Introduction
Despite advances in pharmacology and physiology, chronic frontal rhinosinusitis, which is associated with significant morbidity, remains highly prevalent.Reference Scott, Wormald, Close, Gallagher, Anthony and Maddern 1
For complicated frontal sinus disease, osteoplastic frontal sinus obliteration with abdominal fat has been used as a first-line therapy.Reference Goodale and Montgomery 2 , Reference Hardy and Montgomery 3 Unfortunately, there are a high number of associated complications, such as post-operative abdominal wound infection, unaesthetic cosmetic changes of the frontal bone, supraorbital neuralgia and frontal bossing.Reference Weber, Draf, Keerl, Kahle, Schinzel and Thomann 4 , Reference Silverman, Gray and Busaba 5
Advances in endoscopic techniques have made it possible to simulate external techniques like the Lothrop procedure. Draf developed the Draf type III frontal sinus drainage procedure, which is also known as the frontal sinus drill-out or endoscopic modified Lothrop procedure.Reference Gross, Gross, Becker, Moore and Phillips 6 Furthermore, Weber et al. developed endoscopic techniques for widening the frontal sinus ostium.Reference Weber, Draf, Kratzsch, Hosemann and Schaefer 7
Currently, frontal sinus surgery involves a combination of minimally invasive endoscopic surgery and traditional open frontal sinus obliteration.Reference Chiu 8
The open approach is a reasonable option given its proven success.Reference Silverman, Gray and Busaba 5 Indications for open frontal sinus obliteration as a primary treatment are: the presence of intrafrontal cells; the presence of frontal disease in far lateral locations and a narrow frontal recess; frontal recess neo-osteogenesis; large osteomas; malignant tumours; osteomyelitis; complex frontal bone fractures; fractures of the posterior sinus wall with cerebrospinal fluid leakage; and failed endoscopic surgery due to chronic frontal sinusitis.Reference Weber, Draf, Keerl, Kahle, Schinzel and Thomann 4 , Reference Silverman, Gray and Busaba 5 , Reference Soyka, Annen and Holzmann 9 , Reference Rivera, Rodriguez, Pulido, Garcia-Alcantara and Sanz 10
For successful obliteration of the frontal sinus, the frontal sinus mucosa and the inner bony cortex of the sinus wall must be completely removed, and the nasofrontal duct must be occluded permanently.Reference Rohrich and Mickel 11 , Reference Murphy and Jones 12 The choice of material is also important for successful obliteration.Reference Murphy and Jones 12 Techniques currently used include the implantation of autologous fat, bone and muscle, in combination with spontaneous osteogenesis.Reference Rohrich and Mickel 11 While there are various alloplastic materials used in frontal sinus obliteration, autogenous fat remains the most popular.Reference D'Addario, Haug and Talwar 13
This paper aimed to demonstrate that frontal sinus obliteration with a synthetic, resorbable and osteoconductive bone graft of ß-tricalcium phosphate is a good alternative to the use of autologous fat, bone or muscle and to allogenic spongiosa. It is already used in trauma, orthopaedic and spinal surgical procedures, and in cranio-maxillofacial surgery.Reference Wheeler, Cross, Eschbach, Rose, Gallogly and Lewis 14
Materials and methods
Patients
We report on four patients who underwent osteoplastic frontal sinus obliteration. All were diagnosed with frontal mucocele. The patients’ clinical charts were retrospectively reviewed, including demographics, diagnosis, imaging, prior sinus surgery history and post-operative complications. Information on persisting symptoms and patient outcomes was collected using a telephone questionnaire in February 2016.
Obliteration material
For the obliteration of the frontal sinus after resection of the mucocele, we used a fully synthetic and resorbable bone graft substitute consisting of pure ß-tricalcium phosphate, with a compressive strength similar to that of cancellous bone (chronOS bone graft substitute; Synthes, West Chester, Pennsylvania, USA). This implant material is usually fully resorbed, and is completely remodelled into the host bone within 6–18 months.
