ORIGINAL ARTICLE
Clinical aspects of odontogenic maxillary sinusitis: a case series Anthony B. Longhini, BS1 Berrylin J. Ferguson, MD2
Background: The incidence of odontogenic maxillary sinusitis (OMS) is unknown. Failure to address dental pathology causing sinusitis can lead to failure of medical and surgical treatments. The purpose of this article is to present an OMS patient series. Methods: Retrospective review of prospectively accrued patients. Sinusitis guidelines were reviewed for OMS incidence and management. The clinical aspects of OMS in 21 patients diagnosed by sinus computed tomography (CT) scan over the last 30 months were assessed.
of 21 (67%) of initial sinus CT reports but reevaluation of CT scans found dental pathology in all patients. Conclusion: Dental pathology causing sinusitis was frequently missed on plain dental X-rays and CT scan reports. Dental pain and foul-smelling nasal discharge are present in less than one-half of patients and symptoms commonly persist for years. Otolaryngologists must have a high index of suspicion for an odontogenic cause of refractory maxillary C 2011 ARS-AAOA, LLC. sinusitis.
Key Words: Results: In our series the mean age was 53 years (range, 21–70 years), mean duration of symptoms was 2.6 years (range, 1 month to 15 years), roen smell or bad taste was present in 10 of 21 (48%) patients, dental pain was present in 6 of 21 (29%) patients, and unilateral maxillary opacification was present in 12 of 23 (57%) patients. Dental pathology was not noted in 6 of 7 (86%) of pre-CT dental films and 14
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istorically 10% to 12% of maxillary sinusitis cases have been attributed to odontogenic infections,1 but this is only referenced anecdotally.2 A 2010 article from Romania by Albu and Baciut3 reported a 25% (104/411) incidence of odontogenic maxillary sinusitis (OMS) in patients undergoing endoscopic sinus surgery (ESS) for chronic rhinosinusitis (CRS) without nasal polyps (NP). The authors attributed their higher incidence of OMS to a shared outpatient office with oral-maxillofacial surgeons. Classically, OMS is considered in patients with upper tooth pain, dental infection, dental surgery, unilateral maxillary sinusitis, foul drainage or smell, and resistance to conventional sinusitis therapy.4–7
maxillary sinusitis; odontogenic infection; oroantral fistula; periapical abscess; sinusitis How to Cite this Article: Longhini AB, Ferguson BJ. Clinical aspects of odontogenic maxillary sinusitis: a case series. Int Forum Allergy Rhinol, 2011; 1:409–415
Melen6 reported on the inherent difficulty of diagnosing OMS because “the dental infection may progress slowly and produce only minor symptoms until an exacerbation occurs, and the dental foci can therefore easily be overlooked.” Recognition of OMS is important because failure to address the dental pathology can result in failure of medical and surgical therapies and persistence of symptoms.8,9 We reviewed the English-language medical literature and CRS guidelines with attention to recognition and recommendations for OMS. Prospectively, we enrolled all patients in a 30-month period with OMS based on computed tomography (CT) scan and report on their clinical and demographic findings.
Materials and methods
1
School of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA; 2 Department of Otolaryngology, University of Pittsburgh School of Medicine, Pittsburgh, PA Correspondence to: Anthony Longhini, UPMC Mercy Building D, Suite 2100, 1400 Locust Street, Pittsburgh, PA 15219; e-mail:
[email protected] Potential conflict of interest: B.J.F. is a consultant for MEDA and Schering Plough and performs research for Inverness and Genentech. Received: 13 October 2010; Revised: 18 January 2011; Accepted: 8 February 2011 DOI: 10.1002/alr.20058 View this article online at wileyonlinelibrary.com.
