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Differences in self-reported symptoms in patients with chronic odontogenic and non-odontogenic rhinosinusitis
Am J Otolaryngol xxx (xxxx) xxxx
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Differences in self-reported symptoms in patients with chronic odontogenic and non-odontogenic rhinosinusitis Ivan Oreškia, , Tomislav Gregurićb, Petar Gulina, Natalija Prica Oreškic, Davor Brajdićd, Davor Vagiće ⁎
a
Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Dubrava, Gojka Šuška 6, 10000 Zagreb, Croatia Department of Radiology, University Hospital Center Sestre milosrdnice, Vinogradska cesta 29, 10000 Zagreb, Croatia c Dental Clinic Zagreb, Perkovčeva ulica 3, 10000 Zagreb, Croatia d Department of Oral and Maxillofacial Surgery, University Hospital Dubrava, Avenue G. Šuska 6, 10000 Zagreb, Croatia e Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Center Sestre milosrdnice, Vinogradska cesta 29, 10000 Zagreb, Croatia b
ARTICLE INFO Keywords: Odontogenic Chronic Rhinosinusitis SNOT-22 VAS
ABSTRACT
Purpose: To evaluate the possible differences in self-reported symptoms between patients with chronic odontogenic rhinosinusitis (CORS) and patients with chronic non-odontogenic rhinosinusitis (CnORS). Materials and methods: The study included 64 patients diagnosed with chronic rhinosinusitis according to EPOS guidelines. 32 patients had CORS, and the control group were 32 patients with CnORS. Patients were matched according to gender and age. All the patients underwent a CT scan evaluated by a radiologist, and were evaluated by an oral surgeon and otorhinolaryngologist before being assigned to one of the groups. The severity of the symptoms was assessed through questioners SNOT-22 (sino-nasal outcome test) and VAS (visual analogue scale) symptom score. Kolmogorov-Smirnov's, Fisher's and Mann-Whitney U test were used in the statistical analysis of the data. Results: People with CORS show similar symptomatology on SNOT-22 score to patients with CnORS, with no significant statistical difference between any of the SNOT-22 symptoms. VAS symptom score showed that odontogenic group had a significantly higher score for fever (p = .004) and halitosis (p = .003). Conclusion: Halitosis and fever might be the most important symptoms in differentiating between CORS and CnORS symptomatology. Better diagnostic tools, such as VAS symptom score might help medical professionals to be quicker at recognizing CORS specific symptomatology, and help them treat the disease as early and adequately as possible.
1. Introduction Chronic rhinosinusitis (CRS) is one of the most common chronic diseases. It affects approximately 10–15% of the population in all parts of the world. CRS affects all ethnic and age groups [1,2]. Due to CRS causing symptoms and restriction of life quality, there are approximately 12 million doctor visits, 1.2 million hospital outpatient visits, and more than 70 million restricted activity days annually in the United States [3]. According to the literature, up to 10% of cases are considered to be caused by odontogenic etiology. Moreover, the incidence of chronic odontogenic rhinosinusitis (CORS) is increasing in the USA and UK [4,5], mostly due to dental neglect amongst those who are not able to afford treatment, but also due to the large increase in complex
⁎
reconstructive dentistry, with procedures such as dental implants and bone grafts. This data makes accurate detection and treatment of CORS an ever more important issue in dentistry and otorhinolaryngology [6]. Odontogenic sinusitis generally occurs when the Schneidarian membrane integrity is compromised by dental pathologies. This can happen in patients with maxillary teeth pathology, maxillary dental trauma and due to iatrogenic causes, such as the placement of dental implants and dental extractions [5]. This disease is different in its pathophysiology, microbiology, diagnostics and management from chronic rhinosinusitis of non-odontogenic origin (CnORS), although clinical symptoms are not so evident [7–9]. Microbiological findings show that specimens from CORS are polymicrobial, and anaerobes are present in a majority of patients [10]. The most common bacteria isolated are Gram-negative anaerobic
Corresponding author at: Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Dubrava, Gojka Šuška 6, 10000 Zagreb, Croatia. E-mail address: [email protected] (I. Oreški).
https://doi.org/10.1016/j.amjoto.2020.102388 Received 24 November 2019 0196-0709/ © 2020 Elsevier Inc. All rights reserved.
Please cite this article as: Ivan Oreški, et al., Am J Otolaryngol, https://doi.org/10.1016/j.amjoto.2020.102388
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bacteria, Staphylococcus aureus, Peptostreptococcus species, and members of the Enterobacteriaceae [11]. Microbiology specimens of CnORS show that the most common microorganisms are anaerobic Gram-negative bacilli, Peptostreptococcus species, Staphylococcus aureus and viridans streptococci [12]. H. influenzae and M. catarrhalis are present in CnORS but absent in CORS [10]. The treatment of odontogenic sinusitis often requires management of the sinusitis as well as the odontogenic origin [13]. In this study, we try to evaluate the differences in self-reported symptoms caused by CORS and CnORS, which might lead to a sooner diagnosis and subsequent more efficient treatment of CORS.