We used granules of different sizes, which could be easily formed to completely obliterate the frontal sinus. In line with the principles of frontal sinus obliteration,Reference Weber, Draf, Kahle and Kind 15 the sinus mucosa was first totally removed and the inner cortex of the sinus wall was drilled out. Subsequently, the granules of ß-tricalcium phosphate were filled into the sinus for obliteration. In two patients, we used freeze-dried human cancellous bone (DIZG, Berlin, Germany) for comparison.
A Medline search was then performed to compare our results with data reported in the literature.
Results
Our study included four patients: three males and one female (Table I).
Table I Patients’ characteristics
Pt no. = patient number; M = male; F = female
Patient one, a 71-year-old male, was first diagnosed with a frontal sinus mucocele in 2008 (Figure 1). He had previously undergone external sinus surgery, in 1988, because of an anterior skull base fracture. Subsequently, osteoplastic frontal sinus surgery was performed as a first-line treatment because of ossified ethmoidal and frontal recesses. The complaints were: frontal stabbing pain, upper eyelid swelling, and eye bulb dislocation without double vision. The frontal sinus was obliterated with ß-tricalcium phosphate in 2008 (Figure 2).
Fig. 1 (a) Coronal and (b) axial pre-operative computed tomography scans of a frontal mucocele in patient one.
Fig. 2 (a) Coronal and (b) axial computed tomography scans of patient one at two months after frontal sinus obliteration with β-tricalcium phosphate.
Patient two, a 54-year-old male, was first diagnosed with a frontal sinus mucocele in 2011, a result of prior endoscopic sinus surgery for chronic sinusitis (Figure 3). Osteoplastic frontal sinus obliteration was performed in November 2011 as salvage surgery after previous endoscopic surgery (Figure 4). Pre-operatively, the patient complained of frontal stabbing pain and upper eyelid swelling. Subsequently, in addition to frontal sinus obliteration with ß-tricalcium phosphate, the frontal sinus roof was reconstructed with an absorbable polydioxanone (PDS™) plate (Johnson and Johnson Medical GmbH, Ethicon Germany, Norderstedt, Germany).
Fig. 3 (a) Coronal and (b) axial pre-operative computed tomography scans of a right frontal sinus mucocele in patient two.
Fig. 4 (a) Coronal and (b) axial computed tomography scans of patient two at 27 months after frontal sinus obliteration with β-tricalcium phosphate.
Patient three, a 79-year-old female, was first diagnosed with a frontal sinus mucocele in 2013, a result of prior endoscopic sinus surgery for a pyocele of the left frontal sinus. She had already undergone combined endonasal and extranasal sinus surgery four times, twice in 2007, and again in 2012 and 2013; these procedures were performed in other departments. She complained about an upper eyelid swelling and a stabbing pain in this area. She underwent frontal sinus obliteration as salvage surgery in March 2013, following multiple previous combined endonasal and extranasal sinus surgical procedures. The ethmoidal and frontal recesses were ossified as a result of the former surgical procedures. Pre-operatively, there was already a sinocutaneous fistula draining to the medial eyelid. The fistula was excised and the sinus was obliterated with freeze-dried human cancellous bone.
Patient four, an 83-year-old male, was first diagnosed with a frontal sinus mucocele on both sides in 2013. He had suffered a craniocerebral injury with an anterior skull base fracture in 1971. He complained about a stabbing pain in the frontal area and a proptosis on the left side. He underwent frontal sinus obliteration on both sides, with freeze-dried human cancellous bone, as a first-line treatment in April 2013. A posterior wall defect of the left frontal sinus was covered with TachoSil® (sealant matrix of human fibrinogen and human thrombin; Takeda, Konstanz, Germany) and the anterior wall defect was reconstructed with an absorbable polydioxanone (PDS) plate (Johnson and Johnson Medical GmbH, Ethicon Germany, Norderstedt).
All patients underwent computed tomography (CT) scanning prior to surgery and eyebrow incision.
