References

Costea MC, Bondor CI, Muntean A, Badea ME, Mesaros MS, Kuipers-Jaqtman AM. Proximity of the roots of posterior teeth to the maxillary sinus in different facial biotypes. Am J Orthodont Dentofacial Orthop. 2018; 154:346-355
Kang SH, Kim BS, Kim Y. Proximity of posterior teeth to the maxillary sinus and buccal bone thickness: a biometric assessment using cone beam computed tomography. J Endod. 2015; 41:1839-1846
Tian XM, Qian L, Xin XZ, Wei B, Gong Y. An analysis of the proximity of maxillary posterior teeth to the maxillary sinus using cone beam computed tomography. J Endod. 2016; 42:371-737
Horner K, Eaton K.London: Faculty of General Dental Practice; 2018
Cone Beam CT for Dental and Maxillofacial Radiology. Evidence Based Guidelines. SEDENTEXCT Project. Radiation Protection No. 172. European Commission. http://www.sedentexct.eu/files/radiation_protection_172.pdf (Accessed April 2019)
Bell G. Oro-antral fistulae and fractured tuberosities. Br Dent J. 2011; 211:119-123
Interventions for treating oroantral communications and fistulae due to dental procedures. Cochrane Database Syst Revs 2016, Issue 5. Art No: CD011784. https://www.cochranelibrary.com/cdsr/ (Accessed April 2019)
Von Wowern N. Correlation between the development of an oroantral fistula and the size of the corresponding bony defect. J Oral Surg. 1973; 31:98-102
Peninsula Dental Social Enterprise. Extraction – Management of an oroantral communication (OAC). Version 2. 2017. http://peninsuladental.org.uk/wp-content/uploads/2017/10/Extraction-Management-of-an-Oro-antral-communication-guidelines.pdf (Accessed April 2019 – advice since withdrawn)
Ehrl PA. Oroantral communication: epicritical study of 175 patients, with special concern to secondary operative closure. Int J Oral Surg. 1980; 9:351-358
Selvi F, Cakarer S, Keskin C, Ozyuvaci H. Delayed removal of a maxillary third molar accidentally displaced into the infratemporal fossa. J Craniofac Surg. 2011; 22:1931-1933
Osashi Y, Nakai Y, Ikeoka H Effects of bacterial endotoxin on the ciliary activity in the in vitro eustachian tube. Arch Otorhinolaryngol. 1987; 224:88-90
Simmen D, Jones N. Chapter 8, 2nd edn. : Thieme Medical Publishers; 2013
Chandrasena F, Singh A, Visavadia BG. Removal of a root from the maxillary sinus using functional endoscopis sinus surgery. Br J Oral Maxillofac Surg. 2010; 48:558-559
Tocaciu S, Sillifant P. Spontaneous clearance of a dislodged root in the maxillary antrum. Oral Surg. 2018; 11:224-227
Visscher SH, van Minnen B, Bos RR. Closure of oroantral communications: a review of the literature. J Oral Maxillofac Surg. 2010; 68:1384-1391
Von Wowern N. Closure of oroantral fistula with buccal flap: Rehrmann verses Moczar. Int J Oral Surg. 1982; 11:156-165
Kaneshiro S, Nakajima T, Yoshikawa Y, Iwasaki H, Tokiwa N. The post-operative maxillary cyst: report of 71 cases. J Oral Surg. 1981; 39:191-198
Yamamoto S, Maeda K, Kouchi I Surgical ciliated cyst following maxillary sinus floor augmentation: a case report. J Oral Implantol. 2017; 43:360-364
Decision-making and closure of oroantral communication and fistula. 2019. https://doi.org/10.1186/s40729-019-0165-7 (Accessed April 2019)
Comprehensive review on endonasal endoscopic sinus surgery. 2015. https://doi.org/10.3205/cto000123 (Accessed April 2019)

The Maxillary Sinus: What the General Dental Team Need to Know Part 2: Removal of Teeth; Avoidance and Management of Complications

From Volume 47, Issue 5, May 2020 | Pages 405-414

Authors

Garmon W Bell

BDS, MSc, FDC RCS, FFD RCSI(OS)

Associate Specialist Oral and Maxillofacial Surgery, Dumfries and Galloway Royal Infirmary

