A sthma and sinusitis are inflammatory diseases of respiratory epithehal tissue. and the association of asthma with sinusitis has long been known.

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Scott E. Crater1 Edward J. Peters1 C. Douglas Phillips2 Thomas A. E. Platts-M111s1 Received June 29, 1998; accepted after revision January4, 1999.

1 Scott E. Crater1 Edward J. Peters1 C. Douglas Phillips2 Thomas A. E. Platts-M111s1 Received June 29, 1998; accepted after revision January4, Supported by National Institutes of Health (NlHl grant AI and NIH Asthma Center grant U19-Al Asthma & Allergic Diseases Center, University of Virginia Health Sciences Center, Box 225, Charlottesville, VA Address correspondence to S. E. Crater. 2Department of Radiology, University of Virginia, Charlottesville, VA AJI9 1999:173: X/99/ American Roentgen Ray Society Prospective Analysis of CT of the Sinuses in Acute Asthma OBJECTIVE. Asthma and sinusitis are both inflammatory diseases of the respiratory epithelium, but to our knowledge no prospective analyses of CT of the sinuses in patients with acute asthma have been performed. The purpose of this study was to investigate the type and extent of abnormalities found on CT of the sinuses in patients with acute asthma. SUBJECTS AND METHODS. Sixty-five patients with acute asthma and 62 age-. race-, and sex-matched control subjects were enrolled in the emergency department. Limited coronal sinus CT was performed and scans were interpreted by a radiologist who was unaware of the patient s clinical condition. Scans were analyzed for the presence of mucosal thickening in the sinuses. ostiomeatal complexes. and nasal cavities. Scans were also assigned a CT score for total mucosal thickening. A CT score of 12 or more points indicated extensive disease. RESULTS. Mucosal thickening in the nasal passages (p <.001 ). ostiomeatal complexes (j <.05), and ethmoidal (p <.05) and sphenoidal sinuses (p <.05) was associated with acute asthma. but maxillary mucosal thickening was not (p =.44). CT scores differed significantly between asthmatic patients (7.7 ± 0.8 points) and control subjects (4.1 ± 0.4 points) (p <.001). Nineteen of the 65 asthmatic patients had extensive disease compared with two of the 62 control subjects (p <.001 ). Thirteen asthmatic patients with extensive disease underwent follow-up CT 5 months later, and I I of the 13 patients showed improvement in CT score without having undergone specific therapy for sinusitis. CONCLUSION. Mucosal thickening in the nasal passages and sphenoidal. ethmoidal. and frontal sinuses is more common in patients with acute asthma than in control subjects. However. maxillary sinus mucosal thickening is no more common in asthmatic patients than in control subjects. A sthma and sinusitis are inflammatory diseases of respiratory epithehal tissue. and the association of asthma with sinusitis has long been known. In I 925, Gottleib [ 11observed that 3 1 of a series of I I 7 asthmatic patients complained of sinus symptoms. Since then. several studies have examined the relationship between asthma and sinusitis using conventional sinus radiographs. Estimates of the incidence of sinusitis in asthmatic patients based on conventional sinus radiographs range from 3 1 % to 87% [2-41. Such variability reflects the difficulty of accurately diagnosing sinus disease using conventional radiographs. Although CT offers superior sensitivity in detecting sinus abnormalities, no study has used sinus CT to assess prospectively the extent of disease in acute asthmatic patients compared with nonasthmatic control subjects [5-7]. The purpose of this study was to document the type and extent of sinus abnormalities detected by CT in patients with acute asthma compared with random control subjects. CT scans were evaluated fbr both specific anatomic features (i.e.. polypoid mucosa and ostiomeatal complex occlusion) and total mucosal thickening in the paranasal sinuses and nasal passages. Subjects and Methods Subjects Sixty-nine acute asthmatic patients and 70 age-. race-. and sex-matched control subjects between the ages of I 8 and 50 years were recruited in the emergency department of a university hospital between August 1997 and March Subjects were enrolled under a protocol approved by the human investigations committee. All subjects provided informed consent befre enrollment. AJR:173, July

Crater et al. Control subjects were enrolled at random from the emergency department during the same period as the asthmatic patients.

No exclusions were made on the basis of either cold or sinusitis symptoms or a history of asthma or sinus surgery.

Five control subjects presented with symptoms consistent with an upper respiratory infection. One control subject complained of rhinitis; two, of a sore throat: and two, of an earache.

