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Int. J. Oral Maxillofac. Surg. 2014; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2014.06.007, available online at http://www.sciencedirect.com

Clinical Paper Clinical Pathology

Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis

N. Tomomatsua, N. Uzawaa, T. Aragakia,b, K. Haradaa a Department of Maxillofacial Surgery, Tokyo Medical and Dental University, Japan; b Department of Oral and Maxillofacial Radiology, Tokyo Medical and Dental University, Japan

N. Tomomatsu, N. Uzawa, T. Aragaki, K. Harada: Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis. Int. J. Oral Maxillofac. Surg. 2014; xxx: xxx–xxx. # 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Abstract. Odontogenic maxillary sinusitis (OMS) is an inflammatory disease caused by the spread of dental inflammation into the sinus. The long-term administration of antibiotic medicine and/or treatment of the causative tooth are the usual initial treatments. These initial treatments are not always effective, and the reason is not well understood. The purpose of this study was to identify factors of significance that may contribute to the results of the initial treatment of OMS. Thirty-nine patients were studied, divided into two groups according to the results of initial treatment: effective or non-effective. The effective group comprised 20 patients who were cured by initial treatment. The non-effective group comprised 19 patients who required an additional operation. The duration of symptoms, spread into the other sinuses, aperture width of the osteomeatal complex (OMC) on the side of the maxillary sinus, and anatomical variations in the sinuses were compared between the groups. The only significant difference found was in the aperture width of the OMC, which was significantly narrower in the non-effective group than in the effective group. The aperture width of the OMC may be a significant predictor of the effectiveness of initial treatment of OMS.

Introduction

Odontogenic maxillary sinusitis (OMS) is an inflammatory disease caused by the spread of dental inflammation, directly 0901-5027/000001+05

or indirectly, into the sinus. OMS accounts for approximately 10–12% of maxillary sinusitis cases.1–3 OMS may be caused by the following: a chronic oral antral fistula, foreign bodies (dental fillings, tooth roots,

Keywords: odontogenic maxillary sinusitis; osteomeatal complex; aperture width of the osteomeatal complex; coronal CT image. Accepted for publication 16 June 2014

parts of broken instruments) pushed through the root canal or antral fistula into the sinus, peri-apical granulomas or small inflammatory cysts of the molars and bicuspids, or large odontogenic cysts

# 2014 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Tomomatsu N, et al. Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis, Int J Oral Maxillofac Surg (2014), http://dx.doi.org/10.1016/j.ijom.2014.06.007

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occupying the total or subtotal space of the maxillary sinus. The treatment of OMS requires the management of sinusitis and the infectious source, which could be a tooth, implant, cyst, or tumour. Surgical treatment, such as a classical Caldwell–Luc operation, appears to be required for OMS caused by a large odontogenic cyst/tumour or a foreign body, such as an implant or extracted tooth. However, for OMS caused by a dental lesion, such as a peri-apical granuloma or small inflammatory cyst, initial treatment with the long-term administration of antibiotics and/or treatment of the causative tooth (tooth extraction or root canal treatment) has frequently been performed. The efficacy rate of these initial treatments for OMS has been reported to be 59.5%,4 indicating that these treatments are not always effective. Although the oral administration of antibiotics is effective against oral flora and sinus pathogens,5 administration for more than 3 months is not effective for OMS.4 The factors related to the success of these initial treatments have not been elucidated adequately. The obstruction of the ostium of the maxillary sinus has been shown to be responsible for the majority of maxillary sinusitis cases.6,7 In cases where the initial treatment is not effective, surgery is required to open the obstruction of the ostium. There are two types of surgical approach: the Caldwell–Luc operation and functional endoscopic sinus surgery (FESS).3,8,9 In the Caldwell–Luc operation, the antral lining is removed completely, and the mucociliary lining is replaced with non-functional mucosa. Thus, the Caldwell–Luc operation appears to be detrimental to sinus physiology. In recent years, FESS has been used successfully as an alternative to the Caldwell–Luc approach for managing maxillary sinusitis.10 Its use has been extended to the treatment of OMS. FESS is less invasive compared to the Caldwell–Luc operation, allows the recovery of normal sinus function, and is characterized by spontaneous drainage from the natural ostium. However, these surgical treatments are traumatic and carry a risk of postoperative complications, such as bleeding, facial paraesthesia, and recurrent sinusitis.11 Thus, an invasive operation should be avoided when the symptoms improve without surgery. In recent years, the osteomeatal complex (OMC), including the ostium of the maxillary sinus, has been shown to be an important anatomical index in the spectrum of sinusitis. The OMC consists of the