Articles by Garmon W Bell

Iain Macleod

BDS, PhD, FDS RCS, FRCR DDRRCR FHEA

Consultant Radiologist, Department of Dental Radiology, Newcastle Dental Hospital, Framlington Place, Newcastle-upon-Tyne, NE2 4BW, UK

Articles by Iain Macleod

James C Darcey

BDS, MSc, MDPH MFGDP, MEndo FDS(Rest Dent)

Consultant and Honorary Lecturer in Restorative Dentistry and Specialist in Endodontics, University Dental Hospital of Manchester

Articles by James C Darcey

Colin Campbell

BDS, FDS RCS, BDS, FDSRCS

Specialist in Oral Surgery with sub-specialty interest in Implantology, The Campbell Clinic, Nottingham, NG2 7JS, UK

Articles by Colin Campbell

Email Colin Campbell

Abstract

In the second of this 4-part series we will discuss the removal of teeth closely related to the maxillary sinus, with identification and reduction of risk factors for oro-antral communication and the management of complications.

CPD/Clinical Relevance: Posterior maxillary teeth can be intimately related to the maxillary sinus. The Dental Team should be able to provide oral healthcare procedures avoiding interference with the normal function of the paranasal air-space, but also need to be able to identify and manage complications when they arise.

Article

Garmon W Bell
Iain MacLeod
James C Darcey
Colin Campbell

In part 1 the accurate diagnosis of acute and chronic orofacial pain and headaches was discussed, with reference to the specific diagnostic criteria required for pain related to acute paranasal sinus infection. A variety of symptoms and signs were outlined to facilitate an accurate diagnosis of odontogenic causes of unilateral maxillary pain, thus avoiding incorrect and unnecessary treatment.

When an odontogenic cause is identified, either removal of the tooth or endodontic treatment is indicated. In this second paper of the series the removal of teeth that are intimately related to the maxillary sinus will be discussed, with emphasis on risk assessment and management.

The relation of posterior maxillary teeth to the maxillary sinus is variable for individual patients and specific teeth.1,2 Some patients will have many millimetres of bone between the apices of their posterior maxillary teeth and the maxillary sinus lining, while for some there is none.3 Risk is therefore best assessed for individual teeth, and discussed with the patient as part of the consent process before undertaking any operative procedure. While there is variation in the incidence of oro-antral communications following the removal of various posterior maxillary teeth, there is no percentage that may be reliably quoted to patients as an estimation of risk during the consenting process.

Assessment of risk

Dentists will only be aware of a close relation of a tooth to the maxillary sinus through radiographic assessment. Faculty of General Dental Practice guidelines do not support routine radiography before removal of teeth unless in the presence of adjacent anatomical factors that increase risk.4 In the interests of patient safety, pre-operative radiography would be supported for any maxillary tooth posterior to the canine. Use should be made of pre-existing radiographs where possible. Routine use of Cone Beam Computed Tomography (CBCT) has not been shown to reduce the incidence of complications and cannot be supported for routine exodontia, but is supported for certain endodontic and implant-related scenarios to be discussed in Parts 3 and 4 of this series.5

The maxillary sinus may extend between the roots of individual teeth or between adjacent teeth. Useful tips to assess a pre-operative radiograph are outlined in Figures 1-3. The floor of the maxillary sinus will be identifiable by its corticated outline in relation to the roots of the teeth. When the maxillary sinus floor is not of sufficient thickness to attenuate x-ray photons to be observed on radiographs, the dentist will know that the sinus floor becomes the thin layer of the periodontal ligament space. On occasion, there is no bone between the roots of the teeth and the sinus, particularly with chronic apical periodontitis. In such situations the dentist will be alerted to the increased risk of exposure or perforation of the maxillary sinus lining during removal of teeth.