2 Crater et al. Control subjects were enrolled at random from the emergency department during the same period as the asthmatic patients. The exclusion criterion for control subjects was acute breathlessness at the time of the study. No exclusions were made on the basis of either cold or sinusitis symptoms or a history of asthma or sinus surgery. The most common complaints among control subjects were orthopedic injuries (,z = 29) followed by lacerations (ii = 10) and toothaches (n = 10). Five control subjects presented with symptoms consistent with an upper respiratory infection. One control subject complained of rhinitis; two, of a sore throat: and two, of an earache. The remaining 26 had a variety of complaints ranging from an animal bite to syncope. Eight control subjects reported a history of asthma, but none were wheezing at the time of the study. In addition, two control subjects and three asthmatic patients had undergone functional endoscopic sinus surgery in the past. For the purposes of this study. asthma was defined as acute breathlessness, wheezing on physical examination, and a history of similar episodes. All subjects were judged to need treatment for asthma by the emergency department physician. and all subjects received nebulized albuterol (l U). The race of study subjects was noted because asthma morbidity and mortality are markedly higher among blacks than whites. Spirometry Technique All subjects performed three vital capacity maneuvers into a portable spirometer (Renaissance model; Puritan-Bennett, Wilmington, MA). according to the American Thoracic Society guidelines [8], before enrollment. CT Technique After enrollment in the emergency department, subjects were scheduled to return for outpatient CT. Seven asthmatic patients were admitted and scanned as inpatients. The CT protocol was a modification of the method originally described by Phillips [9] and has previously been described. All subjects were scanned after administration of a nasal decongestant and clearing of the nose. CT Evaluation and Scoring Cr scans were interpreted by a neuroradiologist who was unaware of the subject s clinical condition. CT scans were evaluated using a previously published scoring system [10, 1 1]. Maximal amount of single-wall mucosal thickening in millimeters was measured in all the paranasal sinuses, and a range of from 0 to 3 points was assigned for each sinus (Table 1). For evaluating the ostiomeatal complexes and nasal passages, a score of 0 was given for no disease; 1, for mild disease; 2, for moderate or scattered disease; and 3, for severe mucosal disease. To quantify total mucosal thickening, the scores for the individual sinuses, nasal passages. and ostiomeatal complexes were summed. The range of possible scores was from 0 to 30 points. As in earlier studies using this scoring system, a score of 12 or more points indicated extensive disease [1 1]. Attention was paid to specific features including polypoid-appearing (focally thickened) mucosa, air-fluid levels, and bony changes consistent with chronic sinusitis. Finally, the bony architecture of the sinuses including the agger nasi cells, HaIler cells (infraorbital air cells), concha bullosa, and deviated septa was noted. These abnormal bony structures result in apposition of healthy mucosal surfaces, thus impeding normal mucociliary transport. Altered mucociliary transport may lead to stagnation of mucous, which can cause postobstructive sinusitis [ 12]. Statistics A statistical program (True Epistat; Epistat Services, Richardson, TX) was used for data analysis. The prevalence of specific sinus CT features in asthmatic patients was compared with that in control subjects using chi-square analysis. The CT score values are presented as a mean ± SEM. Mean Cr scores in asthmatic patients and control subjects were compared using the Mann-Whitney test for nonparametric data. Results The demographics of the study population are presented in Table 2. Mean forced expiratot) volume in 1 sec was 55% of predicted in asthmatic patients versus 103% of predicted in control subjects (p <.0001). The mean duration of asthma symptoms was 14.7 years. Before presentation to the emergency department, 27 (42%) of the 65 asthmatic patients were using Scoring System for di. aes Note-V limeters. Mod = moderate. a Maximum total score for mucosal thickening is 30 points. inhaled steroids, seven (I 1%) of the 65 were using oral steroids, and three (5%) of the 65 were using steroid nasal sprays for treatment of allergic rhinitis. None were taking antibiotics for treatment of bacterial sinusitis. Only three (5%) of the 65 asthmatic patients had been referred to an otolaryngologist for evaluation of sinus disease in the past. compared with two (3%) of the 65 control subjects. Sixty-five of 69 asthmatic patients and 62 of the 70 control subjects returned for CT, and mean CT scores of asthmatic patients and control subjects are presented in Table 2. Asthmatic patients underwent scanning 0-9 days (mean, 3.4 ± 0.4 days) after presentation to the emergency department. The emergency department physician treated the study subjects for acute asthma, but no subjects received topical nasal steroids, decongestants, or antihistamines for treatment of sinus symptoms in the emergency department. Specific anatomic features on CT were associated with acute asthma exacerbations: mucosal thickening of the nasal passages. the ostiomeatal complexes, and the sphenoidal and ethmoidal sinuses (Table 3). More severe mucosal thickening (i.e., 6 mm) in these areas was also associated with acute asthma (Table 4). On the other hand, because the incidence of maxillary sinus abnormalities was the same in asthmatic patients (65%) and control subjects (73%), mucosal thickening in the maxillary sinuses was not associated with asthma (Table 3). Polypoid-appearing (focally thickened) tissue anywhere on the.haracterlstlcs Of ACute..sthmadc Patients and :ontrol Subjects at bbecause ofthe smaller size ofthe ethmoidal sinuses rel- versus asthmatic patients was performed usin9 the Mannative to the other sinuses, the same number of points was Whitneytestfornonparametric data; p< 001. given for lesser degrees ofthickening. avalues are expressed as a mean ± SEM. 128 AJR:173, July 1999