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We conducted 2 literature searches, 1 PubMed search was conducted for the terms “odontogenic sinusitis OR odontogenic rhinosinusitis OR odontogenic maxillary sinusitis.” The search was limited to articles with full text available in English published between November 1988 and June 2010. We pursued the primary source material referenced in these articles regarding cited incidence rates. A second PubMed search reviewed rhinosinusitis guidelines to determine how frequently an odontogenic etiology
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TABLE 1. Sinonasogram scale 1 = No problems
No symptoms evident
2 = Mild
Symptoms clearly present but minimal awareness: easily tolerated
3 = Moderate
Definite awareness of symptom that is bothersome but tolerable
4 = Severe
Symptom is hard to tolerate: interferes with activities of daily living and/or sleeping
is listed using a PubMed search for the terms “guideline AND (sinusitis [MeSH Terms]).” The search was limited to articles with full text available in English published between March 1998 and June 2010. We did not evaluate pediatric articles. The full text of each guideline was searched for the terms “dental” and “odontogenic.” We retrospectively reviewed patients with symptoms of CRS and maxillary dental abnormalities on CT scan who were prospectively accrued by the senior author from January 2008 to June 2010. CT evidence of dental pathology and sinusitis was identified by the initial radiographic report or by secondary report by a head and neck radiologist after initial identification by the senior author. The study was reviewed by the Institutional Review Board of the University of Pittsburgh and approved under the exempt heading as a retrospective review of existing medical records. All patients completed a sinonasogram at each visit that assessed their symptoms on the day of the visit and over the previous 4 weeks. The survey included 13 symptoms and 1 global sinonasal assessment using a 4-point scale (Table 1).
Results From January 2008 to June 2010, 21 patients with OMS were identified. In our series 11 patients were female and 10 were male with a mean age of 53 years (range, 21–70 years) and an average duration of symptoms of 2.6 years (range, 1 month to 15 years). Three patients had diabetes mellitus and 1 was insulin dependent. Four patients had a history of environmental allergies. None of the patients in the series had NP. Symptom scores reported on the sinonasogram were not significantly different between the 2 temporal periods, although most patients reported less severe symptoms on the day of the exam than over the preceding 4 weeks. (Fig. 1) A total of 29% (6/21) of patients reported dental pain and 48% (10/21) reported rotten smell or bad taste. A total of 61% (11/18) of the patients reported a history of temporary symptomatic improvement with antibiotic therapy. Antibiotic therapy was not attempted for 3 patients. A total of 62% (13/21) of patients reported visiting a dentist during their disease course before our recognition of OMS. Seven of these 13 patients had dental X-rays,
FIGURE 1. Mean sinonasogram scores for all patients. Symptoms were assessed on a 4-point scale on the day of the visit and for 4 weeks preceding visit. No significant difference was found between the 2 temporal periods. Error bars = standard deviation.
which showed abnormalities in only 1 patient, specifically a case of dental caries, visible on digital but not plain dental X-ray. Thus 86% of patients had dental X-rays that failed to diagnose OMS. Nineteen patients had dental procedures after recognition of OMS. Two patients had ESS concomitant with dental treatment; 1 extraction and 1 extraction with repair of oroantral fistula. One patient, whose symptoms did not resolve with dental therapy alone, required additional ESS, which did lead to resolution of symptoms (Table 2). Without correction of the dental pathology, ESS was unsuccessful in our series. Six patients (29%) received 15 sinus surgeries prior to recognition of OMS. OMS was refractory to ESS in all cases except 2 in which the patient underwent a simultaneous ESS and dental extraction after the recognition of OMS. Fifteen patients had an endoscopic bacterial culture (Table 3). There were 26 isolates with an average of 1.7 bacterial species per patient. Polymicrobial cultures were obtained from 8 patients. Sinus pathogens were rarely TABLE 2. Dental history n (%)
Dental assessment before sinus CT diagnosis of OMS Dental visit
13/21 (62)
Dental X-rays with dental exam
7/13 (54)
Abnormality on dental X-ray
1/7 (14)
Dental assessment after sinus CT diagnosis of OMS Dental procedures
19/21 (90)
Dental extraction
15/19 (79)
Endodontic therapy Resolution of sinusitis symptoms
6/19 (32) 18/19 (95)
CT = computed tomography; OMS = odontogenic maxillary sinusitis.
