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Association between odontogenic infections and unilateral sinus opacification
G Model
ANL-1938; No. of Pages 6 Auris Nasus Larynx xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Association between odontogenic infections and unilateral sinus opacification Yuma Matsumoto, Tetsuya Ikeda, Hidenori Yokoi *, Naoyuki Kohno Department of Otorhinolaryngology, Oral Surgery, Kyorin University School of Medicine, Tokyo, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2014 Accepted 29 December 2014 Available online xxx
Objectives: Consideration of the causes of unilateral paranasal sinusitis, which frequently occurs in routine medical care and is often associated with odontogenic infection. Study Design: Retrospective data analysis. Methods: A review of the charts of all 190 patients treated for unilateral paranasal sinusitis at our department between 2005 and 2012 was carried out. All patients were diagnosed based on clinical signs, symptoms, and imaging findings, including computed tomography (CT), orthopantomography (OP), and other modalities. Patients were classified in three groups: patients with odontogenic infection involvement (Group A); patients without odontogenic infection involvement (Group B); and patients with inconclusive odontogenic infection involvement (Group C). Results: The most common cause of unilateral paranasal sinusitis was odontogenic infection, as seen in 138 cases (72.6%), followed by chronic inflammation in 43 cases (22.6%). Among patients diagnosed with odontogenic infection, one patient was also diagnosed with coexistent polyps and mycosis. Based on CT, OP, EPT, and oral examination, final distribution was 138 patients (72.6%) in Group A, 32 (16.8%) in Group B, and 20 (10.5%) in Group C. Conclusions: Odontogenic infection involvement was implicated in approximately 70% cases of unilateral paranasal sinusitis. Odontogenic maxillary sinusitis can be difficult to diagnose, and consideration of imaging performed under various conditions is recommended. In order to determine the most appropriate treatment for unilateral paranasal sinusitis, whether such treatment will be surgery, dental treatment, conservative therapy, or other treatments, collaboration between concerned doctors is essential. ß 2015 Published by Elsevier Ireland Ltd.
Keywords: Unilateral sinusitis Dental infection Image examination
1. Introduction Unilateral paranasal sinusitis is characterized by obvious primarily single-sided sinus lesions on imaging and chronic or recurrent symptoms of nasal congestion, buccal pain, and ipsilateral postnasal drip. This condition as well as odontogenic maxillary sinusitis, paranasal sinus mycosis, allergic fungal sinusitis, and nasal and sinonasal papilloma, etc. are commonly encountered in clinical practice. In particular, institutions often may face difficulty collaborating with a dentist to diagnose odontogenic sinusitis. As a result, treatment sometimes may become difficult, despite the reportedly high prevalence of 10–40% [1–3] of maxillary sinusitis. Potential causes of the condition include dental caries, periodontal disease, and dental trauma; though it is rare for the causative tooth
* Corresponding author at: Department of Otorhinolaryngology-Head and Neck Surgery, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo 181-8611, Japan. Tel.: +81 422 42 5968; fax: +81 422 42 5968. E-mail address: [email protected] (H. Yokoi).
to remain untreated, insufficient treatment is becoming more commonly reported as an etiology. Most dentists face difficulty evaluating odontogenic infection involvement in sinusitis. Our hospital includes an oral surgery department as the dentist, which enables daily collaboration; odontogenic maxillary sinusitis can be treated cooperatively by both dental and otorhinolaryngological specialist. In the current study, we have described our diagnostic and therapeutic protocols, emphasizing odontogenic maxillary sinusitis as one manifestation of unilateral paranasal sinusitis. In addition, we reviewed pertinent recent literature and included discussions on the findings from these literatures. 2. Patients and methods A total of 190 patients were examined at the Department of Oral Surgery and Otorhinolaryngology between 2005 and 2012 and diagnosed with unilateral paranasal sinusitis based on clinical signs, symptoms, and imaging findings, including computed tomography (CT), orthopantomography (OP), or other modalities.
http://dx.doi.org/10.1016/j.anl.2014.12.006 0385-8146/ß 2015 Published by Elsevier Ireland Ltd.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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ANL-1938; No. of Pages 6 Y. Matsumoto et al. / Auris Nasus Larynx xxx (2015) xxx–xxx
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In this study, unilateral paranasal sinusitis was defined as meeting both of the following conditions: (1) shadows on CT predominantly in the sinus on one side, and always including the maxillary sinus and (2) Lund–Mackey score [4] <2 in the contralateral sinus, with cystic disorders and tumors excluded. CT and OP were the primary diagnostic modalities, but electric pulp testing (EPT) and oral examination were also used in diagnosis. Imaging signs were classified as follows: (1) in cases of pericementitis, periodontal space enlargement; (2) in cases of periodontitis, evidence of bone resorption; (3) in cases of an apical cyst, periodontal space enlargement and the presence of a cystic lesion; (4) in cases of tooth fracture, visible root fracture; (5) in cases of caries, coronal radiolucency; and (6) in cases of osteomyelitis, evidence of maxillary necrosis with maxillary sinusitis secondary to bacterial infection (Fig. 1). EPT was used as an auxiliary tool to assess the pulp response; the device was pressed against the crown and the pulp reaction to an electrical stimulus was compared between abnormal and healthy teeth. Other conditions associated with oral hygiene, such as caries and gingivitis, were also evaluated. Patients diagnosed with unilateral maxillary sinusitis were categorized into three groups: patients with dental infection involvement (Group A); those without dental infection involvement (Group B); and those for whom dental infection involvement was inconclusive (Group C). The 23 patients in Group C underwent additional 1-mm slice CT after providing informed consent.
