alteration
OMC surgery
None
Nasal septum functional correction
None
15
Bilateral
46
Chronic hyperplastic sinusitis
OMC surgery
None
16
Unilateral
43
Sinus mucocele
Mucocele removal/OMC surgery
None
17
Unilateral
55
Sinus mucocele
Mucocele removal/OMC surgery
None
18
Bilateral
50
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
19
Bilateral
52
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
20
Unilateral
54
Chronic hyperplastic sinusitis
OMC surgery
None
21
Bilateral
49
Chronic hyperplastic sinusitis
OMC surgery
None
22
Unilateral
43
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
23
Bilateral
44
Chronic hyperplastic sinusitis
OMC surgery
None
24
Bilateral
38
Chronic hyperplastic sinusitis
OMC surgery
None
25
Bilateral
42
Chronic hyperplastic sinusitis
OMC surgery
None
26
Bilateral
49
Chronic hyperplastic sinusitis
OMC surgery
None
27
Bilateral
59
Chronic hyperplastic sinusitis
OMC surgery
None
28
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
29
Bilateral
41
Chronic hyperplastic sinusitis
OMC surgery
None
30
Unilateral
48
Chronic hyperplastic sinusitis
OMC surgery
None
31
Bilateral
55
Chronic hyperplastic sinusitis
OMC surgery
None
32
Bilateral
51
Chronic hyperplastic sinusitis
OMC surgery
None
33
Bilateral
53
Chronic hyperplastic sinusitis
OMC surgery
None
34
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
35
Bilateral
45
Chronic hyperplastic sinusitis
OMC surgery
None
36
Bilateral
47
Chronic hyperplastic sinusitis
OMC surgery
Graft site swelling
37
Bilateral
58
Chronic hyperplastic sinusitis
OMC surgery
None
38
Bilateral
48
Chronic hyperplastic sinusitis
OMC surgery
None
Swelling of the graft site during the immediate postoperative period was reported by six patients (8.7%) and was resolved by an extension of medical intravenous therapy for 2 days. The sinus disease related to
impaired ventilation was resolved in all treated cases, as confirmed by clinical and radiologic examinations. Preoperative and postoperative patient data are summarized in Table 1.
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Falco et al
In all 69 sites, the radiographs (panoramic and CT scans) highlighted areas of regenerated hard tissue with homogenous radiopacity after 1 year. No areas of radiolucency in the graft, which might indicate inflammation or poor integration of the biomaterial, were detected in the radiographs. No implant failures were observed during the follow-up period. Periodic nasal endoscopy investigations (7, 14, and 30 days; 3 months; and 1 year) showed an open ostiomeatal complex, and no biomaterial particles were found within the maxillary sinuses. At 1 year, CT scans showed, in many cases, sinus membrane thickening with important reduction of ostium patency.