Fig. 1. The osteomeatal complex: coronal CT image. The osteomeatal complex is encircled by the black line. 1, maxillary sinus; 2, ethmoidal cells; 3, middle concha; 4, interior concha; 5, middle meatus; (*) maxillary ostium.

maxillary ostium, ethmoidal infundibulum, uncinate process, ethmoid bulla, hiatus semilunaris, and middle nasal concha (Fig. 1). The OMC is a functional entity of the anterior ethmoid complex that represents the final common pathway for drainage and ventilation of the frontal, maxillary, and anterior ethmoid cells. Anatomical variations that redirect nasal airflow or narrow the OMC have been implicated in the development of chronic rhinosinusitis.1 Opening a closed OMC could result in improvements in the symptoms of sinusitis.12 In OMS patients, opening a closed OMC and the appropriate initial treatment could result in an improvement of the OMS.13 Although the efficacy of rhinosinusitis treatment has been reported to be related to the anatomical structures of the OMC,14 there are few reports showing a correlation between the anatomical measurements of the OMC and the effectiveness of the initial treatment for OMS.15 The purpose of this study was to identify predictors that may contribute to the outcome of the initial treatment for OMS. Patients and methods

We studied 39 patients (Japanese adults) with OMS who were treated in the department of maxillofacial surgery of the university hospital between January 2008 and December 2012. All of these patients were diagnosed with OMS on the basis of the existence of a causative dental lesion and the presence of unilateral maxillary sinusitis by computed tomography (CT). Pretreatment CT images for all of the patients revealed a maxillary sinus that was almost completely occupied by soft tissue and abscess and also obstruction of the ostium. All of the patients in this study

Fig. 2. Odontogenic maxillary sinusitis. All of the patients were diagnosed with odontogenic maxillary sinusitis on the basis of a connection between the sinus and a causative dental lesion (bone loss around the root of the causative tooth).

were diagnosed with OMS when bone loss around the root of the causative tooth and a connection between the sinus and dental lesion were observed on CT images (Fig. 2). Since bilateral sinusitis and pan-sinusitis were regarded as ‘other sinusitis’, these were excluded from the present study. Chronic sinusitis that may have arisen from both dental and non-dental lesions, such as an allergic reaction, viral or Aspergillus infection, or a benign/malignant tumour, were also excluded from this study. Further, those with acute OMS after tooth extraction were also excluded. After dental treatment (extraction or root canal treatment) and oral administration of an antibiotic (clarithromycin, amoxicillin, cefuroxime, etc.) for 3 months,16 we examined the condition of the maxillary sinus by CT. The causative bacteria of OMS are part of the oral flora, including a-haemolytic streptococci, Staphylococcus aureus, and Peptostreptococcus, etc.2 Thus the antibiotics provided had a spectrum of activity covering these bacteria. Amoxicillin or cefuroxime was prescribed for acute sinusitis, and clarithromycin was prescribed for chronic cases. The patients were not given any other medications such as nose drops or steroids. The 39 patients were divided into two groups on the basis of the results of the initial treatment: effective and non-effective. The patients with improved intracavernous inflammation and sinusitis symptoms after the initial treatment were included in the effective group. The improvement in OMS was determined by (1) CT evidence of the reopening of the OMC and a clear sinus (disappearance of radiopacity), including normality of the mucous membrane of the sinus and the opening of the ostium; (2) the disappearance of sinusitis symptoms, such as pain, swelling, headache, and a sense of incongruity. The patients without improvement were

Please cite this article in press as: Tomomatsu N, et al. Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis, Int J Oral Maxillofac Surg (2014), http://dx.doi.org/10.1016/j.ijom.2014.06.007

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Odontogenic maxillary sinusitis included in the non-effective group. The effective group comprised 20 patients who were cured by the initial treatment. The non-effective group comprised 19 patients who required an additional operation. To identify significant factors in the two groups, we examined the following: duration of symptoms, smoking history, spread of inflammation into the other sinuses, aperture width of the osteomeatal complex on the side of the maxillary sinus (aperture width of the OMC), width of the upper OMC, distance between the ostium and floor of the maxillary sinus, distance between the ostium and inferior wall of the maxillary sinus, and anatomical variations of the sinus, such as nasal septum deviation, the presence of Haller’s cells, and concha bullosa of the middle turbinate. These factors were compared between the groups. The aperture width of the OMC was measured on coronal CT. We first drew a line through the base of the inferior nasal concha, parallel to a line linking the alveolar bone crest to the zygomatic bone. The point crossing that line at the bottom of the orbit was set as point ‘A’, and the shortest point on the lower wall of the aperture for the OMC from point A was set as point ‘B’. We measured the distance between A and B as the aperture width of the OMC (Fig. 3). The length was the average of five slices, including the ostium, on the coronal CT image. All of the CT examinations were performed using a 64-slice multidetector CT (MDCT) (SOMATOM Sensation 64; Siemens AG, Erlangen, Germany) operated at 120 kVp with 90 mAs. Both axial and coronal CT scans were performed for all of the patients. Axial scans were obtained