There were no peri-operative complications. Only patient two had post-operative complications, which included a cutaneous fistula in the area of the incision two weeks after surgery. This fistula was excised six weeks post-operatively under local anaesthesia. None of the patients had any further symptoms after external frontal sinus obliteration and there were no aesthetic restrictions. None of the patients underwent any further sinus surgery following the frontal sinus obliteration. Both materials used (ß-tricalcium phosphate and freeze-dried human cancellous bone) were well tolerated.
The post-operative CT scans demonstrated that the frontal sinus was completely obliterated and that the ß-tricalcium phosphate, as expected, had almost completely remodelled into the host bone.
Discussion
There has been much discussion as to whether an endoscopic or an open approach is indicated for frontal sinus disease.
There are a number of radical procedures that use an external approach to treat frontal sinus mucoceles. Unfortunately, these surgical techniques are accompanied by high surgical morbidity, post-operative unaesthetic scar formation, and difficulty in radiological diagnosis of recurrence after obliteration.Reference Aydin and Demir 16 Improvements in the endoscopic technique and the possibility of image-guided navigation have made it possible to use endoscopic procedures to treat these complicated cases.Reference Chandra, Kennedy and Palmer 17 , Reference Dhepnorrarat, Subramaniam and Sethi 18
Open frontal sinus obliteration was once regarded as the ‘gold standard’ for frontal sinus disease treatment.Reference Chiu 8 , Reference Chandra, Kennedy and Palmer 17 Techniques such as the Lynch procedure or the endonasal Lothrop procedureReference Close 19 showed high failure rates.Reference Chiu 8 The modified subtotal Lothrop procedure was developed as an alternative.Reference Eloy, Mady, Kanumuri, Svider and Liu 20 , Reference Anderson and Sindawi 21
A review of the literature showed that the modified Lothrop procedure now functions as a rescue technique for a failed osteoplastic flap for frontal sinus obliteration. It also demonstrated that the endoscopic rescue procedure is technically challenging, requiring an experienced surgeon.Reference Langton-Hewer and Wormald 22 In a prospective study comprising 83 patients, Wormald showed that the endoscopic modified Lothrop procedure is a successful short-term option for different frontal diseases.Reference Wormald 23
A retrospective study of the endoscopic management of frontal sinus mucoceles with anterior table erosion, by Woodworth et al., showed that the endoscopic marsupialisation of frontal sinus mucoceles has a high success rate with a good cosmetic outcome, and often avoids routine reconstruction.Reference Woodworth, Harvey, Neal, Palmer and Schlosser 24 Marsupialisation using endoscopic sinus surgery is regarded as the treatment of choice for mucoceles, given the low recurrence rates and low morbidity.Reference Lund 25 , Reference Kennedy, Josephson, Zinreich, Mattox and Goldsmith 26 Nomura et al. treated frontal mucoceles with conventional endoscopic sinus surgery, resulting in good outcomes.Reference Nomura, Hidaka, Arakawa, Sugawara, Ozawa and Okumura 27 Only one frontal sinus closed during follow up.
The success of endoscopic procedures for the treatment of frontal sinus mucoceles with lateral extension is undoubtedly linked to the localisation of the mucocele medial wall. The determination of mucocele extension beyond a virtual sagittal plane tangential to the medial side of the ocular globe is essential before deciding whether to use an external or an endonasal approach for lateral extended mucoceles.Reference Trimarchi, Bertazzoni and Bussi 28 Sama et al. proposed a new algorithm for the surgical treatment of frontal sinus mucoceles.Reference Sama, McClelland and Constable 29 These authors emphasised variables such as mucocele position, drainage dimensions, the existence of fronto-ethmoidal cells and the degree of neo-osteogenesis. Decisions regarding the use of an endoscopic or external approach based on this classification resulted in a revision rate of 19 per cent.