Figure 1. Peri-apical radiograph of left maxillary teeth. The upper left first molar has an acute irreversible pulpitis. The corticated margin of the sinus floor is identifiable from the canine apex extending across the apices of the premolar teeth. The corticated floor is still identifiable but less obvious in the area of the first molar. The first molar root apices are closely related to the maxillary sinus. The maxillary sinus lining is thickened, but within variation of normal, and not related to any dental disease.
Figure 2. Peri-apical radiograph of left maxillary teeth. The sinus is seen to project between the roots of the second premolar and the second molar. (First molar missing – space closed.) The sinus can be identified as compared to an apical cyst because of the dark lines caused by blood vessels passing through the lateral sinus wall, and also by a persistence of trabecular pattern of bone, as compared to the uniform radiolucency of a radicular cyst. The corticated outline of the sinus floor may be traced but it disappears in the region of the second molar due to insufficient density of bone to attenuate X-ray photons. In this situation, the sinus floor is incredibly thin with no bone so the mucosa directly abuts the roots of the second molar.
Figure 3. Peri-apical radiograph of right maxillary molar teeth. There is an irreversible pulpitis involving the second molar tooth because of leakage below a full coronal restoration, with caries, and extraction is planned. There is a small amount of thickening of the maxillary sinus lining over the apices of the molar teeth which may or may not be attributable to the pulpal disease processes. The thickness of bone on the sinus floor is so thin that X-ray photons are not well attenuated and therefore the corticated outline of the sinus floor can only be identified with difficulty.

However, dentists should also be aware that complete loss of the corticated floor of the maxillary sinus, particularly with poorly defined edges of adjacent bone, is suggestive of malignancy, and appropriate urgent referral would be indicated. The radiograph in Figure 4 illustrates such a case, where there may be no patient symptoms or clinical signs until an advanced stage of disease.

Figure 4. A dental panoramic tomogram with loss of cortical outline of the left maxillary sinus, and increased opacification of air space, associated with malignancy of the maxillary sinus.

Removal of teeth – avoiding displaced roots or lining perforation

In addition to the radiographic features described above, specific anatomical features of the bone or tooth to be removed can predispose to maxillary sinus or tuberosity involvement.6 These are described in Table 1. The removal of teeth involves expansion and displacement of the bone around the tooth roots, and any reduced elasticity or increased thickness or density of bone will resist that process. Fusion of adjacent teeth or divergence of roots will require increased load on the supporting bone during expansion of the socket, with the increased risk of bone fracture involving the maxillary sinus floor or tuberosity. Figure 5 illustrates a case where removal of the maxillary second molar with forceps elevation alone would increase the risk of buccal bone fracture, with the unerupted third molar and bone of tuberosity also being delivered. Figure 6 illustrates a case of concrescence, where teeth are fused by cementum overgrowth thus complicating the removal of one or the other tooth, hence both teeth being delivered together. Concrescence may be identified radiographically by the indistinct outline of the periodontal ligament space between individual teeth.


▪ Enlarged maxillary sinus;
▪ Divergent roots of maxillary molar;
▪ Lone standing maxillary molar;
▪ Second molar scheduled for extraction with unerupted third molar sitting apical;
▪ Thickened and inelastic buccal plate of bone (age and ethnicity dependant);
▪ Hypercementosis;
▪ Concrescence (roots of teeth fused through abnormal cementum growth);
▪ Heavily restored tooth.
Figure 5. Sectional dental panoramic tomogram illustrating impacted left maxillary third molar high in the alveolus, along with an enlarged maxillary sinus presenting as a risk factor for alveolar fracture.
Figure 6. Concrescence between maxillary molar teeth.

Reducing the risk of exposure or perforation of the maxillary sinus lining during removal of teeth requires reduction of the force applied to the alveolus, so that the bony floor remains intact, or at least if the bone comes away the lining remains intact. Methods to reduce this force have been described previously but generally involve removal of buccal bone and division of the roots of molar teeth (where sufficiently divergent), as outlined in Figures 7-9.6

Figure 7. (a, b) Simple forceps delivery with buccal elevation concentrates forces on the lateral floor of the maxillary sinus when stretching bone during elevation of teeth, increasing risk of fracture (red circle) – see Figure 9. Removal of buccal bone reduces the load on the bone of the sinus floor, facilitating alveolar expansion, with the aim of reducing the risk of the sinus floor coming away with the roots.
Figure 8. Division of roots of multi-rooted teeth further reduces the forces placed on the sinus floor during elevation, reducing risk of sinus floor coming away during removal of roots. However, exercise caution with depth of bur to avoid perforation of the sinus floor.
Figure 9. (a, b) Despite removal of buccal bone, the lateral sinus floor came away with the roots. The roots were divergent and should have been divided and elevated separately. However, the sinus lining was intact with no perforation and, having planned soft tissue access in advance, the muco-periosteum was advanced to protect the exposed lining.