membrane. They were all evaluated by a radiologist with an experience over 15 years in sinonasal pathology. The cases included following: oroantral fistula, periapical abscess, disrupted membrane after teeth extraction, and foreign body in maxillary sinus deriving from patients' dental tissue or artificial material from dental prosthetics (Fig. 1). After the CT scan, the patient was also evaluated by an oral surgeon and otorhinolaryngologist in order to confirm the diagnosis and to assign the patient to a specific group. Patients with no CT signs of dental disease and those not confirmed to be CORS by an oral surgeon or otorhinolaryngologist were included in the control group. 2.1. Statistical analysis
2. Materials and methods
The case-control matching procedure was used to randomly match cases and controls based on patients' gender and age (+/− five years). Normality of data distribution for continuous data has been checked with Kolmogorov-Smirnov's test and due to the test results appropriate non-parametric data analysis has been used in the following analyses. Fisher's exact test has been used to assess differences in categorical clinical variables between investigated groups. Mann-Whitney U test was used for differences in quantitative clinical variables (specific VAS scores and SNOT-22) between investigated groups. All P values below 0.05 have been considered significant. MedCalc Statistical Software version 19.1 (MedCalc Software bv, Ostend, Belgium; https://www. medcalc.org; 2019) has been used in all statistical procedures.
This prospective observational study was carried out from September 2015 until May 2019 and included 64 people who voluntarily participated. 32 patients with CnORS were included in the control group, and 32 people with CORS in the experimental group. They were matched according to gender and age (+/− five years). The study was approved by the University of Zagreb's Dental medicine school ethical committee (05-PA-30-11/2018). All of the patients had CRS diagnosed by EPOS (European Position Paper on Rhinosinusitis and Nasal Polyps 2012) guidelines [14] evaluated by an otorhinolaryngology specialist. EPOS guidelines define CRS as condition characterized by two or more symptoms, one of which should be either nasal blockage/obstruction/congestion or nasal discharge (anterior/ posterior nasal drip), and/or facial pain/pressure, and/or reduction or loss of smell; and either endoscopic signs of polyps and/or mucopurulent discharge primarily from middle meatus and/or; edema/mucosal obstruction primarily in middle meatus and/or CT changes showing mucosal changes within the ostiomeatal complex and/or sinuses. Exclusion factors were: age under 18, nasal polyps, cystic fibrosis, acute exacerbation of rhinosinusitis, trauma or tumor of the nasal/sinus cavities, and granulomatous disease affecting the sinus or nasal cavity mucosa. At present, there are is no strict consensus diagnostic criteria to differentiate CORS from CnORS. However, CORS is clearly a distinct clinical entity and it is identified through clinical characteristics including history and radiographic findings as described in the literature [15]. Before undergoing a CT scan, patients were given questioners regarding the subjective assessment of the symptoms of the disease. VAS (visual analogue scale) symptom score test [16] and SNOT-22 (sinonasal outcome test) [17] were used for evaluation. Patients were also given one additional questionnaire which evaluated the presence of asthma, aspirin (ASA) intolerance, allergic rhinitis, smoking, previous sinus surgery, nasal corticosteroid use, antihistaminic and antibiotic use. VAS symptom score includes symptoms listed in Table 1. Patients grade symptoms on a scale, marking the intensity of the symptoms on a straight line from 0 to 10 cm. The symptoms in VAS symptom score test were based on the major and minor factors associated with CRS according to recommendations proposed by the Rhinosinusitis Task Force [16]. SNOT-22 is the most used validated questionnaire that provides a quantitative measure of symptom severity and HRQL for patients with CRS. In this questionnaire the patients evaluate the intensity of the symptoms individually on a Likert scale of 0–5. Score of 0 means no symptoms, and the maximum 5 signifies extreme symptoms [17,18]. In the general population the SNOT-22 score is around 30 points [19]. SNOT-22 questionnaire includes the symptoms listed in Table 2. The CT scan was made on each patient on the multidetector CT scanner with spiral mode scanning and axial cuts of a 0.5-mm thickness and were later evaluated using multiplanar reconstruction images. In order for the patient to be included in the study in the CORS group, patient's CT images had to show signs of affected Schneiderian
3. Results The study found that there were no significant differences regarding categorical clinical variables between CORS and CnORS (Table 3). As case-control matching procedure has been used to randomly match cases and controls based on patients age and gender. It was expected that there were no significant differences in these variables, but since there were no significant differences in other monitored categorical variables, this implies that our two groups are nearly the same regarding these data. Differences in specific VAS scores and total SNOT22 scores between investigated groups are shown in Table 4. CORS group had significantly higher VAS values in assessing fever (P = .004) and halitosis (P = .003). Differences in other values including individual, total SNOT-22 symptoms and the rest of VAS symptoms were not significantly different. 4. Discussion CORS is a very widespread disease with a significant impact worldwide. The incidence and prevalence of odontogenic sinusitis is probably underreported in the literature. Recent studies indicate an incidence much higher than previously thought, and it is estimated that up to 40% of chronic bacterial maxillary sinus infections are attributed to a dental source [7]. CORS causes persistent symptoms with varying intensity, and in rare occasions, even orbital and intracranial complications. CORS and its complications represent a heterogeneous group of conditions that often require multidisciplinary care. CORS has distinct pathophysiology, diagnostic considerations, microbiology, and treatment strategies compared with CnORS. Clinicians who accurately identify odontogenic sources, increase the efficacy of medical and surgical treatments and improve patient outcomes [20]. The problem with studies regarding CORS is that the literature is not always clear on differentiating chronic and acute disease. Also, the term maxillary rhinosinusitis is often referred as a synonym, but this is not entirely correct. Maxillary sinusitis does not always imply CORS, while CORS often implies more sinuses than just the maxillary sinus. CT scans give a detailed examination of the patient's paranasal sinus anatomy and show mucosal changes within the ostiomeatal complex and/or sinuses, which makes this imaging modality the gold standard 2
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Table 1 Example of the VAS questionnaire with a list of symptoms.
