From Volume 47, Issue 6, June 2020 | Pages 500-509
This paper, part 3 of the series, discusses the variation in maxillary sinus mucosal thickening when seen on radiographic images and the relation to disease. The role of apical periodontitis in disease of the maxillary sinus and its lining, the stages of endodontic treatment at which problems can arise and how these can be prevented, are considered. Complications involving extruded endodontic materials will also be discussed.
In this third paper on the maxillary sinus and the importance to the Dental Team, the role that chronic apical periodontitis contributes to maxillary sinus disease of endodontic origin is examined, and the modifications to endodontic technique needed to avoid maxillary sinus involvement are discussed.
It is frequently reported that approximately 12% of cases of unilateral maxillary sinusitis are of dental origin.1 Some authors report as high as 75% prevalence.2,3 Considering the prevalence of apical periodontitis in the population, the relatively high proportion of unilateral cases of maxillary sinusitis attributed to odontogenic causes is not reflected in the work load of most Ear Nose and Throat surgeons, or the Oral/Oral and Maxillofacial surgeons who work alongside them. It is therefore quite probable that, while there is an ample supply of case reports and case series of endodontic and periodontal disease contributing to inflammation of the maxillary sinus lining, or suppurative chronic maxillary sinusitis, there may have been bias in patient selection such that the cases presented may not accurately reflect the prevalence within the greater population.
Oro-antral fistulae, and displaced roots of teeth are the greatest contributory factors to maxillary sinus disease of odontogenic origin.4 Apical periodontitis, periodontal disease, ectopic teeth or odontomes, with or without cystic involvement, may also cause maxillary sinus disease.4 Dental implants with bone regenerative techniques are regarded as making an increasing contribution, and will be discussed in part 4 of this series.
Inflammatory changes of the paranasal sinus lining are generally of an allergenic nature, although these may also occur due to localized or atmospheric irritants. Changes are often identified via co-incidential findings on computed tomography or magnetic reasonance imaging scans performed for purposes other than imaging of the paranasal sinuses.5,6 These inflammatory changes can range from areas of localized thickening, to retention cysts caused by duct obstruction in a sero-mucinous gland, or polyps and expansile mucoceles. Mucosal thickening is a common finding in ethmoid and maxillary sinuses, as are retention cysts. As a result of ostial obstruction, mucoceles can exert pressure, causing bone expansion and resorption. However, these are rarely found in the maxillary sinus, presenting more often in the frontal sinus. One presentation of inflammatory paranasal mucosal swelling does not necessarily progress to another.
There is little correlation between signs of paranasal sinus lining thickening and patient reported symptoms of disease.7 There is little agreement on what level of maxillary sinus thickening is within variation of normal or related to disease, although generalized thickening of 5 mm or more can be associated with increased incidence of ostial obstruction.8,9 There is a recognized cyclical variation over a period of hours of the thickness of nasal and ethmoid sinus mucosa as a result of congestion related to blood flow, such that the mucosa when viewed on cross-sectional imaging will vary depending upon the time of imaging.10 The maxillary sinus lining does not show this same pattern.
Thickening of the paranasal sinus lining has previously been identified on plain radiographs of the paranasal sinuses in 50% of the population, who have no symptoms of disease and were subsequently identified as not having rhinosinal disease.11 Thickening of the maxillary sinus lining has always been visible on plain radiographic intra-oral films and continues to be visible on modern digital systems. With the exponential use of Cone Beam Computed Tomographic (CBCT) scanning in Dentistry, maxillary sinus lining thickening is now observed more often by dentists, as is the incidence of apical periodontitis. However, there are conflicting reports as to the role of apical periodontitis and periodontal disease in contributing to maxillary sinus thickening. Some authors report increased thickness of the maxillary sinus lining in association with periodontal disease, and others reduction in maxillary sinus thickening following treatment of chronic dental infection.12,13 However, others have been unable to demonstrate any significant difference in sinus lining thickening between healthy and unhealthy dentitions.14 Maxillary sinus lining thickening has also been reported in disease-free dentitions.15 There is a risk that, as a result of the additional imaging that is now more freely available, the Dental Profession may be observing something that was always there and not necessarily related to odontogenic disease, particularly when the patient selection is not randomized from the general population (Figures 1 and 2). In the process of making observations from radiographic images and comparing such to the presence or absence of odontogenic disease, the matter of aeration of the sinus and normal muco-ciliary clearance, which contribute to sinus function, may not be considered, nor the presence or absence of patient symptoms.
Retention cysts of the floor of the maxillary sinus are a well-recognized feature of dental radiography. Caused by obstruction of the duct within sero-mucinous glands of the maxillary sinus, they are of no clinical significance on the basis that there are no signs of loss of adjacent bone.