parallel to the nasomeatal line with a slice thickness of 0.6 mm and at intervals of 0.3 mm. The coronal image was obtained perpendicularly to the nasomeatal line with a slice thickness of 0.6 mm at intervals of 0.6 mm through the anterior portion where the OMC, including the maxillary sinus ostium and ethmoid infundibulum, were involved. All of the data are presented as the mean  standard deviation. The two groups were compared using the Mann– Whitney U-test for continuous variables (duration of symptoms, distance between the ostium and the floor of the maxillary sinus, distance between the ostium and the inferior wall of the maxillary sinus, aperture width of the OMC, and width of the upper OMC) and Fisher’s exact test for categorical variables (smoking history, inflammation spread to other sinuses, nasal septum deviation, concha bullosa, and Haller’s cells). The differences were considered significant at P < 0.05. We used the receiver operating characteristic (ROC) curve to determine the cut-off point for the aperture width of the OMC.17 These statistical analyses were performed using IBM SPSS 19.0J software (IBM Corp., Armonk, NY, USA). Results

The results of the study are shown in Table 1. Although the duration of symptoms was longer in the non-effective group compared to the effective group, the difference was not statistically significant. Smoking history and the spread of inflammation to other sinuses were not significantly different between the groups. Nasal septum deviation was present in three patients in the effective group and four patients in the non-effective group. A concha bullosa of the middle turbinate was observed in two patients in

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the effective group and two patients in the non-effective group. Haller’s cells were observed in four patients in the effective group and two patients in the non-effective group. There were no significant differences in anatomical variations, such as nasal septum deviation and Haller’s cells, between the two groups. The difference in the distance between the ostium and the floor of the maxillary sinus/inferior maxillary sinus was not significant between the groups. Although the width of the upper OMC was not significantly different between the groups, the aperture width of the OMC in the non-effective group was significantly narrower compared to the effective group. The aperture width of the OMC was 12.54  2.40 mm in the effective group and 10.09  1.89 mm in the noneffective group (P < 0.05). The distribution of the aperture width of the OMC is presented in Fig. 4a. For further assessment of the ability of the aperture width of the OMC to classify patients correctly into the effective or non-effective group, a ROC analysis was performed. The curve is presented in Fig. 4b. According to the ROC analysis, the cut-off point for the aperture width of the OMC was 11.12 mm. The sensitivity was calculated to be 0.684 and the specificity was calculated to be 0.750 at this cut-off point.15 Discussion

OMS is a type of sinusitis and requires treatment of the dental infection source, such as an apical lesion of the tooth or infected implant. We evaluated the effectiveness of the initial treatment of the causative tooth and long-term oral administration of antibiotic therapy for OMS patients. By comparing the effective and non-effective groups by CT after these

Table 1. Comparison of the two study groups: effective and non-effective initial treatment. a

Fig. 3. Measurement of the aperture width of the OMC. We first drew a line running along the inferior nasal concha base (solid line), parallel to a line linking the alveolar bone crest to the zygomatic bone (dotted line). The point crossing that line at the bottom of an orbit was set as point ‘A’, and the shortest distance to the lower wall of the aperture for the OMC from point A was set as point ‘B’. We measured the distance between A and B as the aperture width of the OMC.

Duration of symptoms (months) Smoking history Inflammation spread to other sinuses Nasal septum deviation Concha bullosa Haller’s cells The distance between the ostium and the floor of the maxillary sinusa (mm) The distance between the ostium and the inferior wall of the maxillary sinusa (mm) The aperture width of the OMCa (mm) The width of the upper OMCa (mm)

Effective

Non-effective

P-value

4.58  5.91 9/20 12/20 3/20 2/20 4/20 34.46  3.05

12.37  29.79 8/19 11/19 4/19 2/19 2/19 36.39  4.77

0.811 1 1 0.695 1 0.661 0.136

22.74  3.53

22.82  3.61

0.500

12.54  2.40 16.02  2.92

10.09  1.89 16.06  3.00

0.028* 0.944

OMC, osteomeatal complex. a The data are presented as the mean  standard deviation. * P < 0.05 versus the non-effective group.