DISCUSSION It has been reported that maxillary sinus elevation may result in some intraoperative or postoperative complications, such as ostium obstruction and resulting sinusitis, graft infections, perforations of the sinus membrane with dislocation of biomaterial in the maxillary sinus, and acute purulent sinusitis. Certain anatomical alterations or disorders may lead to stenosis of the ostiomeatal complex, including ethmoid bulla enlargement, concha bullosa, deviated nasal septum, or turbinate hypertrophy.27,28 Timmenga et al29 studied sinus pathology development after sinus grafting procedures and concluded that postoperative complications, such as chronic sinusitis, often occurred in patients with a predisposition for these conditions. The ventilation of the maxillary sinus is guaranteed by the meatal ostium, which must be surgically expanded in case of obstruction to allow sufficient mucus clearance. Hypertrophy of the sinus membrane and/or reduced patency of the maxillary ostium are two clinical conditions that are strongly associated with postoperative complications such as ostium obstruction and secondary sinusitis. Carmeli et al23 evaluated CT scans to establish the relationship between mucosal shape and thickness and the risk of sinus obstruction. They found that this risk increased by approximately 55% if an irregular or circumferential membrane with a thickness greater than 5 mm was present, by approximately 82% if an irregular membrane of 10 mm was present, and by approximately 100% with a circumferential membrane 10 mm thick. Other authors demonstrated that many complications occurred in patients with a history of sinus clearance dysfunctions as a result of sinus membrane hyperplasia. In the presence of these anatomical alterations, it is recommended that any ENT contraindications to sinus elevation be corrected to reduce the risk of postoperative complications.30
The FESS phase did not include the removal of the entire sinus mucosa but only widening of the ostium. This is probably the cause for the recurrent membrane thickening observed in some patients after 1 year. In the authors’ opinion, it is important to obtain sufficient sinus ventilation during the first phases of bone graft healing (60 to 80 days) to avoid infection. A possible recurrence of mucosal thickening after 1 year does not compromise the final result. Careful preoperative ENT evaluation of patients requiring maxillary sinus elevation by nasal endoscopy and radiologic exams is essential. CT scan investigations should show the sinus ostium, not only the residual bone ridge, to allow full evaluation of the preoperative patency of the ostiomeatal complex. Symptoms such as facial pain, facial swelling, nasal obstruction, and nasal drainage are common in patients affected by chronic rhinosinusitis, but many cases may be asymptomatic. Patients affected by preoperative rhinosinusal diseases or membrane hypertrophy who require a sinus elevation typically must undergo a two-step surgical procedure. In fact, they require endoscopic treatment to treat their ENT condition before the sinus can be elevated. Usually, this treatment is represented by two different surgical procedures: an FESS approach and, after 4 to 6 months of healing, sinus elevation. Endoscopic surgical treatment aims to obtain homeostasis of the nose and sinus to restore the physiologic drainage and ventilation of the maxillary sinus, in accordance with the literature.25 The FESS can be performed simultaneous with sinus elevation to avoid an additional surgery in patients with sinusitis. This leads to a substantial reduction of surgical time and patient suffering.26 The FESS provides sufficient sinus ventilation during the first phase of sinus bone graft healing, preventing any infection, and any subsequent relapse of mucosal thickening does not prevent integration of the graft. A surgical technique that employs two separate phases (FESS, followed by sinus elevation after some months of healing) has not been shown to provide better results than the single-step technique. Postoperative complications such as graft infections are usually caused by insufficient sinus ventilation; thus, FESS aims to obtain proper sinus ventilation. FESS is done for two reasons: to enlarge the ostium (to encourage greater sinus ventilation) and to reduce the volume of hyperplastic mucosa. In the technique presented, maxillary sinus endoscopy was performed a few minutes before sinus elevation. General anesthesia was used to reduce the suffering of the patient generated by the long surgical intervention. General anesthesia and FESS could be avoided if the patient who needs sinus grafting shows only moderate sinus The International Journal of Oral & Maxillofacial Implants 637
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Falco et al
mucosa hypertrophy (thickness < 5 mm) and an open ostiomeatal complex. The presence of severe anatomical alterations or disorders that could be the cause of ostium stenosis is always an indication for sinus augmentation procedures associated with FESS.
CONCLUSIONS The proposed combined surgical protocol has proven to be a predictable approach for patients with sinus disease related to a lack of ventilation who require sinus elevation prior to the insertion of dental implants in the posterior maxilla. Maxillary sinus augmentation associated with functional endoscopic sinus surgery allows for recovery from rhinosinusal diseases and makes possible sinus grafting in a single surgical step, with the advantage of lower morbidity for the patient.
ACKNOWLEDGMENTS The authors declare that they have received no grants or financial support for the present study.