(range) ages were 47.6 years (9–85 years) in men and 48.9 years (4–93 years) in women. The age distribution peaked at 40–49 years in both men and women (Fig. 2). The left sinus was affected in 105 patients and the right in 85, but this difference was not statistically significant. 3.2. Pathologic classification The most common cause of unilateral paranasal sinusitis was odontogenic infection in 138 cases (72.6%), followed by chronic inflammation in 43 (22.6%), mycosis in 21 (11.1%), polyp in 15 (7.9%), and foreign body in 4 (2.1%) (Fig. 3). In patients diagnosed with odontogenic infection, the most common comorbidity was mycosis in 15 cases, followed by polyp in 13 and foreign body in 3 (Fig. 4). 3.3. Causative tooth in odontogenic maxillary sinusitis
3. Results
The first molar was the most frequent odontogenic infectious origin in 74 cases, followed by the second molar (66), second premolar (24), third molar (7), first premolar (5), canines (2), and the central incisor (1) (Fig. 5). Widespread unilateral maxillary necrosis was present in 2 patients. Multiple causative teeth were present in 36 patients. The most common combinations were the first and second molars (18), second premolar and first molar (6), second premolar and second molar (4), and the first and second premolars (2). A range of 2–5 causative teeth was implicated in these cases (Fig. 6).
3.1. Sex, age and laterality distributions
3.4. Imaging conditions and diagnostic findings
In total, 190 patients were evaluated, with a mean age of 47.6 years in the range 4–93 years. There were more men than women examined (109 versus 81 patients, respectively). The mean
Based on the initial imaging, EPT, and oral examination, 125 patients were categorized into Group A, 26 in Group B, and 39 in Group C. High-resolution CT was performed in the 23 Group C
Fig. 1. CT and OP in odontogenic maxillary sinusitis. (1) Periodontal disease: Expansion of the periodontal ligament space; (2) Periodontitis: Bone resorption of alveolar bone; (3) Periodontal cyst: Cystic; (4) Fractured tooth; (5) Dental caries: resorption image in the crown of tooth; (6) Maxillary osteomyelitis: osteonecrosis of the jaw and maxillary sinusitis.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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Fig. 2. Sex, age and laterality distributions. The incidence was highest in the fourth decade for both men and women.
patients, and 13 were further classified into Group A, 6 into Group B, and 4 into Group C. The final distribution was 138 patients (72.6%) in Group A, 32 (16.8%) in Group B, and 20 (10.5%) in Group C (Fig. 7).
3.5. Symptoms Chief complaints of Group A were facial pain, toothache and nasal pain (61: 44.2%), nasal discharge and postnasal drip (48: 34.8%), nasal obstruction (26: 18.8%), discomfort in the face and gums, and bad odor (20: 14.5%). However, in two cases (1.4%), no symptoms were observed and were identified by medical examination. Chief complaints of Group B were facial pain, toothache and nasal pain (11: 34.4%), nasal discharge and postnasal drip (14: 43.8%), nasal obstruction (6: 18.8%), discomfort in the face and gums, and bad odor (7: 21.9%). Chief complaints of Group C were facial pain, toothache and nasal pain (7: 35%), nasal discharge and postnasal drip (6: 30%), nasal obstruction (3: 15%), discomfort in the face and gums, and bad odor (1: 5%). 3.6. Bacterial culture from nasal secretion and pathological analysis Results from a bacterial culture performed in 28 cases out of 138 (20.3%) in Group A showed Staphylococcus group (27: 96.4%),
Fig. 3. Classification of unilateral sinusitis.
Fig. 4. Pathologic classification. This is a diagram showing the condition merged with odontogenic infection. Mycosis is the most observed; and there was a trend that then many polyps were observed.
Fig. 5. Causative tooth in odontogenic maxillary sinusitis. It is shown for the cause of tooth infections. Causative tooth is more in the order of first molar (1 M), second molar (2 M), and second premolars (2 PM).
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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Fig. 6. Multiple causative tooth in odontogenic maxillary sinusitis.