The results of endoscopic and open approaches are comparable.Reference Courson, Stankiewicz and Lal 30 The use of an endoscopic approach or an open frontal sinus obliteration technique should be decided based on the surgeon's experience, the frontal recess anatomy and the nature of the disease.Reference Silverman, Gray and Busaba 5
The long-term outcomes of the techniques are important. The failure rate of drill-outs performed as a result of mucoceles and tumours is significantly higher than that for other diagnoses. Most of the surgical failures occurred within 2 years, while late failures occurred after 12 years.Reference Ting, Wu and Metson 31
The length of time between mucocele origins and presentation varies. In a study by Scangas et al., patients were diagnosed with a mucocele on average 17.7 years after paranasal trauma, 5.3 years after endoscopic surgery and 18.1 years after open sinus surgery.Reference Scangas, Gudis and Kennedy 32 Patients in that study presented with a mucocele as a result of open sinus surgery and trauma 20 years and 42 years later, respectively. Hence, long-term follow up is necessary to determine surgical outcomes.
Silverman et al. demonstrated that open frontal sinus obliteration is still indicated in selected cases as a first-line therapy.Reference Silverman, Gray and Busaba 5 The presence of intrafrontal cells, far lateral frontal sinus disease and a narrow frontal recess are named. The success rate in their study was 91 per cent.
Soyka et al. performed frontal sinus obliteration as a first-line treatment in 36 patients and as a second-line treatment in 41 patients.Reference Soyka, Annen and Holzmann 9 They demonstrated good success, with 80 per cent of patients having no symptoms post-operatively. General complications were reported in 36.4 per cent of patients; of these, 90 per cent were only minor complications.
The material best suited for frontal sinus obliteration remains controversial. A number of various avascular materials have been used for frontal sinus obliteration, including fat, muscle, cancellous bone and hydroxyapatite. Biological properties such as fast revascularisation, no donor site morbidity and material availability are desired.
Kang et al. showed that the combined use of Tisseel® and autogenous calvarian bone for frontal sinus obliteration was suitable in their 17 patients.Reference Kang, Sng and Tay 33 This was associated both with a low complication rate and low donor site morbidity, and avoided the need for a separate donor surgical site. Vironneau et al. used an osteoplastic calvarian bone graft for frontal sinus obliteration in 11 patients.Reference Vironneau, Coste and Prulière-Escabasse 34 All of these patients had improved symptoms and eight of them had no residual complaints following the procedure. Monnazzi et al. reported on eight sinus fracture patients who underwent frontal sinus obliteration with iliac crest bone grafts.Reference Monnazzi, Gabrielli, Pereira-Filho, Hochuli-Vieira, de Oliveira and Gabrielli 35 The complication rate was high in that study.
Obliteration with autologous bone works well in small sinuses with fewer complications. Cases of large and extensively pneumatised frontal sinuses present with many complications, requiring further surgery.
Rodriguez et al. used a mixture of calvarian bone dust and demineralised bone matrix (DBX; Musculoskeletal Transplant Foundation, Edison, New York, USA), a commercially available product, for frontal sinus obliteration in post-traumatic cases.Reference Rodriguez, Uceda, Lobato and Aniceto 36 They demonstrated this technique to be safe and effective, with minimal morbidity, and with proven stability in the long term.
Moshaver et al. showed that an anteriorly based pericranial flap is a good option for frontal sinus obliteration.Reference Moshaver, Harris and Seikaly 37 None of their patients experienced recurrence.
Instead of bone or muscle, autologous fat is often used for frontal sinus obliteration. A retrospective study, by Kristin et al., of patients who received frontal sinus obliteration because of non-endoscopically accessible mucoceles, showed that obliteration with abdominal fat is a successful treatment option.Reference Kristin, Betz, Stelter, Berghaus and Leunig 38 Nine of 10 patients were generally satisfied with the obliteration. Significant symptom improvements, significant reductions in the need for disease-specific drugs and fewer days of missed work were demonstrated.
Mendonca-Caridad et al. investigated a novel approach to frontal sinus obliteration and cranial tissue regeneration.Reference Mendonca-Caridad, Lopez, Fayos and Miery 39 They used a totally autogenous material for frontal sinus obliteration. Platelet-rich and platelet-poor plasma was set to clot with cortical shavings from the skull face. This bioactive scaffold was placed and covered with a platelet-poor plasma membrane and a periosteal flap after the surgical work. No complications or recurrences were reported over the following 6–10 years, and bone formation recovery was demonstrated.