REFERENCES 1. Smiler DG, Johnson PW, Lozada JL, et al. Sinus lift grafts and endosseous implants: Treatment of the atrophic posterior maxilla. Dent Clin North Am 1992;36:151–186. 2. Chanavas M. Maxillary sinus: Anatomy, physiology, surgery, and bone grafting related to implantology—Eleven years of surgical experience (1979-1990). J Oral Implantol 1990;16:2–12. 3. Adell R, Lekholm U, Grondahl K, Brånemark PI, Lindstrom J, Jacobsson M. Reconstruction of severely resorbed edentulous maxillae using fixtures in immediate autogenous bone grafts. Int J Oral Maxillofac Implants 1990;3:233–246. 4. De Leonardis D, Pecora GE. Augmentation of the maxillary sinus with calcium sulfate: One-year clinical report from a prospective longitudinal study. Int J Oral Maxillofac Implants 1999;14:869–878. 5. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surgery 1980;38:613–616. 6. Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol 2003;8:328–343. 7. Del Fabbro M, Testori T, Francetti L, Weinstein R. Systematic review of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 2004;24:565–577. 8. Del Fabbro M, Rosano G, Taschieri S. Implant survival rates after maxillary sinus augmentation. Eur J Oral Sci 2008;116:497–506. 9. Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 2008;35(suppl 8):216–240. 10. Rickert D, Slater JJ, Meijer HJ, Vissink A, Raghoebar GM. Maxillary sinus lift with solely autogenous bone compared to a combination of autogenous bone and growth factors or (solely) bone substitutes. A systematic review. Int J Oral Maxillofac Surg 2012;41:160–167.
11. Crespi R, Vinci R, Capparè P, Gherlone E, Romanos GE. Calvarial versus iliac crest for autologous bone graft material for a sinus lift procedure: A histomorphometric study. Int J Oral Maxillofac Implants 2007;22:527–532. 12. Scarano A, Degidi M, Iezzi G, et al. Maxillary sinus augmentation with different biomaterials: A comparative histologic and histomorphometric study in man. Implant Dent 2006;15:197–207. 13. Won YH, Kim SG, Oh JS, Lim SC. Clinical evaluation of demineralized bone allograft for sinus lifts in humans: A clinical and histologic study. Implant Dent 2011;20:460–464. 14. Steigmann M, Garg AK. A comparative study of bilateral sinus lifts performed with platelet-rich plasma alone versus alloplastic graft material reconstituted with blood. Implant Dent 2005;14:261–266. 15. Small SA, Zinner ID, Panno FV, Shapiro HJ, Stein JI. Augmenting the maxillary sinus for implants: Report of 27 patients. Int J Oral Maxillofac Implants 1993;8:523–528. 16. Lambert F, Léonard A, Drion P, Sourice S, Layrolle P, Rompen E. Influence of space-filling materials in subantral bone augmentation: Blood clot vs. autogenous bone chips vs. bovine hydroxyapatite. Clin Oral Implants Res 2011;22:538–545. 17. Barone A, Crespi R, Aldini NN, Fini M, Giardino R, Covani U. Maxillary sinus augmentation: Histologic and histomorphometric analysis. Int J Oral Maxillofac Implants 2005;20:519–525. 18. Brook I. Sinusitis. Periodontol 2000 2009;49:126–139. 19. Alho OP. Nasal airflow, mucociliary clearance, and sinus functioning during viral colds: Effects of allergic rhinitis and susceptibility to recurrent sinusitis. Am J Rhinol 2004;18:349–355. 20. Timmenga NM, Raghoebar GM, Liem RS, van Weissenbruch R, Manson WL, Vissink A. Effects of maxillary sinus floor elevation surgery on maxillary sinus physiology. Eur J Oral Sci 2003;111:189–197. 21. Hunter WL IV, Bradrick JP, Houser SM, Patel JB, Sawady J. Maxillary sinusitis resulting from ostium plugging by dislodged bone graft: Case report. J Oral Maxillofac Surg 2009;67:1495–1498. 22. Alkan A, Celebi N, Baş B. Acute maxillary sinusitis associated with internal sinus lifting: Report of a case. Eur J Dent 2008;2:69–72. 23. Carmeli G, Artzi Z, Kozlovsky A, Segev Y, Landsberg R. Antral computerized tomography pre-operative evaluation: Relationship between mucosal thickening and maxillary sinus function. Clin Oral Implants Res 2011;22:78–82. 24. Pignataro L, Mantovani M, Torretta S, Felisati G, Sambataro G. ENT assessment in the integrated management of candidate for (maxillary) sinus lift. Acta Otorhinolaryngol Ital 2008;28:110–119. 25. Felisati G, Borloni R, Chiapasco M, Lozza P, Casentini P, Pipolo C. Maxillary sinus elevation in conjunction with transnasal endoscopic treatment of rhino-sinusal pathoses: Preliminary results on 10 consecutively treated patients. Acta Otorhinolaryngol Ital 2010 Dec;30(6):289–293. 