Use of elevators is an essential skill, and use of luxators are a less favourable instrument when used with teeth or roots that are closely related to the maxillary sinus. With elevators, a rotating motion may be used to elevate the root away from the sinus floor. However, luxators require a pushing technique along the long axis of the root or tooth, hence the chance of displacement of the root into the sinus is significantly increased (Figures 10, 11).

Figure 10. Composite image showing safe use of Coupland's elevator at an angle perpendicular to the long axis of the roots and away from the direction of the sinus (a), as compared to apical pushing with the elevator in the direction of the sinus, with risk of root displacement (b).
Figure 11. (a, b) Peri-apical radiographs showing root morphology of maxillary first premolar tooth. The buccal root apex fractured, and exploration using a luxator with vertical force towards the apex displaced the root apex into the sinus.

Central to hard tissue management is soft tissue access. Therefore, the dentist should plan for exposure or perforation of the sinus lining and design soft tissue access around the need for a buccal advancement flap, if required. If, having identified a risk, the dentist is not confident to perform either the soft or hard tissue surgery required, specialist referral would be appropriate.

Managing the complications of raising mucosa and advancement of buccal muco-periosteum has been described before, and is a skill best learned under supervision and controlled conditions.6 There is little to be gained by the general dentist trying to pull the gingival tissues together without proper release of muco-periosteum. Such a technique only traumatizes the gingival tissues and complicates later closure of an oro-antral communication. A fistula, the epithelial-lined tract between two epithelial surfaces, will only develop if the communication does not or is not closed.

Identification of an oro-antral communication

Following complete and successful removal of a tooth, the dentist may wish to determine whether or not there is perforation of the maxillary sinus lining. Techniques are outlined in Table 2 and Figure 12.


Direct inspection
Sound of suction
Bubbles of air in saliva or blood
Fogging of dental mirror
Displacement of cotton pledget from extraction site on expiration
Pinching nose during exhalation
Figure 12. Surgical site following surgical removal of upper left first and second molar teeth. Close relation to the sinus was identified pre-operatively, and precautionary measures taken involving raising the buccal flap so that it could be used as a buccal advancement flap, along with the removal of buccal bone. The sinus lining was attached to the apex of the first molar mesio-buccal root with tearing occurring upon elevation of the tooth (dark area).

Irrigation and direct inspection of the socket is the most reliable technique. The dental team should ensure that high volume suction is not used when inspecting a socket for exposed sinus lining, as the force of suction can often be sufficient to produce a tear of the thin lining. Fine surgical suction is best used for this purpose. The change in noise of air flow when there is a sinus communication is very characteristic, and may be compared to the sound of air escaping through a partially open door or window.

It should be noted that holding the nose during forced expiration to assess sinus lining patency is controversial as the change in pressure by pinching the nose can be sufficient to blow open a perforation in what was a previously intact sinus lining.

There is a divergence of opinions as to whether oro-antral communications should be closed surgically or managed conservatively and observed in the hope that they will heal without fistula formation. There is no evidence for one treatment strategy over another.7 Various dimensions, between 2 and 7 mm, are quoted as being the cut-off diameter at which oro-antral communications will heal spontaneously.8 Most oro-antral communications less than 3 mm diameter will close over without surgical intervention, although the position of such within the socket is critical. A communication at the apex of a deep socket is more likely to heal as compared to a communication closer to the alveolar margin (Figure 13).

Figure 13. Position of perforation of the sinus lining with an upper first molar socket. The oro-antral communication (a), which is at the apex of the mesio-buccal root, will probably heal without fistula formation, as compared to the oro-antral communication (b), which is closer to the gingival margin, and will have a lesser height of coagulum to provide isolation from the oral microflora.

While small communications will heal without the need for intervention, close observation of the patient over the first month following removal of the tooth is recommended, while the patient avoids any activities that would cause a difference between nasal and oral air pressures (Table 3). It is acknowledged that many small oro-antral communications that arise are never observed by the dentist, with the patient experiencing no symptoms and healing occurring without event. There are also a small number of oro-antral communications that will contribute to symptoms in the first month following removal of a tooth which subsequently heal without intervention.