Fig. 7. Classification of unilateral sinusitis by definition. This is the classification process flow chart. Group A, B and C in the unilateral paranasal sinusitis were CT, OP, EPT and oral findings. Furthermore 20 cases of Group C were classified Group A, B and C distributed by 1-mm slice CT. Final number of each case: Group A, 138 cases; Group B, 32 cases and Group C, 20 cases.
coryneform (11: 39.3%), anaero bacteria group (4: 14.3%), Enterobacter (3: 10.7%), Streptococcus (2: 7.1%), Pseudomonas aeruginosa (2: 7.1%), Neisseria (2: 7.1%), Haemophilus influenzae (1: 3.6%), Porphyromonas (1: 3.6%) and Klebsiella (1: 3.6%). For 6 cases out of 32 (18.8%) in Group B showed: Staphylococcus group (7: 116.7%), Streptococcus (4: 66.7%), Neisseria (1: 16.7%), Haemophilus influenzae (1: 16.7%) and anaero bacteria group (1: 16.7%). For 6 cases out of 20 (30%) in Group C showed: Staphylococcus group (6: 100%), coryneform (1: 16.7%), Enterobacter (1: 16.7%), Streptococcus (1: 16.7%) and Mucor (1: 16.7%). Except for one case of Mucor 1 in Group C, all cases were negative for fungus in culture, and some cases were observed in the pathological tissue.
Pathological analysis was performed in 42 cases out of 138 (30.4%) in Group A and showed Aspergillus 14, and a difficulty to identify strain 1: 10.9%. 10 cases out of 32 (31.3%) in Group B showed: aspergillus 1: 3.1%. 8 cases out of 20 (40%) in Group C showed: aspergillus 4, aspergillus +Mucor 1: 25%. 4. Discussion Previous studies linked odontogenic maxillary sinusitis to 10–40% of all maxillary sinusitis cases [1–3], but this is the first known report describing the role of odontogenic maxillary sinusitis in unilateral paranasal sinusitis. Our results suggest that
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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odontogenic infection is involved in 72.6% of unilateral paranasal sinusitis cases, an extremely high proportion compared to maxillary sinusitis involvement. This observation may reflect the proactive therapeutic coordination between the otorhinolaryngology and oral surgery (as dentists) departments. According to Mehra and Murad [3], odontogenic maxillary sinusitis is more common in women, but in our study, men were more frequently affected. Our findings were consistent with those of Kaneko et al. [5], who observed a higher incidence in patients aged 40–49 years. Potentially, the higher incidence among men and people aged 40–49 years may result from lifestyle time constraints limiting proactive oral care or dental examinations, as well as disturbances in the oral environment. Clinical symptoms of each group were considered, and facial pain, toothache and nasal pain were the most common in all groups, and no odontogenic characteristics were observed. Several patients suffered from polyps or mycosis in addition to odontogenic infection, suggesting that multiple causes should be considered during therapeutic planning. There are few studies reporting an association between odontogenic infection and mycosis, a particularly interesting finding. In this study, 15/21 (71.4%) patients were diagnosed with both paranasal sinus mycosis and odontogenic infection. Odontogenic infection is associated with both anaerobic and aerobic bacteria [6], with anaerobic bacteria implicated in 90% of apical abscesses [7]. Anaerobic bacteria are reported in approximately 50% of microbial cultures from patients with paranasal sinus mycosis [8]. Odontogenic maxillary sinusitis and paranasal sinus mycosis cause unilateral paranasal sinus inflammation. Over 70% of patients in this study suffered from both, suggesting both anaerobic bacterial and fungal growth. In odontogenic infection, the bacterial flora, including anaerobic bacteria, increase and cause maxillary sinusitis. This chronic inflammation causes the closure of the osteo-meatal complex (OMC) and creates a hypoxic environment in the maxillary sinus. Mucosal swelling and purulent accumulations in the maxillary sinus also contribute to the anaerobic environment. Most fungi can use metabolic pathways substituting nitrates or nitrites in place of oxygen under anaerobic conditions [9]; in addition, the organic calcium and iron salts present in dental treatment materials promote fungal proliferation [10]. The maxillary sinuses may therefore provide a favorable environment for fungal proliferation, enhancing their pathogenicity. Although nasal culture sampling was not carried out in any of the cases we considered, the Staphylococcus group was high in each group. Although four cases of anaerobic bacteria were observed in Group A, anaerobic bacterial cultures were not obtained from all patients. Culture samples were obtained as the paranasal sinuses were opened, and this air contact may have hindered anaerobic culture; this limitation warrants further investigation. In nasal culture samples for fungus, a lower positive rate was obtained and a histological search was needed. As a result, groups with actual or suspected odontogenic infection showed a higher positive rate. According to Oscar Arias-Irimia et al. [11], the first molar is the most frequent source of odontogenic infection, followed by the third and second molars, whereas Ugincius [12] and Lin et al. [13] report the second molar, first molar, and second premolar as the most frequent sites of origin. In this study, the first molar was the most common source, followed by the second molar and the second premolar, and multiple causative teeth were present in some cases, requiring particular care in diagnosis. According to OP and CT results and in agreement with previous reports, a common reason why molars are often the cause is related