Being able to separate a retention cyst from an odontogenic lesion is a basic skill for the dental surgeon. An odontogenic cyst will have a corticated upper border as the area of bone apical to the source of infection will have expanded upwards. If the tooth that is the source of infection remains, it is usually centrally positioned within the cystic lesion. A retention cyst which has arisen within the mucosa of the sinus lining will not have any bone involvement and, as such, will not have a corticated upper border and will appear opaque as compared to the surrounding air of the sinus (Figures 3 and 4).
The apices of maxillary teeth distal to the canine lie in close proximity to the maxillary sinus, and this can only be evaluated by radiography. There are many publications reporting the relation of roots of various teeth to the floor of the maxillary sinus, involving a broad range of imaging modalities. Despite the increased amount of information available from CBCT, for most diagnostic and therapeutic purposes peri-apical radiography of maxillary teeth should be sufficient.16,17 Periapical radiographs should be grade 1 (National Radiological Protection Board), with 3 mm of tissue visible beyond the apex.18 CBCT should not be regarded as a first line radiographic investigation for endodontic diagnosis or treatment.16
The radiographic artefact, known as the lamina dura, should be traced around each root where possible, acknowledging that, on occasions, there will be no bone between the roots of posterior maxillary teeth and the lining of the maxillary sinus.19 Changes can be described from thickening of the lamina dura, widening of the periodontal ligament space or frank loss of lamina dura. Condensing osteitis may be seen frequently in the mandible but rarely in the posterior maxilla. When a radiolucency exists, diffuse margins may reflect recent bone loss and well corticated margins reflect a chronic disease process (Figures 5–7).
On rare occasions, odontogenic infection within the maxillary sinus may behave in a fashion similar to severe acute bacterial rhinosinal disease by extension into the orbit and from there intracranially.20
Involvement of the maxillary sinus floor or mucosa in apical periodontitis should not be regarded as a contra-indication to conventional endodontic treatment. On the basis that there are no suppurative changes in the sinus, conventional root canal treatment should be undertaken and the lesion will resolve21,22 (Figure 8).
The primary mechanical and biological goals of root canal treatment are to create a shape within the canal that can be predictably cleaned and filled.23,24 Although it is accepted that the radiographic and anatomical apex are rarely coincident, shaping, cleaning and obturation within 1–2 mm of the radiographic apex is associated with improved outcomes.25,26,27 From a purely endodontic perspective, over preparation and any subsequent over fill or over extension of endodontic material is associated with a significant reduction in success of treatment.26 With respect to preventing sinus inflammation and disease, length control is equally important. Not only is the maxillary sinus in close proximity to the apices, it offers little or no resistance to endodontic extrusions. This potentially increases the risk of:
The consequences of these preventable complications to the sinus are discussed below.
Routine root canal treatment is associated with apical tissue damage, but iatrogenic mechanical trauma from instrumentation and introduction of both debris and bacteria into the tissues will result in more inflammation.28,29,30,31,32 The extrusion of inter-appointment dressings, such as calcium hydroxide, will result in inflammation because of alkalinity that may cause transient pain.33,34,35 Small debris and bacteria are readily phagocytosed, may be removed by muco-ciliary function, and are of little consequence. Larger portions that cannot be cleared will cause inflammation, tissue damage and stasis with infection.
The principle irrigant of choice remains sodium hypochlorite and the extrusion of this apically can result in tissue damage.36,37,38 This can result in immediate severe pain, haemorrhage and swelling. As the inflammatory reaction increases, there may be increased swelling, bruising and ultimately tissue necrosis, with or without paresthesia of oral mucosa or skin of the face, depending on the extent of extrusion.39
Inadvertent extrusion of hypochlorite into the maxillary sinus airspace will rarely cause pain, as the mucosa will protect the underlying bone. The mucosa will experience a chemical injury and muco-ciliary clearance will be reduced. Most patients will only experience an unpleasant hypochlorite taste for the following few hours until the small volume of hypochlorite is removed by residual muco-ciliary function. One case report described the need for antral access, lavage and ultimately extraction of the tooth.38 However, as the paranasal sinuses and nasal cavity combined produce 1.5–2.0 litres of sero-mucinous secretions per day, the maxillary sinus should be regarded as self-cleansing and have sufficient volume of secretions to overcome any ingress of irrigant, on the basis that the concentration is not so high as to cause a severe chemical injury to the mucosa.
Over extension of obturation materials may result in a more prolonged inflammatory response. Larger areas of GP may become encapsulated, whereas finer debris may result in a more intense inflammatory response. Either way, there may be a degree of chronic inflammation.40 Over-extended gutta percha can contribute to chronic sinusitis as a result of a foreign body producing inflammation and stasis, by reduced muco-ciliary clearance.41,42
The risk of these sinus complications and endodontic failure can be reduced with the following simple steps:
When orthograde treatment has failed and retreatment is not possible via an orthograde approach, endodontic surgery may be the only option remaining to control persistent disease. Treatment of maxillary premolars and molars will often necessitate surgery in close proximity to the sinus. Key ambitions for successful surgery without sinus complications will be:
Reports suggest that damage to the sinus lining may be common during traditional surgery.43,44,45,46 In itself this may have no long-term significance as it has been demonstrated that full regeneration of the sinus membrane will occur around 5 months following surgery.47,48 It may be that displacement of materials or the failure to control the contamination may be the main contributory factor in the initiation or persistence of inflammation of the sinus tissues.