Seriousness of the complaints: Please draw a vertical line to the point that best corresponds to, how bothersome were the following symptoms within the last month, as given to the example: * Nasal discharge:
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
* Headache:
None
More than I can imagine
* Dental pain:
None
More than I can imagine
* Fatigue:
None
More than I can imagine
* Ear pressure:
None
More than I can imagine
* Fever:
None
More than I can imagine
* Halitosis:
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
* Nasal obstruction:
* Postnasal discharge:
* Smell impairment:
* Facial pain/pressure:
* Facial fullness:
* Cough:
* Nasal itching:
* Sneezing:
* Eye tearing:
for radiographic evaluation in patients with CRS [5]. CORS due to the nature of the disease always affects the maxillary sinus. All of our CORS patients had signs of affected Schneiderian membrane and mucosal changes in the maxillary sinuses. There are a lot of studies comparing CT finding and the severity of the disease in CRS. Most of them found no association of CT score with the overall disease severity score [21,22]. To this day, there is no research in the literature which directly compares CT findings of CORS and CnORS. Lee and Lee tried to assess the radiological characteristics of CORS [23]. Their study shows that CORS affects less paranasal sinuses and produces less mucosal thickening (using Lund – Mackay score) than CRS [24]. It must be noted that comparing radiological findings of CORS with CRS is not the same as comparing with CnORS, because CRS might also include CORS patients, which makes the comparison less valuable. Further research is needed
in radiological characteristics of CORS, especially in comparison with CnORS. Some studies showed CORS had a significantly larger presence of unilateral disease and is more often associated with symptoms of dental pain, ipsilateral facial pain, foul smell and nasal secretion [7,25]. However, currently used questionnaires are not adequate for the diagnosis of unilateral disease, and according to some studies, symptoms such as dental pain and hypersensitivity, do not reliably predict an odontogenic cause. Brook [26] hypothesized that the lack of dental complaints might be due to the preserved patency of the ostiomeatal complex, which allows egress of pressure from within the sinus. In this study, we matched the patients according to gender because some studies show there may be differences in the perception of CRS between genders. According to the study by Jurlin et al. [27], gender 3
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Table 2 Example of the SNOT-22 questionnaire with a list of symptoms.
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long symptom duration, but also had similar overall symptom duration, with 50th percentile's median of 41.0 months for CORS and 42.0 months for CnORS. The reason for the convergence of symptoms in the long term might be found in the difference between the two pathophysiological phases of odontogenic sinusitis. An acute phase, characterized by an initial activation of the innate immune system (neutrophils and macrophages), and a chronic phase found in CORS, in which the lesion is much more organized and characterized by an adaptive immune response [30]. In a recent study by Simuntis et al. [31], patients with CORS had significantly higher scores in SNOT-22 with regards to emotional disturbance, while CnORS group had significantly higher worse scores in sleep and functional disturbance [31]. Individual symptoms, as in our study, showed no difference. This study also included malodor as an additional 23rd symptom, which proved to be the most differentiating individual symptom between odontogenic and nonodontogenic group. Unlike in the SNOT-22, however, we found interesting differences in VAS symptom score. VAS showed a significant self-reported difference in halitosis and fever. The main chemicals causing the odor in halitosis seem to be volatile sulphur compounds [32]. It may be that those compounds formulate more frequently during inflammation in CORS than CnORS due to the different bacterial biofilms. Biofilms are dynamic polymicrobial communities of slowly-replicating and metabolically-quiescent strains embedded in a matrix rich in exopolysaccharides, proteins, and nucleic acid [30]. Along with halitosis, we found statistically higher self-reported fever in CORS group. In the literature, there is no research which tried to correlate temperature and rhinosinusitis subtypes. The reason for this phenomenon is yet to be explained. It may be the case that odontogenic infections produce a slightly more intensive inflammation response overall, which activates more pyrogenic cytokines such as tumor necrosis factor (TNF), interleukin (IL)-1, IL-6, and interferons. Halitosis and temperature, along with malodor [31], make a triad of symptoms which might help create the possibility for earlier diagnosis of the patients with odontogenic etiology, and help to preserve the QOL of the patients with CORS. Better diagnostics between CnORS and CORS might lead to better timing, extent and method of surgery. CnORS is generally treated with medical therapy, including nasal saline irrigation and topical nasal steroid spray. When medical therapy fails to improve symptoms, or in the presence of actual or impending complications, surgery is usually considered. Functional endoscopic sinus surgery (FESS) is now considered a standard practice [33]. CORS refractory to medical therapy often involves a different approach and requires a definitive treatment of the underlying dental pathology, including endodontic treatment with root canal, dental extraction or apicoectomy. Functional endoscopic sinus surgery (FESS) is required only for patients with possible persistent disease after dental procedures [23,34,35]. Although most of the studies highlight the importance of dental surgery as the primary treatment for CORS, there is new evidence which suggests that FESS alone might be an effective approach for the treatment of the disease [36,37]. Further studies are needed to determine a definitive algorithm in the surgical treatment of CORS.