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TABLE 3. Microbiology Organism
Number of isolates
Alpha hemolytic Streptococcus
4
Group A Streptococcus
1
Beta hemolytic Streptococcus
1
Streptococcus intermedius
1
Streptococcus morbillorum
1
Streptococcus veridans
1
Coagulase-negative Staphylococcus
3
Methicillin-sensitive Staphylococcus aureus
3
Methicillin-resistant Staphylococcus aureus
1
Diptheroids
3
Haemophilus influenzae
1
Enterobacter aerogenes
2
Serratia marcescens
2
“Negative”
2
cultured and cultures yielded oral flora and organisms generally thought to be commensal such as alpha-hemolytic Streptococcus, diphtheroids, and coagulase-negative Staphylococcus. Anaerobic cultures were rarely obtained and, even when obtained in the operating room, were negative. All patients had evidence of dental disease associated with sinusitis on sinus CT (Table 4). Periapical abscesses, including those with fistula, were present in 95% of patients on CT scan (Fig. 2); 24% demonstrated oroantral fistula. In our series there were no oroantral fistulas involving an absent tooth. Our definition of oroantral fistula included apical abscesses that had perforated into the maxillary antrum (Fig. 3).
FIGURE 3. Unenhanced axial image from a sinus CT shows a periapical abscess (white arrow) with communication into the maxillary sinus that represents an oral-antral fistula.
A total of 91% of patients had maxillary opacification and in all cases the opacification was ipsilateral to dental disease. Frontal opacification was present in 43% of patients and ethmoid opacification was present in 65% of patients. Dental pathology was reported on initial sinus CT radiology report in only 30% of patients. Two patients, who were not included in our series, had no maxillary sinus radiographic abnormality except for dental disease appreciated on sinus CT. In these 2 patients symptoms resolved with dental therapy.
Discussion Over the course of 30 months we prospectively accrued 21 patients with OMS. In only 2 patients were symptoms present for less than 3 months; thus, for the vast majority TABLE 4. Radiology n (%)
Evidence of dental disease on CT Periapical cyst
2/21 (5)
Oroantral fistula
5/21 (24)
Maxillary opacification
ing right maxillary molar periapical abscess (white arrow) in a tooth with a prior root canal.
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20/21 (95)
Periodontal disease
Initial radiologist comment
FIGURE 2. Coronal reformatted CT with no initial comment made regard-
21/21 (100)
7/21 (33) 21/21 (100)
Bilateral
9/21 (43)
Unilateral
12/21 (57)
Frontal opacification
10/21 (48)
Ethmoid opacification
15/21 (71)
CT & equals; computed tomography.
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of patients in our series, OMS meets the definition of CRS. The actual importance of odontogenic sinusitis as a cause of CRS is probably underappreciated. The diagnosis was initially missed by the radiologist on CT scan in 66% of our patients.
OMS literature search We found 58 articles in our search on odontogenic sinusitis with full text available in English published between November 1988 and June 2010. Thirteen articles gave an OMS incidence range, of either 10% to 12% or 4.6% to 47%. The source documents referenced in the articles for these incidence values of OMS are reviewed under “Primary sources of incidence of OMS.”
Primary sources of incidence of OMS Most of the primary source data for incidence of OMS is from Sweden and Germany and 5 of 7 source documents were published prior to 1965. The most recent article, Albu and Baciut,3 carefully defined their population as chronic maxillary sinusitis without NP. This reference was published after all of the currently available sinusitis guidelines. Table 2 presents the year, country, number of patients, incidence, and method of diagnosis for all cited and available source data. Ten articles10–17 cite a range of 10% to 12% that originates from Maloney and Doku’s18 1968 paper entitled “Maxillary sinusitis of odontogenic origin,” which cites the incidence rate from 2 papers from 1954 and 195819,20 (Table 5). However these 2 “primary” sources present no patient data to support their claims. Silcox’s19 1958 article states that “about 10% of all maxillary sinus infections are of a dental origin”; however, there are no references to support this assertion. Fleming’s20 1954 article does not provide an incidence of OMS, despite being referenced for this incidence in several reviews.
Three articles21–23 cite Melen’s incidence range of 4.6% to 47% that traces back to 4 articles written from 1949 to 198224–27 (Table 5). Incidence of symptoms is rarely presented in these papers; the exception is Bjork,27 who found that 46 of the 47 cases of OMS were unilateral and foul smelling. Several articles described the inherent difficulty in diagnosing OMS and attribute the wide range in incidence values to this difficulty. In 1986, Melen et al.7 reported an incidence of OMS of 40.6% (99/198) in a highly selected population of patients with at least 3 months of symptoms and objective evidence of disease on endoscopy or plain sinus X-ray. This series incorporated their earlier smaller series from 1982, which found an OMS incidence of 47% (29/62). The diagnostic methods used were ear, nose, and throat (ENT) examination, routine dental examination, dental and sinus X-rays, nasal endoscopy, and extended maxillodental examination. OMS was considered in patients with oroantral fistula or evidence of dental disease interfacing with the maxillary sinus on radiography or nasal endoscopy. In addition, he found that over one-half of patients referred with a diagnosis of chronic sinusitis actually had no objective evidence of sinusitis.