Advances in the approach to endodontic surgery may have a significant impact upon the risk of adverse complications from the sinus. The use of magnification, microsurgical instruments, piezo and bioceramics provide the following advantages:49
Nonetheless, should the operator be aware of damage to the sinus lining, the placement of iodine-soaked (if the patient is not allergic to iodine) gauze will help reduce the risk of displacement of the root tip or retrograde materials into the sinus. Patient and clinicians should be reassured that it is unlikely that this will have an impact upon success of the treatment.49,50 It is important to have discussed this possible risk with the patient pre-operatively as part of the consenting process.
There are many case reports and case series of Aspergillosis occurring in the presence of extruded endodontic filling materials, predominantly zinc oxide based materials, and primarily gutta percha. It has been suggested that 85% of cases of Aspergillosis involving the maxillary sinus are related to over extended endodontic filling materials.51 It has also been suggested that zinc plays a crucial role in the development of Aspergillosis of the maxillary sinus as the fungus requires zinc as an essential co-enzyme to function, and with the high zinc content in endodontic filling materials the ideal environment is provided.52
Aspergillus species are a group of fungi normally present in the environment, although some warm, damp environments will contain a higher proportion of fungi. Therefore, it is inevitable that everyone will breathe aspergillus species into the naso-pharyngeal airways on a regular basis.53,54 What determines the outcome is the local environment within a person's nasal and paranasal airspaces, and also whether the host is immunocompetent or immunocompromised.55
Extruded endodontic filling materials within the maxillary sinus will act as foreign bodies, causing local inflammation and, if normal muco-ciliary clearance cannot remove the irritant, stasis will occur such that infection will arise. Aspergillosis is one such species that will take advantage of that stasis in the immunocompetent individual and produce infection. This may result in the formation of collections of material within the sinus airspace called mycetoma (fungus balls) which, if time and local conditions allow, may become calcified and can be observed as antroliths on radiographs (Figures 9 and 10). Should Aspergillosis arise within the maxillary sinus, diagnosis and treatment would be undertaken by an Ear Nose and Throat surgeon.
When fungal infection, Aspergillosis or Mucormycosis occurs in the immune-compromised individual, it does so often in the absence of any dental material and can demonstrate invasive behaviour similar to that seen in invasive malignancy of the maxillary sinus.56 Urgent referral is essential should any clinical signs or symptoms suggestive of rhinosinal malignancy present to the Dental Team (Table 1).
| Symptoms | Clinical Signs |
|---|---|
| Recurrent recent onset unilateral epistaxis | Unexplained buccal expansion of maxillary alveolus |
| Recent onset unexplained orofacial pain | Recent onset trismus |
| Diplopia | Loss of corticated outline of maxillary sinus floor or walls (radiographic sign) |
| Loss of sensation in maxillary division of trigeminal nerve | Mobility of teeth in absence of periodontal or periapical disease |
| Unilateral presence of soft tissue in anterior nares | |
| Non-healing extraction site | |
| Spontaneous formation of oro-antral fistula | |
| Dull tone to percussion of multiple posterior maxillary teeth |
Aspergillosis is relatively rare in developed societies with advanced healthcare systems. Invasive Aspergillosis of the paranasal sinuses is an increasing problem within immunocompromised patients, particularly with haematological malignancy.57 However, it is invasive pulmonary Aspergillosis in the immunocompromised patient that contributes most to morbidity and mortality.58
Dispelling the concept that zinc materials actively contribute to Aspergillosis of the maxillary sinus is the finding that there is no evidence of any influence on growth between individual Aspergillus species with differing concentrations of zinc cement.59 Therefore, rather than zinc-based endodontic materials contributing to Aspergillosis infection through a chemical route, it is more probably mediated through the route of a local irritant causing inflammation and stasis. This concept is further supported by the fact that Aspergillosis infection has been reported in the maxillary sinus when dental implants, which are zinc free, have perforated the sinus lining.60
In this paper the mechanisms of inflammatory changes within the maxillary sinus lining and how these present have been discussed. The role of acute and chronic apical periodontitis in maxillary sinus disease of endodontic origin has also been discussed. When using CBCT, caution has been urged in assuming that any thickening of the maxillary sinus lining in the presence of dental infection is dentally related: such thickening is also seen in the absence of dental infection, and should be regarded as a normal variation in the immunological response of the sinus lining to irritants.
The role of extruded endodontic materials in the maxillary sinus acting as chemical irritants, causing inflammation and stasis, and contributing to either bacterial or fungal infection, has been outlined. In the final paper in this series, the role of dental implantology in relation to maxillary sinus health and function will be discussed.