▪ Nose blowing;
▪ Forcefully holding in a sneeze;
▪ Popping one's ears in response to change in air pressure;
▪ Sucking through a straw;
▪ Playing wind musical instruments requiring maintenance of high oral cavity pressure;
▪ Snorkelling or scuba diving;
▪ Self-inflation of balloon or any other air-filled device;
▪ Spending time in a decompression or hyperbaric chamber.

Historically, most guidelines for primary care dentists recommend conservative management, with referral only for large oro-antral communications or when the presence of a fistula is confirmed, or persistent signs of maxillary sinus infection are confirmed.9 There is a risk with this strategy that, if healing does not occur, chronic infection of the maxillary sinus arises. It has been suggested that maxillary sinus infection may become established within 2–3 days following exposure to oral microflora.10 The established sinus infection can be more difficult to control at a later date, often involving prolonged uncomfortable and unpleasant symptoms for the patient. Additionally, delayed surgical intervention can be more extensive and carries a greater risk of failed surgical closure of any fistula because of infection within the sinus. It is for this reason that some surgeons recommend closure of any oro-antral communication within the first 2–3 days following its creation.

Discussion with the patient both pre- and post-operatively, enabling shared decision-making, is recommended in these circumstances. A contemporaneous record of such discussions should be made.

The exposed and intact maxillary sinus lining, if not protected by a sufficient depth of coagulum or by primary repair within 2–3 days of surgery, may prolapse through the extraction site into the oral cavity, as illustrated in Figure 14. A prolapsed lining as shown will always require surgical repair.

Figure 14. Composite image of two cases of prolapsed maxillary sinus lining. (a) A smaller prolapse that had been present for over one year and had become epithelized by the oral mucosa. (b) A larger prolapse that has become haemorrhagic and congested.

Identification of displaced roots or teeth

In the event of the dentist losing control of a root of a maxillary posterior tooth during elevation, displacement into the maxillary sinus is likely. Deeply impacted maxillary third molars may be displaced into the pterygoid soft tissues, but this procedure is unlikely to be performed by the general dental surgeon.11

On occasion the root may still be visible at the apex of the socket, with removal via the socket being the route of choice. However, the exposed and torn sinus lining will require repair and, if the general dentist is not confident in performing the hard and soft tissue surgery required, specialist referral is recommended.

Once the roots or the whole tooth is lost from the socket, the position should be confirmed radiographically. A Dental Panoramic Tomogram (DPT) is the radiograph used most often for this purpose. However, the focal trough of the DPT is often more narrow than the width of the maxillary sinus, such that marked lateral or medial positioning of the root in the sinus is not visible, as it is outside the plane of focus (Figure 15). Therefore, the CBCT is the imaging modality of choice for identification of displaced roots of teeth into the maxillary sinus.

Figure 15. Axial slice of Cone Beam Computed Tomographic (CBCT) image at the level of greatest lateral dimension of the maxillary sinus with the focal area of the DPT superimposed. The sharpest focus in the trough is intense yellow; lesser peripheral focus is translucent yellow.

Removal of displaced roots or teeth from the sinus

When the roots of teeth or whole teeth are displaced they should be removed as, along with the persistent leakage of oral micro-organisms, they will form a focus of infection within the maxillary sinus, contributing to disease of odontogenic origin. Endotoxins from bacteria reduce ciliary activity, contributing to secondary impaired muco-ciliary clearance and infection due to stasis.12 The removal of displaced teeth or roots and sinus lavage is generally not required immediately, and involves planning and discussion with the patient, but prolonged delay will contribute more to chronic maxillary sinus infection, that can be more difficult to resolve.

If it is not possible to remove roots of teeth through the socket, then the most convenient approach for the specialist dental team is the anterior wall of the maxilla via a high labial antrostomy. Limiting the size of the high labial antrostomy reduces the recognized complications of infra-orbital paraesthesia, alveolar anaesthesia, and post-operative facial oedema and ecchymosis (Figure 16). This role is best performed by a specialist, and referral is recommended.

Figure 16. A high labial antrostomy being used for removal of a displaced root from the left maxillary sinus. An antrostomy width of less than 10 mm is generally sufficient.