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to their relative anatomic position to the maxillary floor. In 2 patients, maxillary sinusitis was not associated with a specific tooth but instead with bisphosphonate-related necrosis of the jaw (BRONJ). Paranasal sinusitis reportedly occurs in approximately 50% of patients with BRONJ [14]; therefore, obtaining a detailed pharmaceutical history is also essential. Recent studies report that high-resolution CT and cone-beam CT (CBCT) are useful in diagnosing odontogenic infection [15]. We have also found that electric pulp testing combined with highresolution CT and OP is quite useful for dental diagnosis. Caution is required during image evaluation depending on the imaging conditions. Normal paranasal sinus CT images are usually scanned at a 4 mm thickness and include coronal sections in at least one orientation. On CT images scanned in single-orientation coronal sections at 4–5 mm thickness, lesions encompassing a wide area may be imaged incidentally while apical lesions are often unclear. However, if the same patient is scanned in multiple orientations at 1-mm thickness, alveolar bone resorption and other lesions are more easily visualized. Thus, by changing the patient imaging parameters, lesions may be easily detected. In this study, we reduced the slice thickness, which may have significantly reduced artifacts associated with dental materials and improved apical lesion detection. Although sagittal and coronal sections are useful for diagnosing odontogenic infection [16], sagittal sections were only available for 7 patients, and therefore their utility could not be clearly established. Nevertheless, the high incidence of concurrent odontogenic infection far greater than previously reported may result from our diagnostic protocol, such as the use of OP and thinslice CT in at least 2 orientations. The examination method in this study was useful in 19 patients (10.0%). A negative pulp reaction on EPT, used as an auxiliary diagnosis, indicates either complete pulp necrosis or previous root canal treatment, while a positive reaction indicates a healthy tooth or incomplete pulp necrosis. These results are useful when assessing the pulp condition, which is difficult to determine on diagnostic imaging. EPT uses an electrical stimulus to stimulate myelinated nerves [17,18], and the patient senses the electrical stimulus when it reaches the pain threshold. This threshold is affected by numerous factors including age, pain perception, and tooth surface conduction [18]. EPT reliability is low in healthy immature teeth [17]. Even in mature teeth, patients with strong calcification may exhibit a poor reaction [19], and orthodontic treatment, other dental treatments, residual pulpitis, and persistent pulp necrosis may cause false reactions [17]. Thus, diagnosis cannot be made based on EPT alone, and a comprehensive evaluation including imaging is required. Despite the detailed diagnostic protocol in this study, an association to odontogenic infection could not be determined in 20 patients (10.5%), and further diagnostic measures were required. On the question of collaboration with dentists, previous studies have found that 86% of patients with suspected odontogenic paranasal sinusitis were judged not to have any dental disease during examination [20]. Collaboration with dentists can be inadequate, and dentists are not usually involved in paranasal sinusitis treatment. In some patients, it was impossible to determine odontogenic involvement even when evaluated by both an otorhinolaryngologist and a dentist, and thus, careful follow-up is required after treatment. Finally, one issue warranting further investigation is the unilateral paranasal sinusitis therapy. Currently, there are no clear treatment criteria, but patients in Group A underwent dental treatment and those who did not improve subsequently received medical or surgical treatment. Patients in Groups B and C underwent medical treatment or surgery initially, and additional dental treatment was considered if they did not improve.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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5. Conclusions [6]
We found that odontogenic infection was implicated in approximately 70% of unilateral paranasal sinusitis cases. Odontogenic maxillary sinusitis can be difficult to diagnose, and imaging performed under a variety of conditions must be investigated. Our results also suggest that diagnosis based on imaging alone may be problematic and additional procedures such as pulp testing may be required. Further investigation of the appropriate treatment for unilateral paranasal sinusitis, whether surgery, dental treatment, conservative therapy, or other treatments, is necessary, and collaboration with dentists is therefore essential.
[12]
Conflict of interest
[13]
None of the authors have a funding, financial relationship, or conflict of interest which should be disclosed.
[7] [8] [9] [10] [11]
[14]
[15]
References [1] Brook I. Sinusitis of odontogenic origin. Otolaryngol Head Neck Surg 2006;135:349–55. [2] Melen I, Lindahl L, Andreasson L, Rundcrantz H. Chronic maxillary sinusitis. Definition, diagnosis and relation to dental infections and nasal polyposis. Acta Otolaryngol 1986;101:320–7. [3] Mehra P, Murad H. Maxillary sinus disease of odontogenic origin. Otolaryngol Clin North Am 2004;37:347–64. [4] Lund VJ, Mackay IS. Staging in rhinosinusitis. Rhinology 1993;31:183–4. [5] Kaneko I, Harada K, Ishii T, Furukawa K, Yao K, Takahashi H, et al. Clinical feature of odontogenic maxillary sinusitis – symptomatology and the grade in