Please cite this article in press as: Tomomatsu N, et al. Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis, Int J Oral Maxillofac Surg (2014), http://dx.doi.org/10.1016/j.ijom.2014.06.007

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Fig. 4. (a) Distribution of the aperture width of the OMC. (b) A ROC curve for the aperture width of the OMC was used to predict the prognosis for OMS; the sensitivity is plotted against 1 specificity, corresponding to the true-positive rate against the false-positive rate.

treatments, we aimed to identify factors of significance that may affect the outcome of the initial treatment for OMS. Pruna15 analyzed 208 nasal fossae with coronal CT and statistically correlated 15 parameters of OMC structure and anatomical variance with chronic sinusitis. He observed that only antero-posterior uncinate process angulation had clinical relevance, and this parameter had a negative predictive value and very low sensitivity. Thus, he concluded that no association with radiological parameters exists to explain chronic sinusitis. Fadda et al.14 indicated that although a statistically significant association was found between the presence of septal deviation and maxillary sinusitis, there was no significant correlation between other common and uncommon anatomical variations and sinus mucosal pathologies.

Our present results are similar to these previous reports, except for the aperture width of the OMC. In the pathogenesis of maxillary sinusitis, the maxillary ostium is one of the most important structures. However, measuring its size by CT is difficult. The ostium is approximately 2.4–4 mm in diameter and is located superiorly on the medial wall of the maxillary sinus cavity.12,18 The bone window is much larger, but the effective ostium is reduced by the uncinate process, an extension of the inferior turbinate, and the surrounding soft tissues.18 Determining the exact diameter of the ostium, including the surrounding soft tissues (sinus mucosa) by coronal CT is difficult; thus, we attempted to measure the aperture width of the OMC in this study. The hypertrophic mucosa in the maxillary sinus could obstruct the maxillary ostium,

and the narrow aperture width of the OMC might be the cause of intractable maxillary sinusitis. The present study demonstrated that the aperture width of the OMC was significantly different in the effective and non-effective initial treatment groups. This difference in the aperture width might have been caused by the nasal space and presence of Haller’s cells. Although the presence of Haller’s cells might be one of the most important factors associated with the pathogenesis of chronic inflammation in maxillary sinusitis,14,19 the presence of Haller’s cells and the width of the upper OMC were not significant factors in this study. The reasons for this difference may be the following: In OMS patients, the oedema and thickening of the sinus mucosa caused by odontogenic inflammation may obstruct the OMC and drainage, while in non-odontogenic maxillary sinusitis patients, the narrowness of the OMC itself by the presence of Haller’s cells, etc., may cause OMC obstruction. If the aperture width of the OMC is narrow, the ostium can be obstructed easily by the inflammation and subsequent thickening of the sinus mucosa, regardless of whether the causative tooth has been treated appropriately by root canal therapy or extraction. The narrow aperture width of the OMC was found to be a significant factor in chronic maxillary sinus inflammation and could not be improved by the initial treatment for OMS. In this study, we determined the cut-off point for the aperture width of OMC by ROC analysis to be 11.12 mm. Therefore, for patients in whom the aperture width is less than 11.12 mm on pretreatment coronal CT imaging, a favourable outcome with only the initial treatment would not be assured. In addition, we could advise the patient of the necessity of additional surgical treatment such as a Caldwell–Luc operation or FESS before initial treatments. Consequently, a shortening of the total treatment period might be possible. To preserve physiological nasal cavity function, the combination of an intraoral approach (extraction or apicoectomy of the causative tooth) and FESS might be effective, as reported previously.20 Cone beam CT scanning has been used in recent years and has been shown to be significantly more sensitive in detecting the expansion of peri-apical lesions into the maxillary sinus than two-dimensional CT.21,22 Imaging the OMC by cone beam CT is useful to evaluate the structure of the OMC and measure the aperture width of the OMC easily and precisely. The aperture width of the OMC may be a significant predictor of the effectiveness

Please cite this article in press as: Tomomatsu N, et al. Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis, Int J Oral Maxillofac Surg (2014), http://dx.doi.org/10.1016/j.ijom.2014.06.007

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Odontogenic maxillary sinusitis of initial treatment for OMS (antibiotic medicine and/or treatment of the causative tooth). Therefore, preoperative evaluation of the aperture width of the OMC may be useful when considering the treatment strategy for OMS. Funding