With the development of surgical endoscopes, access may also be gained to the maxillary sinus through the nasal cavity by removal of the uncinate process and overlying soft tissue in the middle meatus.13,14 This is a procedure performed by ear, nose and throat (ENT) surgeons and facilitates removal of foreign bodies from the sinus and also facilitates improved drainage from the sinus when the ostium is narrowed.

On occasion, displaced roots of teeth may be voided from the maxillary sinus through the ostium by the same mechanism that provides muco-ciliary clearance.15 Therefore, it is prudent for the surgeon to perform radiological assessment, using CBCT, a day prior to scheduled surgery on the basis that the root(s) may have already been voided and exploration is no longer required (Figure 17).

Figure 17. Coronal reconstruction of multi-slice computed tomographic scan showing displaced root of maxillary molar tooth at the ostium of the right maxillary sinus awaiting transfer into the nasal space where it will be swallowed along with mucus secretions, and passed naturally from the body. The oral communication closed without surgery following displacement of the root, such that chronic infection did not occur. There is no mucosal thickening of the sinus and it is well aerated.

Management of long-standing maxillary sinus disease of odontogenic origin

For chronic maxillary sinus infection as a result of long-standing oro-antral fistula, displaced teeth, roots of teeth, or dental materials, hospital-based care is recommended. Treatment in the dental practice is not advised as there are many other factors to be taken into consideration, such as established infection, with soft tissue hyperplasia in the sinus obscuring access, and the possibility of reduced patency of the ostium in the middle meatus because of mucosal oedema. Without restoration of normal muco-ciliary clearance from the sinus, recovery will not occur. Therefore, a combined intra-nasal approach with endoscopic sinus surgery by ENT surgeons is often required.

Various surgical options have been reported for the excision and closure of oro-antral fistulas. They are best classified as either one or two stage procedures,16 but there is no evidence that one procedure is more reliable than another, as most reports are of single patients, small case series or very limited randomized control studies.7 Various autografts, xenografts, alloplastic materials, metal or plastic sheets and adhesives have been described.16 The decision of which technique or material to use will depend on the individual needs of the patient and the preference of the treating surgeon. However, the buccal advancement flap is generally regarded as the most reliable and readily available tissue for repair of an oro-antral communication or fistula.17

An interesting observation, which demonstrates the special ability of the paranasal sinus environment to respond to contamination, is that of a long-standing, small oro-antral fistula persisting without chronic infection of the maxillary sinus (Figure 18). Such a fistula will still subsequently require repair to avoid infection should the physiological balance within the sinus change at a later date.

Figure 18. Coronal reconstruction of a multi-slice computed tomographic scan of the paranasal sinuses demonstrating a small persistent fistula at the site of the left second molar (red arrow), without signs of infection in the sinus. A periodontal probe can be passed through the fistula. The displaced root in the sinus from the time of extraction had already been voided through muco-ciliary clearance.

Post-operative surgical ciliated cyst

Dental surgery involving the maxillary sinus such as that required to remove teeth or roots, cysts or tumours from the maxillary sinus, or orthognathic surgery to the maxilla, but also dental implant placement involving the sinus floor can, on occasion, lead to the development of cysts at a later date. The cysts, composed of respiratory epithelial lining, may be referred to by various names; post-operative maxillary cyst, surgical ciliated cyst or implantation cyst, and they arise through disruption of the maxillary sinus lining. Management is through surgical enucleation.18,19

Summary

The maxillary sinus has a unique physiological function that dentists should aim to preserve. Even when roots of teeth or dental materials are displaced into the sinus, muco-ciliary clearance will often remove such contaminants, but the ability to do so depends upon the host response and the extent of the insult from toxins arising from teeth and roots, oral bacteria, or irritation from dental materials.

We have intentionally not developed the text to cover some of the details of surgery for the specialist surgeon. Interested readers may wish to refer to other texts related to various techniques for closure of oro-antral communications and also endoscopic paranasal surgery.16,20,21

In Part 3 of this series maxillary sinus disease of endodontic origin will be discussed. This will include the variation of the maxillary sinus lining in health and disease, with emphasis on accurate endodontic diagnosis, including management of complications from endodontic materials extruded into the sinus space.