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development of the maxillary sinus in cases of dental maxillary sinusitis. Nihon Jibiinkoka Gakkai Kaiho 1990;93:1034–40. Brook I. Microbiology and management of endodontic infections in children. J Clin Pediatr Dent 2003;28:13–7. Brook I. Microbiology of acute and chronic maxillary sinusitis associated with an odontogenic origin. Laryngoscope 2005;115:823–5. Brook I. Recovery of aerobic and anaerobic bacteria in sinus fungal ball. Otolaryngol Head Neck Surg 2011;145:851–2. Shoun H, Kim DH, Uchiyama H, Sugiyama J. Denitrification by fungi. FEMS Microbiol Lett 1992;94:277–82. Stammberger H, Jakse R. Mykotische Erkrankungen im HNO–Bereich. HNO 1987;35:139–76. Oscar AI, Cristina BD, Juan AS, Natalia MR, Jose´ MM. Meta-analisis of the etiology of odontogenic maxillary sinusitis. Med Oral Patol Oral Cir Bucal 2010;15:70–3. Ugincius P, Kubilius R, Gervickas A, Vaitkus S. Chronic odontogenic maxillary sinusitis. Stomatologija 2006;8:44–8. Lin PT, Bukachevsky R, Blake M. Management of odontongenic sinusitis with persistent oro-antral fistula. Ear Nose Throat J 1991;70:488–90. Maurer P, Sandulescu T, Kriwalsky MS, Rashad A, Hollstein S, Stricker I, et al. Bisphosphonate-related osteonecrosis of the maxilla and sinusitis maxillaris. Int J Oral Maxillofac Surg 2011;40:285–91. Patel NA, Ferguson BJ. Odontogenic sinusitis: an ancient but under-appreciated cause of maxillary sinusitis. Curr Opin Otolaryngol Head Neck Surg 2012;20: 24–8. Abrahams JJ, Glassberg RM. Dental disease: a frequently unrecognized cause of maxillary sinus abnormalities. AJR Am J Roentgenol 1996;166: 1219–23. Bender IB. Reversible and irreversible painful pulpitides: diagnosis and treatment. Aust Endod J 2000;26:10–4. Mumford JM. Thermal and electrical stimulation of teeth in the diagnosis of pulpal and periapical disease. Proc R Soc Med 1967;60:197–200. Bender IB. Pulpal pain diagnosis – a review. J Endod 2000;26:175–9. Longhini AB, Ferguson BJ. Clinical aspect of the disease burden of sinusitis: a case series. Int Forum Allergy Rhinol 2011;1:409–15.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
ANL-1938; No. of Pages 6 Auris Nasus Larynx xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Association between odontogenic infections and unilateral sinus opacification Yuma Matsumoto, Tetsuya Ikeda, Hidenori Yokoi *, Naoyuki Kohno Department of Otorhinolaryngology, Oral Surgery, Kyorin University School of Medicine, Tokyo, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 June 2014 Accepted 29 December 2014 Available online xxx
Objectives: Consideration of the causes of unilateral paranasal sinusitis, which frequently occurs in routine medical care and is often associated with odontogenic infection. Study Design: Retrospective data analysis. Methods: A review of the charts of all 190 patients treated for unilateral paranasal sinusitis at our department between 2005 and 2012 was carried out. All patients were diagnosed based on clinical signs, symptoms, and imaging findings, including computed tomography (CT), orthopantomography (OP), and other modalities. Patients were classified in three groups: patients with odontogenic infection involvement (Group A); patients without odontogenic infection involvement (Group B); and patients with inconclusive odontogenic infection involvement (Group C). Results: The most common cause of unilateral paranasal sinusitis was odontogenic infection, as seen in 138 cases (72.6%), followed by chronic inflammation in 43 cases (22.6%). Among patients diagnosed with odontogenic infection, one patient was also diagnosed with coexistent polyps and mycosis. Based on CT, OP, EPT, and oral examination, final distribution was 138 patients (72.6%) in Group A, 32 (16.8%) in Group B, and 20 (10.5%) in Group C. Conclusions: Odontogenic infection involvement was implicated in approximately 70% cases of unilateral paranasal sinusitis. Odontogenic maxillary sinusitis can be difficult to diagnose, and consideration of imaging performed under various conditions is recommended. In order to determine the most appropriate treatment for unilateral paranasal sinusitis, whether such treatment will be surgery, dental treatment, conservative therapy, or other treatments, collaboration between concerned doctors is essential. ß 2015 Published by Elsevier Ireland Ltd.
Keywords: Unilateral sinusitis Dental infection Image examination
1. Introduction Unilateral paranasal sinusitis is characterized by obvious primarily single-sided sinus lesions on imaging and chronic or recurrent symptoms of nasal congestion, buccal pain, and ipsilateral postnasal drip. This condition as well as odontogenic maxillary sinusitis, paranasal sinus mycosis, allergic fungal sinusitis, and nasal and sinonasal papilloma, etc. are commonly encountered in clinical practice. In particular, institutions often may face difficulty collaborating with a dentist to diagnose odontogenic sinusitis. As a result, treatment sometimes may become difficult, despite the reportedly high prevalence of 10–40% [1–3] of maxillary sinusitis. Potential causes of the condition include dental caries, periodontal disease, and dental trauma; though it is rare for the causative tooth
* Corresponding author at: Department of Otorhinolaryngology-Head and Neck Surgery, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo 181-8611, Japan. Tel.: +81 422 42 5968; fax: +81 422 42 5968. E-mail address: [email protected] (H. Yokoi).
to remain untreated, insufficient treatment is becoming more commonly reported as an etiology. Most dentists face difficulty evaluating odontogenic infection involvement in sinusitis. Our hospital includes an oral surgery department as the dentist, which enables daily collaboration; odontogenic maxillary sinusitis can be treated cooperatively by both dental and otorhinolaryngological specialist. In the current study, we have described our diagnostic and therapeutic protocols, emphasizing odontogenic maxillary sinusitis as one manifestation of unilateral paranasal sinusitis. In addition, we reviewed pertinent recent literature and included discussions on the findings from these literatures. 2. Patients and methods A total of 190 patients were examined at the Department of Oral Surgery and Otorhinolaryngology between 2005 and 2012 and diagnosed with unilateral paranasal sinusitis based on clinical signs, symptoms, and imaging findings, including computed tomography (CT), orthopantomography (OP), or other modalities.