26. Chiapasco M, Felisati G, Zaniboni M, Pipolo C, Borloni R, Lozza P. The treatment of sinusitis following maxillary sinus grafting with the association of functional endoscopic sinus surgery (FESS) and an intra-oral approach. Clin Oral Implants Res 2013;24:623–629. 27. Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impact on implant survival. J Periodontol 2004;75:511–516. 28. Testori T, Drago L, Wallace SS, et al. Prevention and treatment of postoperative infections after sinus elevation surgery: Clinical consensus and recommendations. Int J Dent 2012;2012:365809. Epub 2012 Aug 9. 29. Timmenga NM, Raghoebar GM, Boering G, van Weissenbruch R. Maxillary sinus function after sinus lifts for the insertion of dental implants. J Oral Maxillofac Surg 1997;55:936–939. 30. Torretta S, Mantovani M, Testori T, Cappadona M, Pignataro L. Importance of ENT assessment in stratifying candidates for sinus floor elevation: A prospective clinical study. Clin Oral Implants Res 2013 Aug;24(suppl A100):57–62. Epub 2011 Nov 22.
638 Volume 30, Number 3, 2015 © 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
T
he maxillary alveolar process undergoes irreversible bone resorption after tooth loss, which leads to both horizontal and vertical bone atrophy. The increased pneumatization of the maxillary sinus and atrophy of the alveolar bone consequent to this hard tissue resorption significantly reduce the amount of bone available for dental implant placement.1,2 Different surgical techniques have been developed to this effect to allow
1Private
Practice, Pescara, Italy. Physician, ENT and Maxillofacial Surgery Department, Lanciano Hospital, Chieti, Italy. 3Head, ENT and Maxillofacial Surgery Department, Lanciano Hospital, Chieti, Italy. 2 Attending
Correspondence to: Dr Marco Berardini, Via Galilei 8, 65122 Pescara (Italy). Fax: +390-85-7933050. Email: [email protected] ©2015 by Quintessence Publishing Co Inc.
implant-supported rehabilitation of the atrophied maxilla, including ridge augmentation through inlay bone grafts, Le Fort I osteotomy with bone graft interposition, maxillary sinus elevation, and onlay bone graft.3,4 Maxillary sinus grafting through elevation of the sinus membrane was first described by Tatum in 1977 and published by Boyne and James in 1980.5 This surgical technique allows vertical bone augmentation in the posterior maxilla via the formation of new bone between the sinus membrane and the maxillary sinus floor. Titanium dental implants could be inserted during the same surgical step or after a healing period of 6 to 9 months. The procedure is predictable, and published implant success and survival rates are higher than 90%.6–9 Different graft materials have been used to support bone regeneration beneath the maxillary sinus membrane: autogenous bone,10,11 demineralized allograft,12,13 freeze-fried bone allograft, alloplast,14,15 resorbable and nonresorbable hydroxyapatite,16 and xenografts.17 The International Journal of Oral & Maxillofacial Implants 633
© 2015 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Falco et al
Although high success rates have been reported for this surgical technique, intraoperative or postoperative complications to sinus elevation surgery could have several negative effects on sinus homeostasis. Obstruction of the ostium of the sinus and secondary rhinosinusitis, periosteal inflammation, inhibition of ciliary mucosa,18–20 graft bacterial infection, membrane perforations, and penetration of graft material into the maxillary sinus21,22 are among the complications that may lead to graft and implant failure. Bacterial infection of a graft could spread to the orbit and endanger the patient’s life. It has been reported that patients with sinus membranes with circumferential thickness > 5 mm who are subjected to sinus elevation have a substantial risk of obstruction of the ostiomeatal unit and subsequent sinusitis.23 Reversible ear-nose-throat (ENT) contraindications to sinus elevation are represented by anatomical alterations of the region (ostium obstruction, sinus membrane hypertrophy), infectious-inflammatory processes (acute or chronic), sinus mucocele, and benign neoplasms of the rhinosinus area. Preoperative evaluation of the patient by an ENT specialist is thus necessary to identify these nasosinusal diseases. Accurate identification of those reversible contraindications to the sinus elevation procedure through evaluations (including nasal endoscopy) by an otorhinolaryngologist is essential.24 The patient, in case of ENT diseases, should