Fig. 1. CT scan of a 50-year-old patient with an oroantral fistula on the right side with CORS. Table 3 Differences between groups in categorical clinical variables: Fisher's exact test. Group
P
CnORS N = 32
Gender Asthma ASA intolerance Allergic rhinitis Smoking Previous sinus surgery Nasal corticosteroid use Antihistaminic use Antibiotic use
Male Female No Yes No Yes No Yes No Yes No Yes No Yes No Yes No Yes
CORS N = 32
N
%
N
%
19 13 30 2 30 2 26 6 27 5 25 7 11 21 29 2 29 3
59.4% 40.6% 93.8% 6.3% 93.8% 6.3% 81.3% 18.8% 84.4% 15.6% 78.1% 21.9% 34.4% 65.6% 93.5% 6.5% 90.6% 9.4%
19 13 31 1 32 0 28 4 24 8 29 3 15 17 27 5 25 7
59.4% 40.6% 96.9% 3.1% 100.0% 0.0% 87.5% 12.5% 75.0% 25.0% 90.6% 9.4% 46.9% 53.1% 84.4% 15.6% 78.1% 21.9%
1.000 1.000 0.492 0.732 0.536 0.302 0.446 0.426 0.302
appears to be a major confounder affecting overall disease severity in CRS without polyps, and it may be that the pathogenesis is different in females compared to males. Patients were also matched by age, because of different expression of CRS in different age groups [28,29]. We found no significant difference between SNOT-22 score in our two groups. We also did not find any difference between any of the individual symptoms in SNOT-22. Similar results were reported by Gaudin et al. [15] They showed in their retrospective study of 21 patients that CORS was not associated with more intense CRS symptoms (measured by SNOT-22 score), however, patients with CORS had a significantly greater general health-related QoL detriment. One of the hypotheses for this phenomenon might be that CORS patients were once suddenly struck by the disease, while CnORS patients frequently had slowly incremental symptomatology and therefore might be more accustomed. This might be annulled by precise symptom durationmatching because it seems that over time, CORS and CnORS converge to a very similar symptomatology. It needs to be noted that patients in our study not only had a strict criterion of a minimum of three months
5. Conclusion This study shows that patients matched by age and gender with CORS and CnORS have similar symptomatology. However, patients with CORS had a statistically significant higher score in fever and halitosis, which might be the most important symptoms in differentiating these two entities. This finding could make VAS symptom score questionnaire a more useful diagnostic tool than SNOT-22 in the diagnostic of CORS. Further research with a large number of patients is needed to make definite conclusions on this topic. 5
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Table 4 Differences in specific VAS symptom scores and SNOT-22 between investigated groups: Mann-Whitney U test. N
Age (years) Symptoms duration (months) SNOT22 Score (total) VAS1 nasal discharge VAS2 postnasal discharge VAS3 nasal obstruction VAS4 smell impairment VAS5 facial pain/pressure VAS6 facial fullness VAS7 headache VAS8 dental pain VAS9 fatigue VAS10 ear pressure VAS11 fever VAS12 halitosis VAS13 cough VAS14 nasal itching VAS15 sneezing VAS16 eye tearing
CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS
32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32
Minimum
Maximum
20.00 25.00 4.00 4.00 5.00 13.00 0.50 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
74.00 70.00 360.00 360.00 72.00 86.00 10.00 9.50 10.00 10.00 10.00 10.00 9.50 9.00 10.00 10.00 10.00 8.90 10.00 9.50 10.00 9.40 9.30 8.00 10.00 8.90 3.00 4.00 10.00 10.00 10.00 9.40 10.00 8.80 10.00 9.80 10.00 9.80
Percentiles
P
25th
50th (median)
75th
35.00 35.25 12.00 7.25 27.25 26.75 1.73 1.13 4.83 4.45 4.38 2.75 0.00 0.00 2.26 0.95 0.00 0.03 0.85 0.93 0.00 0.03 0.00 0.13 0.00 0.00 0.00 0.00 0.00 0.03 0.08 0.10 0.00 0.00 0.00 0.23 0.00 0.00
41.00 42.00 42.00 42.00 42.50 44.50 4.30 4.90 7.90 6.75 7.95 6.45 0.65 0.45 4.43 5.05 2.28 2.35 5.60 2.85 0.00 0.80 3.68 2.80 1.00 0.35 0.00 0.00 0.00 3.75 1.20 0.70 1.40 0.45 1.90 1.30 0.55 0.35
56.25 50.75 120.00 120.00 56.75 55.00 6.13 6.95 9.10 8.00 9.40 8.28 3.73 5.30 8.35 7.75 5.98 7.25 8.86 7.75 3.48 4.88 6.90 5.28 7.33 2.40 0.00 0.10 1.65 7.50 4.83 3.30 5.03 4.78 4.80 4.48 4.45 3.05
0.783 0.647 0.682 0.995 0.480 0.103 0.646 0.532 0.639 0.353 0.138 0.543 0.770 0.004 0.003 0.441 0.641 0.903 0.651
* Bold and underline data show a significant difference (p < 0.05)
CRediT authorship contribution statement
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Differences in self-reported symptoms in patients with chronic odontogenic and non-odontogenic rhinosinusitis Ivan Oreškia, , Tomislav Gregurićb, Petar Gulina, Natalija Prica Oreškic, Davor Brajdićd, Davor Vagiće ⁎
a
Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Dubrava, Gojka Šuška 6, 10000 Zagreb, Croatia Department of Radiology, University Hospital Center Sestre milosrdnice, Vinogradska cesta 29, 10000 Zagreb, Croatia c Dental Clinic Zagreb, Perkovčeva ulica 3, 10000 Zagreb, Croatia d Department of Oral and Maxillofacial Surgery, University Hospital Dubrava, Avenue G. Šuska 6, 10000 Zagreb, Croatia e Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Center Sestre milosrdnice, Vinogradska cesta 29, 10000 Zagreb, Croatia b
ARTICLE INFO Keywords: Odontogenic Chronic Rhinosinusitis SNOT-22 VAS
ABSTRACT
Purpose: To evaluate the possible differences in self-reported symptoms between patients with chronic odontogenic rhinosinusitis (CORS) and patients with chronic non-odontogenic rhinosinusitis (CnORS). Materials and methods: The study included 64 patients diagnosed with chronic rhinosinusitis according to EPOS guidelines. 32 patients had CORS, and the control group were 32 patients with CnORS. Patients were matched according to gender and age. All the patients underwent a CT scan evaluated by a radiologist, and were evaluated by an oral surgeon and otorhinolaryngologist before being assigned to one of the groups. The severity of the symptoms was assessed through questioners SNOT-22 (sino-nasal outcome test) and VAS (visual analogue scale) symptom score. Kolmogorov-Smirnov's, Fisher's and Mann-Whitney U test were used in the statistical analysis of the data. Results: People with CORS show similar symptomatology on SNOT-22 score to patients with CnORS, with no significant statistical difference between any of the SNOT-22 symptoms. VAS symptom score showed that odontogenic group had a significantly higher score for fever (p = .004) and halitosis (p = .003). Conclusion: Halitosis and fever might be the most important symptoms in differentiating between CORS and CnORS symptomatology. Better diagnostic tools, such as VAS symptom score might help medical professionals to be quicker at recognizing CORS specific symptomatology, and help them treat the disease as early and adequately as possible.