Sinusitis guidelines that reference OMS We found 85 sinusitis guidelines published in English with full text available from March 1998 to June 2010. Eleven (13%) guidelines mentioned a dental or odontogenic cause of maxillary sinusitis.2,28–37 In Table 6 we analyze the total number of pages of each of these guidelines and the number of sentences devoted to OMS. None of the 11 guidelines provided incidence values for OMS. Three articles provided a recommendation for the evaluation of a dental pathology. The senior author’s 2009 article suggests a CT scan to identify periodontal disease and periapical abscess as causes of sinusitis.28 Tichenor
TABLE 5. Primary sources from literature for OMS incidence Author
Year
Country
Incidence values
Total number of patients
2010
Romania
25% of nonpolypoid maxillary sinusitis
411
1958
Canada
10%
0
Not specified
1954
Australia
None provided
0
Not specified
Lindahl et al.24
1982
Sweden
47%
62
Schuchardt et al.25
1964
Germany
77%
1233
Not specified
1952
Germany
12.4%
1792
Patient history, symptoms, X-rays, operative report, history of dental extraction or cyst
1949
Sweden
4.6%
1019
Signs and symptoms, transillumination
3
Albu and Baciut
Method of diagnosis
ENT and dental exam with oral maxillofacial surgeon, sinus CT scan
10%-12% incidence Silcox19 20
Fleming
4.6%-47% incidence
Martensson Bjork27
26
ENT and dental examination, orthopantomogram and intraoral radiographs, antral puncture
CT = computed tomography; ENT = ear, nose, and throat; OMS = odontogenic maxillary sinusitis.
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TABLE 6. Sinusitis guidelines that reference odontogenic maxillary sinusitis Author 28
Ferguson et al.
Total number
Sentences dedicated
Year
of pages
to OMS
2009
14
7
Comments on OMS
Include OMS in differential diagnosis of CRS with mucopurulence Diagnosis and treatment of OMS discussed
29
Tichenor et al.
2008
13
10
Endoscopy can be used to identify OMS Include oral surgeon in treatment of OMS
Fokkens et al.2
2007
137
5
“CRS of dental origin should not be overlooked when considering the etiology of CRS.” Management schemes for adults and children state to “exclude dental infection” “Anaerobes are more prevalent in infections secondary to dental problems.”
Slavin et al.30
2005
35
2
Management scheme for sinusitis lists dental infection listed as an “other diagnosis” Describes anatomical considerations of odontogenic maxillary sinusitis
31
Klossek and Federspil
2005
9
1
Notes that French guidelines recommend antibacterial therapy for “sinusitis associated with dental infection”
Fokkens et al.32
2005
19
0
Management scheme for adult acute rhinosinusitis states “exclude dental infection”
Blomgren et al.
2005
6
4
Paragraph on diagnosis and treatment of odontogenic sinusitis as a “special consideration”
Meltzer et al.34
2004
62
1
Some cases of anaerobic acute sinusitis result from a primary dental pathology
2004
45
1
Lists dental infection as a predisposing factor for acute bacterial rhinosinusitis
2000
32
1
Lists dental infection as a predisposing factor for acute bacterial rhinosinusitis
1998
60
3
Maxillary sinusitis may be secondary dental infections or dental procedures
33
35
Anon et al. (SAHP) SAHP
36
Spector et al.37
Bad breath is often a symptom of OMS CRS = chronic rhinosinusitis; OMS = odontogenic maxillary sinusitis; SAHP = Sinus and Allergy Health Partnership.