be first treated by an ENT specialist and, in a subsequent surgical session, by the oral surgeon for maxillary sinus elevation. This will result in two surgical steps, with considerable discomfort for the patient. A one-step surgical procedure that includes maxillary sinus floor elevation in association with functional endoscopic sinus surgery (FESS) has been presented.25,26 This surgical treatment demonstrated good results in some patients with reversible contraindications to sinus elevation. It seemed appropriate to perform a clinical investigation of 69 treated maxillary sinuses to determine whether this surgical approach can be proposed as a predictable option to treat minor reversible contraindications to maxillary sinus floor elevation and perform bone augmentation at the same time. The aim of the present study was to evaluate the clinical and radiologic results of sinus elevation done through the lateral approach simultaneous with FESS in patients with reversible ENT contraindications.
MATERIALS AND METHODS Thirty-eight patients (total of 69 sinuses) with ages ranging from 36 to 59 years (mean age, 48 years) were recruited between January 2010 and January 2012 at Lanciano Hospital ENT and Maxillofacial Surgery
Department (Chieti, Italy). All patients were investigated with nasal endoscopy associated with panoramic radiographs and with maxillofacial computed tomography (CT) scans. The inclusion criteria were insufficient bone height (< 5 mm) in the posterior maxilla to receive dental implants associated with inflammatory diseases and anatomical alterations in the rhinosinusal region (eg, chronic hyperplastic sinusitis, mucocele, ostium obstruction, anatomical alterations of the nasal septum). The majority of cases involved asymptomatic hyperplastic chronic inflammatory disease of the maxillary sinuses. In some patients, this condition was bilateral. In 4 cases, a unilateral maxillary mucocele was found and removed. Sinusitis was treated with a functional correction of the nasal septum and radiodecongestion of the inferior turbinates in 5 patients, whereas in the other 33 cases, surgery on the ostiomeatal complex was sufficient to widen the ostium to support sinus ventilation. The patients were treated under general anesthesia in a single surgical session involving an ENT surgeon (who performed the FESS) and an oral surgeon who performed the sinus elevation via the lateral approach. The standard protocol involved intravenous anesthesia (remifentanil infusion) with orotracheal intubation. The patient was positioned at 30 to 40 degrees with the head up to facilitate venous return from the head and neck. The aim of FESS is to restore proper ventilation to the sinuses by widening the meatal ostium and removing any obstruction to sinus drainage. It is performed with different endoscopes assisted by video (for the maxillary sinus, these are angled by 30 to 45 degrees) and sharp, angled surgical tools. The endoscopic approach included, depending on the clinical circumstances, inferior uncinectomy, mucocele removal, septoplasty, or partial middle turbinectomy. Sinus elevation was performed by creating a lateral trapezoidal flap with a horizontal incision on the edentulous ridge and vertical incisions at least 1 cm from the edge of the mesial and distal antrostomy. The bony window was created with a 3-mm diamond bur at high speed under abundant irrigation with cold sterile saline solution. The window shape was ellipsoidal, with the horizontal longest margin parallel to the crestal margin. It was removed or eroded and the sinus membrane was elevated using periosteal instruments with rounded edges and different lengths, sizes, and angles. Bio-Oss xenograft (Geistlich) was inserted after membrane elevation. The biomaterial particles were 1 to 2 mm in size. The graft material was compacted to stabilize it between the bone walls and the sinus membrane. Hermetic and passive sutures were applied. Postoperative medical treatment included nasal emollient oil in the nasal cavity and oral chlorhexidine
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Fig 1a Meatus middle opening. Pus is present. Fig 1b Internal view of the maxillary sinus through the middle meatus. Fig 1c Suction of the suppuration using an endoscopic aspirator from the right sinus. Fig 1d Middle right antrotomy. Fig 1e Sinus elevation by the lateral approach. The bone window was created with a 3-mm diamond bur, and the membrane was elevated by periosteal instruments.