http://dx.doi.org/10.1016/j.anl.2014.12.006 0385-8146/ß 2015 Published by Elsevier Ireland Ltd.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
G Model
ANL-1938; No. of Pages 6 Y. Matsumoto et al. / Auris Nasus Larynx xxx (2015) xxx–xxx
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In this study, unilateral paranasal sinusitis was defined as meeting both of the following conditions: (1) shadows on CT predominantly in the sinus on one side, and always including the maxillary sinus and (2) Lund–Mackey score [4] <2 in the contralateral sinus, with cystic disorders and tumors excluded. CT and OP were the primary diagnostic modalities, but electric pulp testing (EPT) and oral examination were also used in diagnosis. Imaging signs were classified as follows: (1) in cases of pericementitis, periodontal space enlargement; (2) in cases of periodontitis, evidence of bone resorption; (3) in cases of an apical cyst, periodontal space enlargement and the presence of a cystic lesion; (4) in cases of tooth fracture, visible root fracture; (5) in cases of caries, coronal radiolucency; and (6) in cases of osteomyelitis, evidence of maxillary necrosis with maxillary sinusitis secondary to bacterial infection (Fig. 1). EPT was used as an auxiliary tool to assess the pulp response; the device was pressed against the crown and the pulp reaction to an electrical stimulus was compared between abnormal and healthy teeth. Other conditions associated with oral hygiene, such as caries and gingivitis, were also evaluated. Patients diagnosed with unilateral maxillary sinusitis were categorized into three groups: patients with dental infection involvement (Group A); those without dental infection involvement (Group B); and those for whom dental infection involvement was inconclusive (Group C). The 23 patients in Group C underwent additional 1-mm slice CT after providing informed consent.
(range) ages were 47.6 years (9–85 years) in men and 48.9 years (4–93 years) in women. The age distribution peaked at 40–49 years in both men and women (Fig. 2). The left sinus was affected in 105 patients and the right in 85, but this difference was not statistically significant. 3.2. Pathologic classification The most common cause of unilateral paranasal sinusitis was odontogenic infection in 138 cases (72.6%), followed by chronic inflammation in 43 (22.6%), mycosis in 21 (11.1%), polyp in 15 (7.9%), and foreign body in 4 (2.1%) (Fig. 3). In patients diagnosed with odontogenic infection, the most common comorbidity was mycosis in 15 cases, followed by polyp in 13 and foreign body in 3 (Fig. 4). 3.3. Causative tooth in odontogenic maxillary sinusitis
3. Results
The first molar was the most frequent odontogenic infectious origin in 74 cases, followed by the second molar (66), second premolar (24), third molar (7), first premolar (5), canines (2), and the central incisor (1) (Fig. 5). Widespread unilateral maxillary necrosis was present in 2 patients. Multiple causative teeth were present in 36 patients. The most common combinations were the first and second molars (18), second premolar and first molar (6), second premolar and second molar (4), and the first and second premolars (2). A range of 2–5 causative teeth was implicated in these cases (Fig. 6).
3.1. Sex, age and laterality distributions
3.4. Imaging conditions and diagnostic findings
In total, 190 patients were evaluated, with a mean age of 47.6 years in the range 4–93 years. There were more men than women examined (109 versus 81 patients, respectively). The mean
Based on the initial imaging, EPT, and oral examination, 125 patients were categorized into Group A, 26 in Group B, and 39 in Group C. High-resolution CT was performed in the 23 Group C
Fig. 1. CT and OP in odontogenic maxillary sinusitis. (1) Periodontal disease: Expansion of the periodontal ligament space; (2) Periodontitis: Bone resorption of alveolar bone; (3) Periodontal cyst: Cystic; (4) Fractured tooth; (5) Dental caries: resorption image in the crown of tooth; (6) Maxillary osteomyelitis: osteonecrosis of the jaw and maxillary sinusitis.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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Fig. 2. Sex, age and laterality distributions. The incidence was highest in the fourth decade for both men and women.
patients, and 13 were further classified into Group A, 6 into Group B, and 4 into Group C. The final distribution was 138 patients (72.6%) in Group A, 32 (16.8%) in Group B, and 20 (10.5%) in Group C (Fig. 7).
3.5. Symptoms Chief complaints of Group A were facial pain, toothache and nasal pain (61: 44.2%), nasal discharge and postnasal drip (48: 34.8%), nasal obstruction (26: 18.8%), discomfort in the face and gums, and bad odor (20: 14.5%). However, in two cases (1.4%), no symptoms were observed and were identified by medical examination. Chief complaints of Group B were facial pain, toothache and nasal pain (11: 34.4%), nasal discharge and postnasal drip (14: 43.8%), nasal obstruction (6: 18.8%), discomfort in the face and gums, and bad odor (7: 21.9%). Chief complaints of Group C were facial pain, toothache and nasal pain (7: 35%), nasal discharge and postnasal drip (6: 30%), nasal obstruction (3: 15%), discomfort in the face and gums, and bad odor (1: 5%). 3.6. Bacterial culture from nasal secretion and pathological analysis Results from a bacterial culture performed in 28 cases out of 138 (20.3%) in Group A showed Staphylococcus group (27: 96.4%),
Fig. 3. Classification of unilateral sinusitis.