None. Competing interests

None declared. Ethical approval

This study was approved by the Research Ethics Committee of Tokyo Medical and Dental University (approval number: 830). Patient consent

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5. Mehra P, Murad H. Maxillary sinus disease of odontogenic origin. Otolaryngol Clin North Am 2004;37:347–64. 6. Kurabayashi T, Ida M, Yoshino N, Hosokawa A, Sasaki T, Ishii J, et al. Usefulness of CT images for diagnosis of odontogenic maxillary sinusitis. Oral Radiol 1995;11:71–80. 7. Kato M, Kaneda T, Kato M, Sakayanagi M, Yamashita Y, Fujita Y, et al. Assessment of the relationship between odontogenic maxillary sinusitis and findings in the osteomeatal unit on coronal CT images. Dent Radiol 2007;47:47–52. 8. Ikeda K, Hirano K, Oshima T, Shimomura A, Suzuki H, Sunose H, et al. Comparison of complications between endoscopic sinus surgery and Caldwell–Luc operation. Tohoku J Exp Med 1996;180:27–31. 9. Na¨rkio¨-Ma¨kela¨ M, Qvarnberg Y. Endoscopic sinus surgery or Caldwell–Luc operation in the treatment of chronic and recurrent maxillary sinusitis. Acta Otolaryngol Suppl 1997;529:177–80. 10. Costa M, Emanuelli E, Robiony M, Zerman N, Polini F, Politi M. Endoscopic surgical treatment of chronic maxillary sinusitis of dental origin. J Oral Maxillofac Surg 2007;65:223–8. 11. Huang YC, Chen WH. Caldwell–Luc operation without inferior meatal antrostomy: a retrospective study 50 cases. J Oral Maxillofac Surg 2011;70:2080–4. 12. Bell GW, Joshi BB, Macleod RI. Maxillary sinus disease: diagnosis and treatment. Br Dent J 2011;210:113–8. 13. Montani M, Larsen P, Hansen H, Tos M, Berner B, Orntoft S. Coronal CT of the paranasal sinuses before and after functional endoscopic sinus surgery. Eur Radiol 1996;6: 920–4. 14. Fadda GL, Rosso S, Aversa S, Petrelli A, Ondolo C, Succo G. Multiparametric statistical correlations between paranasal sinus anatomic variations and chronic rhinosinusitis. Acta Otorhinolaryngol Ital 2012;32:244–51. 15. Pruna X. Morpho-functional evaluation of osteomeatal complex in chronic sinusitis by coronal CT. Eur Radiol 2003;13:1461–8.

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16. Scadding GK, Durham SR, Mirakian R, Jones NS, Drake-Lee AB, Dixon TA, et al. BSACI guidelines for the management of rhinosinusitis and nasal polyposis. Clin Exp Allergy 2007;38:260–75. 17. Zweig MH, Campbell G. Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem 1993;39:561–77. 18. Anon JB, Rontal M, Zinreich SJ. Anatomy of the paranasal sinuses. New York: Thieme; 1996: 18–21. 19. Iwatsubo T, Matsune S, Miyanohara I, Nishizono H, Ushikai M, Kurano Y. Image diagnosis of chronic sinusitis – relevance of Haller’s cell. Jibirinsho 2000;93:923–7. 20. Chiapasco M, Felisati G, Zaniboni M, Pipolo C, Borloni R, Lozza P. The treatment of sinusitis following maxillary sinus grafting with the association of FESS and an intraoral approach. Clin Oral Implants Res 2013;24:623–9. 21. Cymerman JJ, Cymerman DH, O’Dwyer RS. Evaluation of odontogenic maxillary sinusitis using cone-beam computed tomography: three case reports. J Endod 2011;37:1465–9. 22. Nair UP, Nair MK. Maxillary sinusitis of odontogenic origin: cone-beam volumetric computerized tomography-aided diagnosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:e53–7.

Address: Narikazu Uzawa Department of Maxillofacial Surgery Graduate School Tokyo Medical and Dental University 1-5-45 Yushima Bunkyo-ku Tokyo 113-8549 Japan Tel: +81 3 5803 5499; Fax: +81 3 5803 5500 E-mail: [email protected]

Please cite this article in press as: Tomomatsu N, et al. Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis, Int J Oral Maxillofac Surg (2014), http://dx.doi.org/10.1016/j.ijom.2014.06.007

Aperture width of the osteomeatal complex as a predictor of successful treatment of odontogenic maxillary sinusitis.

Odontogenic maxillary sinusitis (OMS) is an inflammatory disease caused by the spread of dental inflammation into the sinus. The long-term administrat...
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