et al.29 suggests that endoscopy can identify dental disease in the maxillary sinuses. The Finnish Clinical Practice Guidelines suggested sinus puncture, plain X-ray, dental panoramic radiograph, and a dental referral.33 The current widely quoted 10% to12% incidence of OMS is drawn from primary sources dating back over 50 years. Careful examination of these source documents shows that they fail to support this incidence. In a more recent investigation of the incidence of OMS, Melen et al.7 found that in a highly selected population of 198 adults referred for evaluation with refractory CRS, 40% of affected maxillary sinuses were from an odontogenic cause and of these 18% were bilateral OMS. Recently, guidelines have advocated division of CRS into NP and no NP. In the same study, Melen et al.7 noted NP were associated with OMS in 13.1% of cases and 23.4% of non-OMS cases. Similarly, bilateral sinus disease was less frequent in OMS cases than in non-OMS cases, 18% and 23%, respectively. In 2010, Albu and Baciut3 reported that 25% (104/411) of patients without NP undergoing ESS for CRS had OMS. None of our OMS patients had NP. We found that only 11 of 85 (13%) recent sinusitis guidelines mention an odontogenic or dental cause of sinusitis. Only 3 of these guidelines outlined diagnostic procedures for OMS.28,29,33 Given the common nature of dental disease and sinusitis, we recommend that future guidelines on diagnosis and management of rhinosinusitis, especially CRS, include odontogenic sinusitis in the differential diag-
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nosis with the recommendation that treatment of the dental pathology is usually required to resolve OMS.
Case series A recent meta-analysis of 15 articles by Arias-Irimia et al.38 found that OMS is most often diagnosed in the fifth decade of life and is more common in females. Melen et al.7 found that only 2 of the 99 patients in his series with OMS were under the age of 30. In our series the average age was in the sixth decade of life and no gender difference was found. Symptoms that classically have been thought to indicate a dental source include unilateral maxillary opacification on CT, found in 57% of our series, and patient perception of rotten smell or bad taste, present in 48% of patients in our series. Dental pain was present in only 29% of our patients. Brook1 also noted that dental pain is infrequent in OMS which he hypothesized was due to the ostiomeatal complex remaining patent and venting pressure from the diseased tooth. In 11% of patients with acute radiographic sinusitis by plain film, Williams and Simel39 found that pain in the upper teeth was the most specific indicator of an abnormal plain sinus film. Dental pain appears to be neither sensitive nor specific for a dental etiology and can also represent nonodontogenic causes of maxillary sinusitis. The symptom most frequently present and given the highest bothersome score in patients with OMS on the
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sinonasogram was nasal obstruction. This symptom is neither specific nor sensitive for OMS since nasal obstruction is common to rhinosinusitis regardless of etiology and is also frequently the most bothersome symptom in disorders that affect only the nose, irrespective of sinus involvement, such as allergic rhinitis. Diabetes could contribute to complications or dental disease; however, we found no evidence of increased risk of OMS in our series due to diabetes. Three (14%) of our patients had diabetes, consistent with the predicted incidence of diabetes of 23.1% (12.2 million) of Americans aged 60 years and older according to the American Diabetes Association.40 Periodontal disease is a common complication of diabetes and reduced sensation of dental pain due to diabetic neuropathy could potentially allow more advanced dental infection to occur before dental intervention. In our series, dentists were not able to reliably detect dental infection causing sinusitis. One-half of our patients saw a dentist during their sinus disease, but only 1 of 7 (14%) was noted to have dental pathology on dental X-ray. Thus dental pathology was missed in 86% of cases. This is similar to the report by Melen et al.7 that 56 in 99 (55%) of OMS cases are missed on routine dental examination including dental X-ray. Physicians should be mindful that a negative dental report does not exclude a dental etiology. Five patients in our series had unsuccessful ESS and our previous article has suggested that OMS is a cause of ESS failure.9 Presurgical CT scans provide an opportunity to examine for dental pathology before conducting unnecessary and usually unsuccessful ESS. The majority of the bacterial isolates in this series were Staphylococcus and Streptococcus species. Brook16 reports that almost 100% of bacterial maxillary sinusitis is anaerobic and that the organisms associated with OMS typically consist of a mixed polymicrobial infection with anaerobes outnumbering aerobes. Our failure to recover anaerobic bacteria may have been caused by failure to obtain anaerobic cultures, endoscopic sampling technique instead of antral tap, and lack of rapid transportation to the microbiology laboratory. Brook16 utilized rapid processing and careful handling of samples to recover a high percentage of anaerobic isolates. Over one-half of patients reported improvement of symptoms while on antibiotics; however, symptoms returned following both long and short courses of antibiotics, when antibiotics were withdrawn. For 90% of patients in our series, OMS was a chronic (