Fig. 4. Pathologic classification. This is a diagram showing the condition merged with odontogenic infection. Mycosis is the most observed; and there was a trend that then many polyps were observed.
Fig. 5. Causative tooth in odontogenic maxillary sinusitis. It is shown for the cause of tooth infections. Causative tooth is more in the order of first molar (1 M), second molar (2 M), and second premolars (2 PM).
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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Fig. 6. Multiple causative tooth in odontogenic maxillary sinusitis.
Fig. 7. Classification of unilateral sinusitis by definition. This is the classification process flow chart. Group A, B and C in the unilateral paranasal sinusitis were CT, OP, EPT and oral findings. Furthermore 20 cases of Group C were classified Group A, B and C distributed by 1-mm slice CT. Final number of each case: Group A, 138 cases; Group B, 32 cases and Group C, 20 cases.
coryneform (11: 39.3%), anaero bacteria group (4: 14.3%), Enterobacter (3: 10.7%), Streptococcus (2: 7.1%), Pseudomonas aeruginosa (2: 7.1%), Neisseria (2: 7.1%), Haemophilus influenzae (1: 3.6%), Porphyromonas (1: 3.6%) and Klebsiella (1: 3.6%). For 6 cases out of 32 (18.8%) in Group B showed: Staphylococcus group (7: 116.7%), Streptococcus (4: 66.7%), Neisseria (1: 16.7%), Haemophilus influenzae (1: 16.7%) and anaero bacteria group (1: 16.7%). For 6 cases out of 20 (30%) in Group C showed: Staphylococcus group (6: 100%), coryneform (1: 16.7%), Enterobacter (1: 16.7%), Streptococcus (1: 16.7%) and Mucor (1: 16.7%). Except for one case of Mucor 1 in Group C, all cases were negative for fungus in culture, and some cases were observed in the pathological tissue.
Pathological analysis was performed in 42 cases out of 138 (30.4%) in Group A and showed Aspergillus 14, and a difficulty to identify strain 1: 10.9%. 10 cases out of 32 (31.3%) in Group B showed: aspergillus 1: 3.1%. 8 cases out of 20 (40%) in Group C showed: aspergillus 4, aspergillus +Mucor 1: 25%. 4. Discussion Previous studies linked odontogenic maxillary sinusitis to 10–40% of all maxillary sinusitis cases [1–3], but this is the first known report describing the role of odontogenic maxillary sinusitis in unilateral paranasal sinusitis. Our results suggest that
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odontogenic infection is involved in 72.6% of unilateral paranasal sinusitis cases, an extremely high proportion compared to maxillary sinusitis involvement. This observation may reflect the proactive therapeutic coordination between the otorhinolaryngology and oral surgery (as dentists) departments. According to Mehra and Murad [3], odontogenic maxillary sinusitis is more common in women, but in our study, men were more frequently affected. Our findings were consistent with those of Kaneko et al. [5], who observed a higher incidence in patients aged 40–49 years. Potentially, the higher incidence among men and people aged 40–49 years may result from lifestyle time constraints limiting proactive oral care or dental examinations, as well as disturbances in the oral environment. Clinical symptoms of each group were considered, and facial pain, toothache and nasal pain were the most common in all groups, and no odontogenic characteristics were observed. Several patients suffered from polyps or mycosis in addition to odontogenic infection, suggesting that multiple causes should be considered during therapeutic planning. There are few studies reporting an association between odontogenic infection and mycosis, a particularly interesting finding. In this study, 15/21 (71.4%) patients were diagnosed with both paranasal sinus mycosis and odontogenic infection. Odontogenic infection is associated with both anaerobic and aerobic bacteria [6], with anaerobic bacteria implicated in 90% of apical abscesses [7]. Anaerobic bacteria are reported in approximately 50% of microbial cultures from patients with paranasal sinus mycosis [8]. Odontogenic maxillary sinusitis and paranasal sinus mycosis cause unilateral paranasal sinus inflammation. Over 70% of patients in this study suffered from both, suggesting both anaerobic bacterial and fungal growth. In odontogenic infection, the bacterial flora, including anaerobic bacteria, increase and cause maxillary sinusitis. This chronic inflammation causes the closure of the osteo-meatal complex (OMC) and creates a hypoxic environment in the maxillary sinus. Mucosal swelling and purulent accumulations in the maxillary sinus also contribute to the anaerobic environment. Most fungi can use metabolic pathways substituting nitrates or nitrites in place of oxygen under anaerobic conditions [9]; in addition, the organic calcium and iron salts present in dental treatment materials promote fungal proliferation [10]. The maxillary sinuses may therefore provide a favorable environment for fungal proliferation, enhancing their pathogenicity. Although nasal culture sampling was not carried out in any of the cases we considered, the Staphylococcus group was high in each group. Although four cases of anaerobic bacteria were observed in Group A, anaerobic bacterial cultures were not obtained from all patients. Culture samples were obtained as the paranasal sinuses were opened, and this air contact may have hindered anaerobic culture; this limitation warrants further investigation. In nasal culture samples for fungus, a lower positive rate was obtained and a histological search was needed. As a result, groups with actual or suspected odontogenic infection showed a higher positive rate. According to Oscar Arias-Irimia et al. [11], the first molar is the most frequent source of odontogenic infection, followed by the third and second molars, whereas Ugincius [12] and Lin et al. [13] report the second molar, first molar, and second premolar as the most frequent sites of origin. In this study, the first molar was the most common source, followed by the second molar and the second premolar, and multiple causative teeth were present in some cases, requiring particular care in diagnosis. According to OP and CT results and in agreement with previous reports, a common reason why molars are often the cause is related