1. Introduction Chronic rhinosinusitis (CRS) is one of the most common chronic diseases. It affects approximately 10–15% of the population in all parts of the world. CRS affects all ethnic and age groups [1,2]. Due to CRS causing symptoms and restriction of life quality, there are approximately 12 million doctor visits, 1.2 million hospital outpatient visits, and more than 70 million restricted activity days annually in the United States [3]. According to the literature, up to 10% of cases are considered to be caused by odontogenic etiology. Moreover, the incidence of chronic odontogenic rhinosinusitis (CORS) is increasing in the USA and UK [4,5], mostly due to dental neglect amongst those who are not able to afford treatment, but also due to the large increase in complex
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reconstructive dentistry, with procedures such as dental implants and bone grafts. This data makes accurate detection and treatment of CORS an ever more important issue in dentistry and otorhinolaryngology [6]. Odontogenic sinusitis generally occurs when the Schneidarian membrane integrity is compromised by dental pathologies. This can happen in patients with maxillary teeth pathology, maxillary dental trauma and due to iatrogenic causes, such as the placement of dental implants and dental extractions [5]. This disease is different in its pathophysiology, microbiology, diagnostics and management from chronic rhinosinusitis of non-odontogenic origin (CnORS), although clinical symptoms are not so evident [7–9]. Microbiological findings show that specimens from CORS are polymicrobial, and anaerobes are present in a majority of patients [10]. The most common bacteria isolated are Gram-negative anaerobic
Corresponding author at: Department of Otorhinolaryngology and Head and Neck Surgery, University Hospital Dubrava, Gojka Šuška 6, 10000 Zagreb, Croatia. E-mail address: [email protected] (I. Oreški).
https://doi.org/10.1016/j.amjoto.2020.102388 Received 24 November 2019 0196-0709/ © 2020 Elsevier Inc. All rights reserved.
Please cite this article as: Ivan Oreški, et al., Am J Otolaryngol, https://doi.org/10.1016/j.amjoto.2020.102388
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bacteria, Staphylococcus aureus, Peptostreptococcus species, and members of the Enterobacteriaceae [11]. Microbiology specimens of CnORS show that the most common microorganisms are anaerobic Gram-negative bacilli, Peptostreptococcus species, Staphylococcus aureus and viridans streptococci [12]. H. influenzae and M. catarrhalis are present in CnORS but absent in CORS [10]. The treatment of odontogenic sinusitis often requires management of the sinusitis as well as the odontogenic origin [13]. In this study, we try to evaluate the differences in self-reported symptoms caused by CORS and CnORS, which might lead to a sooner diagnosis and subsequent more efficient treatment of CORS.
membrane. They were all evaluated by a radiologist with an experience over 15 years in sinonasal pathology. The cases included following: oroantral fistula, periapical abscess, disrupted membrane after teeth extraction, and foreign body in maxillary sinus deriving from patients' dental tissue or artificial material from dental prosthetics (Fig. 1). After the CT scan, the patient was also evaluated by an oral surgeon and otorhinolaryngologist in order to confirm the diagnosis and to assign the patient to a specific group. Patients with no CT signs of dental disease and those not confirmed to be CORS by an oral surgeon or otorhinolaryngologist were included in the control group. 2.1. Statistical analysis
2. Materials and methods
The case-control matching procedure was used to randomly match cases and controls based on patients' gender and age (+/− five years). Normality of data distribution for continuous data has been checked with Kolmogorov-Smirnov's test and due to the test results appropriate non-parametric data analysis has been used in the following analyses. Fisher's exact test has been used to assess differences in categorical clinical variables between investigated groups. Mann-Whitney U test was used for differences in quantitative clinical variables (specific VAS scores and SNOT-22) between investigated groups. All P values below 0.05 have been considered significant. MedCalc Statistical Software version 19.1 (MedCalc Software bv, Ostend, Belgium; https://www. medcalc.org; 2019) has been used in all statistical procedures.