a
b
c
d
Fig 1f Preoperative CT scan showing pro- Fig 1g Control CT scan after 6 nounced hyperplasia of the sinus membrane. months showing graft healing and resolution of sinus membrane hyperplasia.
e
Fig 1h Control CT scan after 1 year of implant load. The ostiomeatal complex is open, and the graft shows good integration.
Fig 2a Patient no. 4, preoperative CT scan. The patient showed unilateral chronic sinusitis caused by blocked ventilation of the sinus. Fig 2b Patient no. 4, 6 months postoperative. The patient shows resolution of the chronic sinusitis. No complications occurred during the graft integration period. a
spray on the wound, broad-spectrum antibiotics (amoxicillin 1 g 1 pill twice daily by mouth for 7 days), and corticosteroids (Deflazacort 30 mg 1 pill twice daily for 5 days). Nasal packing with Merocel (Medtronic) was performed after the surgery in three patients and was removed on the second day. The patients were instructed to use saline solution for nasal rinse (twice daily for the following 10 days) and nasal drops of Nafazolina nitrate (7.5 mg) and Tirotricina (3 mg twice daily for 10 days). In all cases, a mask-type refrigerant (Hilotherm) was placed. Medical examinations and nasal endoscopies were performed at 7 days, 14 days, 30 days, and 3 months after sinus surgery. Dental implants (Biomet 3i, n = 137) were inserted according to the prosthetic plan after 6 months of healing. The implant sites were prepared using traditional burs without the use of osteotomes
b
because of the high density of the regenerated tissue. Insertion torque was above 45 Ncm for all implants placed. At 6 months and 1 year after sinus surgery, all patients were investigated with panoramic radiographs and CT scans. All patients were followed for at least 1 year. The parameters evaluated were intraoperative complications, postoperative complications, clinical and radiologic resolution of ENT disease, radiologic graft integration, and implant survival rate.
RESULTS Images from two treated patients are shown in Figs 1 and 2. In one case the sinus membrane was perforated intraoperatively; it was treated by application of a resorbable membrane (Bio-Gide, Geistlich). The International Journal of Oral & Maxillofacial Implants 635
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Falco et al
Table 1 Patient Data Patient Unilateral or no. bilateral surgery Age (y)
ENT disease
FESS surgical treatment
Complications
1
Unilateral
40
Chronic hyperplastic sinusitis
OMC surgery
None
2
Bilateral
58
Chronic hyperplastic sinusitis
OMC surgery
Graft site swelling
3
Unilateral
34
Sinusitis and nasal septum alteration
Nasal septum functional correction
None
4
Bilateral
56
Chronic hyperplastic sinusitis
OMC surgery
None
5
Bilateral
45
Chronic hyperplastic sinusitis
OMC surgery
None
6
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
7
Bilateral
36
Chronic hyperplastic sinusitis
OMC surgery
None
8
Bilateral
49
Sinusitis and chronic hyperplastic sinusitis
OMC surgery
Membrane perforation, graft site swelling
9
Bilateral
47
Chronic hyperplastic sinusitis