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to their relative anatomic position to the maxillary floor. In 2 patients, maxillary sinusitis was not associated with a specific tooth but instead with bisphosphonate-related necrosis of the jaw (BRONJ). Paranasal sinusitis reportedly occurs in approximately 50% of patients with BRONJ [14]; therefore, obtaining a detailed pharmaceutical history is also essential. Recent studies report that high-resolution CT and cone-beam CT (CBCT) are useful in diagnosing odontogenic infection [15]. We have also found that electric pulp testing combined with highresolution CT and OP is quite useful for dental diagnosis. Caution is required during image evaluation depending on the imaging conditions. Normal paranasal sinus CT images are usually scanned at a 4 mm thickness and include coronal sections in at least one orientation. On CT images scanned in single-orientation coronal sections at 4–5 mm thickness, lesions encompassing a wide area may be imaged incidentally while apical lesions are often unclear. However, if the same patient is scanned in multiple orientations at 1-mm thickness, alveolar bone resorption and other lesions are more easily visualized. Thus, by changing the patient imaging parameters, lesions may be easily detected. In this study, we reduced the slice thickness, which may have significantly reduced artifacts associated with dental materials and improved apical lesion detection. Although sagittal and coronal sections are useful for diagnosing odontogenic infection [16], sagittal sections were only available for 7 patients, and therefore their utility could not be clearly established. Nevertheless, the high incidence of concurrent odontogenic infection far greater than previously reported may result from our diagnostic protocol, such as the use of OP and thinslice CT in at least 2 orientations. The examination method in this study was useful in 19 patients (10.0%). A negative pulp reaction on EPT, used as an auxiliary diagnosis, indicates either complete pulp necrosis or previous root canal treatment, while a positive reaction indicates a healthy tooth or incomplete pulp necrosis. These results are useful when assessing the pulp condition, which is difficult to determine on diagnostic imaging. EPT uses an electrical stimulus to stimulate myelinated nerves [17,18], and the patient senses the electrical stimulus when it reaches the pain threshold. This threshold is affected by numerous factors including age, pain perception, and tooth surface conduction [18]. EPT reliability is low in healthy immature teeth [17]. Even in mature teeth, patients with strong calcification may exhibit a poor reaction [19], and orthodontic treatment, other dental treatments, residual pulpitis, and persistent pulp necrosis may cause false reactions [17]. Thus, diagnosis cannot be made based on EPT alone, and a comprehensive evaluation including imaging is required. Despite the detailed diagnostic protocol in this study, an association to odontogenic infection could not be determined in 20 patients (10.5%), and further diagnostic measures were required. On the question of collaboration with dentists, previous studies have found that 86% of patients with suspected odontogenic paranasal sinusitis were judged not to have any dental disease during examination [20]. Collaboration with dentists can be inadequate, and dentists are not usually involved in paranasal sinusitis treatment. In some patients, it was impossible to determine odontogenic involvement even when evaluated by both an otorhinolaryngologist and a dentist, and thus, careful follow-up is required after treatment. Finally, one issue warranting further investigation is the unilateral paranasal sinusitis therapy. Currently, there are no clear treatment criteria, but patients in Group A underwent dental treatment and those who did not improve subsequently received medical or surgical treatment. Patients in Groups B and C underwent medical treatment or surgery initially, and additional dental treatment was considered if they did not improve.
Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006
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5. Conclusions [6]
We found that odontogenic infection was implicated in approximately 70% of unilateral paranasal sinusitis cases. Odontogenic maxillary sinusitis can be difficult to diagnose, and imaging performed under a variety of conditions must be investigated. Our results also suggest that diagnosis based on imaging alone may be problematic and additional procedures such as pulp testing may be required. Further investigation of the appropriate treatment for unilateral paranasal sinusitis, whether surgery, dental treatment, conservative therapy, or other treatments, is necessary, and collaboration with dentists is therefore essential.
[12]
Conflict of interest
[13]
None of the authors have a funding, financial relationship, or conflict of interest which should be disclosed.
[7] [8] [9] [10] [11]
[14]
[15]
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Please cite this article in press as: Matsumoto Y, et al. Association between odontogenic infections and unilateral sinus opacification. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2014.12.006