This prospective observational study was carried out from September 2015 until May 2019 and included 64 people who voluntarily participated. 32 patients with CnORS were included in the control group, and 32 people with CORS in the experimental group. They were matched according to gender and age (+/− five years). The study was approved by the University of Zagreb's Dental medicine school ethical committee (05-PA-30-11/2018). All of the patients had CRS diagnosed by EPOS (European Position Paper on Rhinosinusitis and Nasal Polyps 2012) guidelines [14] evaluated by an otorhinolaryngology specialist. EPOS guidelines define CRS as condition characterized by two or more symptoms, one of which should be either nasal blockage/obstruction/congestion or nasal discharge (anterior/ posterior nasal drip), and/or facial pain/pressure, and/or reduction or loss of smell; and either endoscopic signs of polyps and/or mucopurulent discharge primarily from middle meatus and/or; edema/mucosal obstruction primarily in middle meatus and/or CT changes showing mucosal changes within the ostiomeatal complex and/or sinuses. Exclusion factors were: age under 18, nasal polyps, cystic fibrosis, acute exacerbation of rhinosinusitis, trauma or tumor of the nasal/sinus cavities, and granulomatous disease affecting the sinus or nasal cavity mucosa. At present, there are is no strict consensus diagnostic criteria to differentiate CORS from CnORS. However, CORS is clearly a distinct clinical entity and it is identified through clinical characteristics including history and radiographic findings as described in the literature [15]. Before undergoing a CT scan, patients were given questioners regarding the subjective assessment of the symptoms of the disease. VAS (visual analogue scale) symptom score test [16] and SNOT-22 (sinonasal outcome test) [17] were used for evaluation. Patients were also given one additional questionnaire which evaluated the presence of asthma, aspirin (ASA) intolerance, allergic rhinitis, smoking, previous sinus surgery, nasal corticosteroid use, antihistaminic and antibiotic use. VAS symptom score includes symptoms listed in Table 1. Patients grade symptoms on a scale, marking the intensity of the symptoms on a straight line from 0 to 10 cm. The symptoms in VAS symptom score test were based on the major and minor factors associated with CRS according to recommendations proposed by the Rhinosinusitis Task Force [16]. SNOT-22 is the most used validated questionnaire that provides a quantitative measure of symptom severity and HRQL for patients with CRS. In this questionnaire the patients evaluate the intensity of the symptoms individually on a Likert scale of 0–5. Score of 0 means no symptoms, and the maximum 5 signifies extreme symptoms [17,18]. In the general population the SNOT-22 score is around 30 points [19]. SNOT-22 questionnaire includes the symptoms listed in Table 2. The CT scan was made on each patient on the multidetector CT scanner with spiral mode scanning and axial cuts of a 0.5-mm thickness and were later evaluated using multiplanar reconstruction images. In order for the patient to be included in the study in the CORS group, patient's CT images had to show signs of affected Schneiderian
3. Results The study found that there were no significant differences regarding categorical clinical variables between CORS and CnORS (Table 3). As case-control matching procedure has been used to randomly match cases and controls based on patients age and gender. It was expected that there were no significant differences in these variables, but since there were no significant differences in other monitored categorical variables, this implies that our two groups are nearly the same regarding these data. Differences in specific VAS scores and total SNOT22 scores between investigated groups are shown in Table 4. CORS group had significantly higher VAS values in assessing fever (P = .004) and halitosis (P = .003). Differences in other values including individual, total SNOT-22 symptoms and the rest of VAS symptoms were not significantly different. 4. Discussion CORS is a very widespread disease with a significant impact worldwide. The incidence and prevalence of odontogenic sinusitis is probably underreported in the literature. Recent studies indicate an incidence much higher than previously thought, and it is estimated that up to 40% of chronic bacterial maxillary sinus infections are attributed to a dental source [7]. CORS causes persistent symptoms with varying intensity, and in rare occasions, even orbital and intracranial complications. CORS and its complications represent a heterogeneous group of conditions that often require multidisciplinary care. CORS has distinct pathophysiology, diagnostic considerations, microbiology, and treatment strategies compared with CnORS. Clinicians who accurately identify odontogenic sources, increase the efficacy of medical and surgical treatments and improve patient outcomes [20]. The problem with studies regarding CORS is that the literature is not always clear on differentiating chronic and acute disease. Also, the term maxillary rhinosinusitis is often referred as a synonym, but this is not entirely correct. Maxillary sinusitis does not always imply CORS, while CORS often implies more sinuses than just the maxillary sinus. CT scans give a detailed examination of the patient's paranasal sinus anatomy and show mucosal changes within the ostiomeatal complex and/or sinuses, which makes this imaging modality the gold standard 2
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Table 1 Example of the VAS questionnaire with a list of symptoms.