Alternative synthetic materials are also available. Taghizadeh et al. compared the use of fat with hydroxyapatite cement for frontal sinus obliteration after mucocele resection.Reference Taghizadeh, Krömer and Laedrach 40 Treatment failed for 2 of the 16 patients in the fat obliteration group; there were no cases of failure in the hydroxyapatite group. The authors concluded that, given the minimal morbidity and lack of contour deficit, hydroxyapatite is an effective and well-tolerated material for frontal sinus obliteration.
Eloy et al. demonstrated that calcium phosphate bone cement was an alternative material for sinus obliteration in a rabbit model.Reference Eloy, Altman, Hoch, Munoz and Shohet 41 Further investigations are needed for long-term evaluation and proof of benefit in chronically infected sinuses.
In our patients, we used a fully synthetic, osteoconductive and resorbable bone graft substitute consisting of pure ß-tricalcium phosphate, with a compressive strength similar to that of cancellous bone. Over the past 25 years, this material has been used in trauma, orthopaedic and spinal surgical procedures.Reference Becker, Maissen, Ponomarev, Stoll, Rahn and Wilke 42 , Reference Gazdag, Lane, Glaser and Forster 43 Autologous bone grafting is associated with various deficiencies and several complications. Donor site pain can continue for many years after surgery. Inadequate quality or volume can limit bone harvesting. Allogenic bone grafts may be infected as a result of the donor.
The advantage of using a synthetic material like ß-tricalcium phosphate is the uniform quality, the unlimited availability, and the avoidance of a donor site with all its possible associated complications such as wound infection, pain, paraesthesia and scar formation. The osteoconductive property of ß-tricalcium phosphate, associated with overall porosity and macropores, helps to induce the bone remodelling process by encouraging the ingrowing of bone cells and blood vessels. ß-tricalcium phosphate mimics cancellous bone. It is resorbed and completely remodelled into the host bone within 6–18 months after implantation. It is easy to use as an ‘off-the-shelf’ product, and is available as granules of different sizes to fit precisely into the bone defects. Thus, operating time is significantly reduced. ß-tricalcium phosphate is rapidly resorbed because it is chemically and structurally similar to bone. Osteoclasts resorb the ß-tricalcium phosphate. Fortunately, resorption and bone remodelling takes place at the same time. While osteoclasts resorb, the tricalcium-phosphate osteoblasts fill the lacunes created by osteoclasts by producing an extracellular matrix, which is subsequently calcified. In contrast, hydroxyapatite resorbs very slowly.Reference Buser, Hoffmann, Bernard, Lussi, Mettler and Schenk 44 The bone remodelling is evident on post-operative CT scans.
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• Osteoplastic frontal sinus obliteration is a key first-line and salvage surgical treatment for chronic frontal sinus disease
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• The best material for frontal sinus obliteration remains controversial
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• This paper reports our experience with resorbable β-tricalcium phosphate for frontal sinus obliteration in frontal sinus mucocele patients
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• β-tricalcium phosphate is a good, safe and cost-effective alternative to autologous and allogenic materials
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• Its use avoids donor site morbidity and complications, and shortens surgery time
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• Furthermore, it has unlimited availability and uniform quality, with no chance of infection
In our study, both ß-tricalcium phosphate and freeze-dried human cancellous bone were well tolerated. Both are easily used as ‘off-the-shelf’ products. Nevertheless, the cost of ß-tricalcium phosphate is a third lower than that of allogenic spongiosa, and there is no possible chance of donor infection.
Hence, ß-tricalcium phosphate is a good, safe and cost-effective alternative to autologous bone and fat, because it avoids donor site morbidity and complications, shortens the duration of overall surgery, and has unlimited availability and uniform quality. It is a good alternative to commercially available allogenic bone grafts regarding possible donor infection and costs. No patient in the ß-tricalcium phosphate group showed further symptoms or had additional surgery during the five- and eight-year follow-up periods. Further studies comprising more patients are needed to confirm these findings.