OMC surgery
None
10
Unilateral
48
Sinus mucocele
Mucocele removal/OMC surgery
None
11
Unilateral
40
Sinus mucocele
Mucocele removal/OMC surgery
None
12
Bilateral
51
Chronic hyperplastic sinusitis
OMC surgery
None
13
Bilateral
53
Chronic hyperplastic sinusitis
14
Bilateral
47
Sinusitis and nasal septum alteration
OMC surgery
None
Nasal septum functional correction
None
15
Bilateral
46
Chronic hyperplastic sinusitis
OMC surgery
None
16
Unilateral
43
Sinus mucocele
Mucocele removal/OMC surgery
None
17
Unilateral
55
Sinus mucocele
Mucocele removal/OMC surgery
None
18
Bilateral
50
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
19
Bilateral
52
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
20
Unilateral
54
Chronic hyperplastic sinusitis
OMC surgery
None
21
Bilateral
49
Chronic hyperplastic sinusitis
OMC surgery
None
22
Unilateral
43
Sinusitis and nasal septum alteration
Nasal septum functional correction
Graft site swelling
23
Bilateral
44
Chronic hyperplastic sinusitis
OMC surgery
None
24
Bilateral
38
Chronic hyperplastic sinusitis
OMC surgery
None
25
Bilateral
42
Chronic hyperplastic sinusitis
OMC surgery
None
26
Bilateral
49
Chronic hyperplastic sinusitis
OMC surgery
None
27
Bilateral
59
Chronic hyperplastic sinusitis
OMC surgery
None
28
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
29
Bilateral
41
Chronic hyperplastic sinusitis
OMC surgery
None
30
Unilateral
48
Chronic hyperplastic sinusitis
OMC surgery
None
31
Bilateral
55
Chronic hyperplastic sinusitis
OMC surgery
None
32
Bilateral
51
Chronic hyperplastic sinusitis
OMC surgery
None
33
Bilateral
53
Chronic hyperplastic sinusitis
OMC surgery
None
34
Bilateral
50
Chronic hyperplastic sinusitis
OMC surgery
None
35
Bilateral
45
Chronic hyperplastic sinusitis
OMC surgery
None
36
Bilateral
47
Chronic hyperplastic sinusitis
OMC surgery
Graft site swelling
37
Bilateral
58
Chronic hyperplastic sinusitis
OMC surgery
None
38
Bilateral
48
Chronic hyperplastic sinusitis
OMC surgery
None
Swelling of the graft site during the immediate postoperative period was reported by six patients (8.7%) and was resolved by an extension of medical intravenous therapy for 2 days. The sinus disease related to
impaired ventilation was resolved in all treated cases, as confirmed by clinical and radiologic examinations. Preoperative and postoperative patient data are summarized in Table 1.
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In all 69 sites, the radiographs (panoramic and CT scans) highlighted areas of regenerated hard tissue with homogenous radiopacity after 1 year. No areas of radiolucency in the graft, which might indicate inflammation or poor integration of the biomaterial, were detected in the radiographs. No implant failures were observed during the follow-up period. Periodic nasal endoscopy investigations (7, 14, and 30 days; 3 months; and 1 year) showed an open ostiomeatal complex, and no biomaterial particles were found within the maxillary sinuses. At 1 year, CT scans showed, in many cases, sinus membrane thickening with important reduction of ostium patency.