Seriousness of the complaints: Please draw a vertical line to the point that best corresponds to, how bothersome were the following symptoms within the last month, as given to the example: * Nasal discharge:
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
* Headache:
None
More than I can imagine
* Dental pain:
None
More than I can imagine
* Fatigue:
None
More than I can imagine
* Ear pressure:
None
More than I can imagine
* Fever:
None
More than I can imagine
* Halitosis:
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
None
More than I can imagine
* Nasal obstruction:
* Postnasal discharge:
* Smell impairment:
* Facial pain/pressure:
* Facial fullness:
* Cough:
* Nasal itching:
* Sneezing:
* Eye tearing:
for radiographic evaluation in patients with CRS [5]. CORS due to the nature of the disease always affects the maxillary sinus. All of our CORS patients had signs of affected Schneiderian membrane and mucosal changes in the maxillary sinuses. There are a lot of studies comparing CT finding and the severity of the disease in CRS. Most of them found no association of CT score with the overall disease severity score [21,22]. To this day, there is no research in the literature which directly compares CT findings of CORS and CnORS. Lee and Lee tried to assess the radiological characteristics of CORS [23]. Their study shows that CORS affects less paranasal sinuses and produces less mucosal thickening (using Lund – Mackay score) than CRS [24]. It must be noted that comparing radiological findings of CORS with CRS is not the same as comparing with CnORS, because CRS might also include CORS patients, which makes the comparison less valuable. Further research is needed
in radiological characteristics of CORS, especially in comparison with CnORS. Some studies showed CORS had a significantly larger presence of unilateral disease and is more often associated with symptoms of dental pain, ipsilateral facial pain, foul smell and nasal secretion [7,25]. However, currently used questionnaires are not adequate for the diagnosis of unilateral disease, and according to some studies, symptoms such as dental pain and hypersensitivity, do not reliably predict an odontogenic cause. Brook [26] hypothesized that the lack of dental complaints might be due to the preserved patency of the ostiomeatal complex, which allows egress of pressure from within the sinus. In this study, we matched the patients according to gender because some studies show there may be differences in the perception of CRS between genders. According to the study by Jurlin et al. [27], gender 3
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Table 2 Example of the SNOT-22 questionnaire with a list of symptoms.
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long symptom duration, but also had similar overall symptom duration, with 50th percentile's median of 41.0 months for CORS and 42.0 months for CnORS. The reason for the convergence of symptoms in the long term might be found in the difference between the two pathophysiological phases of odontogenic sinusitis. An acute phase, characterized by an initial activation of the innate immune system (neutrophils and macrophages), and a chronic phase found in CORS, in which the lesion is much more organized and characterized by an adaptive immune response [30]. In a recent study by Simuntis et al. [31], patients with CORS had significantly higher scores in SNOT-22 with regards to emotional disturbance, while CnORS group had significantly higher worse scores in sleep and functional disturbance [31]. Individual symptoms, as in our study, showed no difference. This study also included malodor as an additional 23rd symptom, which proved to be the most differentiating individual symptom between odontogenic and nonodontogenic group. Unlike in the SNOT-22, however, we found interesting differences in VAS symptom score. VAS showed a significant self-reported difference in halitosis and fever. The main chemicals causing the odor in halitosis seem to be volatile sulphur compounds [32]. It may be that those compounds formulate more frequently during inflammation in CORS than CnORS due to the different bacterial biofilms. Biofilms are dynamic polymicrobial communities of slowly-replicating and metabolically-quiescent strains embedded in a matrix rich in exopolysaccharides, proteins, and nucleic acid [30]. Along with halitosis, we found statistically higher self-reported fever in CORS group. In the literature, there is no research which tried to correlate temperature and rhinosinusitis subtypes. The reason for this phenomenon is yet to be explained. It may be the case that odontogenic infections produce a slightly more intensive inflammation response overall, which activates more pyrogenic cytokines such as tumor necrosis factor (TNF), interleukin (IL)-1, IL-6, and interferons. Halitosis and temperature, along with malodor [31], make a triad of symptoms which might help create the possibility for earlier diagnosis of the patients with odontogenic etiology, and help to preserve the QOL of the patients with CORS. Better diagnostics between CnORS and CORS might lead to better timing, extent and method of surgery. CnORS is generally treated with medical therapy, including nasal saline irrigation and topical nasal steroid spray. When medical therapy fails to improve symptoms, or in the presence of actual or impending complications, surgery is usually considered. Functional endoscopic sinus surgery (FESS) is now considered a standard practice [33]. CORS refractory to medical therapy often involves a different approach and requires a definitive treatment of the underlying dental pathology, including endodontic treatment with root canal, dental extraction or apicoectomy. Functional endoscopic sinus surgery (FESS) is required only for patients with possible persistent disease after dental procedures [23,34,35]. Although most of the studies highlight the importance of dental surgery as the primary treatment for CORS, there is new evidence which suggests that FESS alone might be an effective approach for the treatment of the disease [36,37]. Further studies are needed to determine a definitive algorithm in the surgical treatment of CORS.
Fig. 1. CT scan of a 50-year-old patient with an oroantral fistula on the right side with CORS. Table 3 Differences between groups in categorical clinical variables: Fisher's exact test. Group
P
CnORS N = 32
Gender Asthma ASA intolerance Allergic rhinitis Smoking Previous sinus surgery Nasal corticosteroid use Antihistaminic use Antibiotic use
Male Female No Yes No Yes No Yes No Yes No Yes No Yes No Yes No Yes
CORS N = 32
N
%
N
%
19 13 30 2 30 2 26 6 27 5 25 7 11 21 29 2 29 3
59.4% 40.6% 93.8% 6.3% 93.8% 6.3% 81.3% 18.8% 84.4% 15.6% 78.1% 21.9% 34.4% 65.6% 93.5% 6.5% 90.6% 9.4%
19 13 31 1 32 0 28 4 24 8 29 3 15 17 27 5 25 7
59.4% 40.6% 96.9% 3.1% 100.0% 0.0% 87.5% 12.5% 75.0% 25.0% 90.6% 9.4% 46.9% 53.1% 84.4% 15.6% 78.1% 21.9%
1.000 1.000 0.492 0.732 0.536 0.302 0.446 0.426 0.302
appears to be a major confounder affecting overall disease severity in CRS without polyps, and it may be that the pathogenesis is different in females compared to males. Patients were also matched by age, because of different expression of CRS in different age groups [28,29]. We found no significant difference between SNOT-22 score in our two groups. We also did not find any difference between any of the individual symptoms in SNOT-22. Similar results were reported by Gaudin et al. [15] They showed in their retrospective study of 21 patients that CORS was not associated with more intense CRS symptoms (measured by SNOT-22 score), however, patients with CORS had a significantly greater general health-related QoL detriment. One of the hypotheses for this phenomenon might be that CORS patients were once suddenly struck by the disease, while CnORS patients frequently had slowly incremental symptomatology and therefore might be more accustomed. This might be annulled by precise symptom durationmatching because it seems that over time, CORS and CnORS converge to a very similar symptomatology. It needs to be noted that patients in our study not only had a strict criterion of a minimum of three months
5. Conclusion This study shows that patients matched by age and gender with CORS and CnORS have similar symptomatology. However, patients with CORS had a statistically significant higher score in fever and halitosis, which might be the most important symptoms in differentiating these two entities. This finding could make VAS symptom score questionnaire a more useful diagnostic tool than SNOT-22 in the diagnostic of CORS. Further research with a large number of patients is needed to make definite conclusions on this topic. 5
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Table 4 Differences in specific VAS symptom scores and SNOT-22 between investigated groups: Mann-Whitney U test. N
Age (years) Symptoms duration (months) SNOT22 Score (total) VAS1 nasal discharge VAS2 postnasal discharge VAS3 nasal obstruction VAS4 smell impairment VAS5 facial pain/pressure VAS6 facial fullness VAS7 headache VAS8 dental pain VAS9 fatigue VAS10 ear pressure VAS11 fever VAS12 halitosis VAS13 cough VAS14 nasal itching VAS15 sneezing VAS16 eye tearing
CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS CORS CnORS
32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32
Minimum
Maximum
20.00 25.00 4.00 4.00 5.00 13.00 0.50 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
74.00 70.00 360.00 360.00 72.00 86.00 10.00 9.50 10.00 10.00 10.00 10.00 9.50 9.00 10.00 10.00 10.00 8.90 10.00 9.50 10.00 9.40 9.30 8.00 10.00 8.90 3.00 4.00 10.00 10.00 10.00 9.40 10.00 8.80 10.00 9.80 10.00 9.80
Percentiles
P
25th
50th (median)
75th
35.00 35.25 12.00 7.25 27.25 26.75 1.73 1.13 4.83 4.45 4.38 2.75 0.00 0.00 2.26 0.95 0.00 0.03 0.85 0.93 0.00 0.03 0.00 0.13 0.00 0.00 0.00 0.00 0.00 0.03 0.08 0.10 0.00 0.00 0.00 0.23 0.00 0.00
41.00 42.00 42.00 42.00 42.50 44.50 4.30 4.90 7.90 6.75 7.95 6.45 0.65 0.45 4.43 5.05 2.28 2.35 5.60 2.85 0.00 0.80 3.68 2.80 1.00 0.35 0.00 0.00 0.00 3.75 1.20 0.70 1.40 0.45 1.90 1.30 0.55 0.35
56.25 50.75 120.00 120.00 56.75 55.00 6.13 6.95 9.10 8.00 9.40 8.28 3.73 5.30 8.35 7.75 5.98 7.25 8.86 7.75 3.48 4.88 6.90 5.28 7.33 2.40 0.00 0.10 1.65 7.50 4.83 3.30 5.03 4.78 4.80 4.48 4.45 3.05
0.783 0.647 0.682 0.995 0.480 0.103 0.646 0.532 0.639 0.353 0.138 0.543 0.770 0.004 0.003 0.441 0.641 0.903 0.651
* Bold and underline data show a significant difference (p < 0.05)
CRediT authorship contribution statement
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Ivan Oreški:Conceptualization, Investigation, Methodology, Writing - original draft.Tomislav Gregurić:Investigation, Writing review & editing, Supervision.Petar Gulin:Data curation, Visualization, Formal analysis.Natalija Prica Oreški:Investigation, Writing original draft.Davor Brajdić:Investigation.Davor Vagić:Conceptualization, Supervision, Writing - review & editing. Declaration of competing interest None. References [1] Pleis JR, Lucas JW, Ward BW. Summary health statistics for U.S. adults: National Health Interview Survey, 2008. Vital health stat. Series 10 vol. 242. 2009. p. 1–157. Data from the National Health Survey. [2] Meltzer EO, Hamilos DL. Rhinosinusitis diagnosis and management for the clinician: a synopsis of recent con- sensus guidelines. Mayo Clin Proc Mayo Clinic 2011;86(5):427–43. [3] Adams PF, Hendershot GE, Marano MA. Current estimates from the National Health Interview Survey, 1996. 10(200). National Center for Health Statistics Vital Health Stat; 1999. [4] Hoskison E, Daniel M, Rowson JE, et al. Evidence of an increase in the incidence of odontogenic sinusitis over the last decade in the UK. J Laryngol Otol 2012;126:43. [5] Little RE, Long CM, Loehrl TA, Poetker DM. Odontogenic sinusitis: a review of the current literature. Laryngoscope Investig Otolaryngol 2018;3(2):110–4. [6] Nash D, Wald E. Sinusitis. Pediatr Rev 2001;22(4):111–7.
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