DISCUSSION It has been reported that maxillary sinus elevation may result in some intraoperative or postoperative complications, such as ostium obstruction and resulting sinusitis, graft infections, perforations of the sinus membrane with dislocation of biomaterial in the maxillary sinus, and acute purulent sinusitis. Certain anatomical alterations or disorders may lead to stenosis of the ostiomeatal complex, including ethmoid bulla enlargement, concha bullosa, deviated nasal septum, or turbinate hypertrophy.27,28 Timmenga et al29 studied sinus pathology development after sinus grafting procedures and concluded that postoperative complications, such as chronic sinusitis, often occurred in patients with a predisposition for these conditions. The ventilation of the maxillary sinus is guaranteed by the meatal ostium, which must be surgically expanded in case of obstruction to allow sufficient mucus clearance. Hypertrophy of the sinus membrane and/or reduced patency of the maxillary ostium are two clinical conditions that are strongly associated with postoperative complications such as ostium obstruction and secondary sinusitis. Carmeli et al23 evaluated CT scans to establish the relationship between mucosal shape and thickness and the risk of sinus obstruction. They found that this risk increased by approximately 55% if an irregular or circumferential membrane with a thickness greater than 5 mm was present, by approximately 82% if an irregular membrane of 10 mm was present, and by approximately 100% with a circumferential membrane 10 mm thick. Other authors demonstrated that many complications occurred in patients with a history of sinus clearance dysfunctions as a result of sinus membrane hyperplasia. In the presence of these anatomical alterations, it is recommended that any ENT contraindications to sinus elevation be corrected to reduce the risk of postoperative complications.30
The FESS phase did not include the removal of the entire sinus mucosa but only widening of the ostium. This is probably the cause for the recurrent membrane thickening observed in some patients after 1 year. In the authors’ opinion, it is important to obtain sufficient sinus ventilation during the first phases of bone graft healing (60 to 80 days) to avoid infection. A possible recurrence of mucosal thickening after 1 year does not compromise the final result. Careful preoperative ENT evaluation of patients requiring maxillary sinus elevation by nasal endoscopy and radiologic exams is essential. CT scan investigations should show the sinus ostium, not only the residual bone ridge, to allow full evaluation of the preoperative patency of the ostiomeatal complex. Symptoms such as facial pain, facial swelling, nasal obstruction, and nasal drainage are common in patients affected by chronic rhinosinusitis, but many cases may be asymptomatic. Patients affected by preoperative rhinosinusal diseases or membrane hypertrophy who require a sinus elevation typically must undergo a two-step surgical procedure. In fact, they require endoscopic treatment to treat their ENT condition before the sinus can be elevated. Usually, this treatment is represented by two different surgical procedures: an FESS approach and, after 4 to 6 months of healing, sinus elevation. Endoscopic surgical treatment aims to obtain homeostasis of the nose and sinus to restore the physiologic drainage and ventilation of the maxillary sinus, in accordance with the literature.25 The FESS can be performed simultaneous with sinus elevation to avoid an additional surgery in patients with sinusitis. This leads to a substantial reduction of surgical time and patient suffering.26 The FESS provides sufficient sinus ventilation during the first phase of sinus bone graft healing, preventing any infection, and any subsequent relapse of mucosal thickening does not prevent integration of the graft. A surgical technique that employs two separate phases (FESS, followed by sinus elevation after some months of healing) has not been shown to provide better results than the single-step technique. Postoperative complications such as graft infections are usually caused by insufficient sinus ventilation; thus, FESS aims to obtain proper sinus ventilation. FESS is done for two reasons: to enlarge the ostium (to encourage greater sinus ventilation) and to reduce the volume of hyperplastic mucosa. In the technique presented, maxillary sinus endoscopy was performed a few minutes before sinus elevation. General anesthesia was used to reduce the suffering of the patient generated by the long surgical intervention. General anesthesia and FESS could be avoided if the patient who needs sinus grafting shows only moderate sinus The International Journal of Oral & Maxillofacial Implants 637
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Falco et al
mucosa hypertrophy (thickness < 5 mm) and an open ostiomeatal complex. The presence of severe anatomical alterations or disorders that could be the cause of ostium stenosis is always an indication for sinus augmentation procedures associated with FESS.
CONCLUSIONS The proposed combined surgical protocol has proven to be a predictable approach for patients with sinus disease related to a lack of ventilation who require sinus elevation prior to the insertion of dental implants in the posterior maxilla. Maxillary sinus augmentation associated with functional endoscopic sinus surgery allows for recovery from rhinosinusal diseases and makes possible sinus grafting in a single surgical step, with the advantage of lower morbidity for the patient.
ACKNOWLEDGMENTS The authors declare that they have received no grants or financial support for the present study.
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