CT of the Sinuses in Acute Asthma scan was more common in asthmatic patients, but this finding did not reach statistical significance (Table 3).

This patient had extensive sinus disease Chi-square analysis: p<.001. bchi.square analysis: p <.05. CpOlypOjd mucosa refers to the presence of polypoid-appearing tissue anywhere on the scan.

Patient presented with 2-week history of wheezing and rhinorrhea and 10- year history of asthma and sinus problems. Coronal CT scan shows involvement of all paranasal sinuses. CT score = 25 points.

3 CT of the Sinuses in Acute Asthma scan was more common in asthmatic patients, but this finding did not reach statistical significance (Table 3). One asthmatic patient reported a history of aspirin sensitivity: 1 year earlier she had received aspirin at an outside hospital and subsequently required intubation for respiratory distress. This patient had extensive sinus disease Chi-square analysis: p<.001. bchi.square analysis: p <.05. CpOlypOjd mucosa refers to the presence of polypoid-appearing tissue anywhere on the scan. These lesions may represent either true polyps or mucous-retention cysts. Fig year-old black woman with Samter s syndrome (asthma, nasal polyps, aspirin sensitivity). Patient presented with 2-week history of wheezing and rhinorrhea and 10- year history of asthma and sinus problems. Coronal CT scan shows involvement of all paranasal sinuses. CT score = 25 points. Scores for total mucosal thickening in the asthmatic patients ranged from 0 to 25 points of a possible 30 points (Figs. 2 and 3); scores for control subjects ranged from 0 to 14 points. As in previous studies using this system, a score of I 2 or more points indicated extensive sinus disease [10, 1 1j. Extensive disease corre- with polypoid features (Fig. 1). lated significantly with acute asthma by chi-. d Abnormalities Found on CT ofthe Sinuses ofasthmatic Patlnts and Conol Subjects square analysis; 19 of the 65 asthmatic patients had extensive disease, compared with two of the 62 control subjects (p <.001). Follow-up sinus CT scores were obtained for 13 of 19 individuals with extensive sinus disease. Partial to near-complete improvement was seen in I I of the 13 asthmatic patients during a 5-month period, although none of the I I subjects who improved had received any specific therapy for sinus disease (Figs. 4 and 5). Bony thickening suggestive of chronic sinusitis was observed in only three of the 65 asthmatic patients and one of the 62 control subjects (p =.64). Other structural abnormalities commonly associated with sinusitis such as HaIler cells, agger nasi cells, concha bullosa, and deviated septa were not significantly different between asthmatic patients and control subjects. Discussion This study, to our knowledge. is the first controlled. prospective analysis of sinus abnormalities detected by CT in an unselected population of patients with acute asthma and control subjects. Earlier reports of CT findings in asthmatic patients with sinus disease were drawn from retrospective analyses of highly selected populations referred for surgical treatment of chronic sinusitis and not acute asthma [ 10, 1 11.The available studies of sinus abnormalities in patients with acute asthma used conventional sinus radiographs [2-4]. These studies are flawed because conventional sinus radiographs are much less sensitive than CT scans for detecting sinus abnormalities [5-7J. In fact, Laz.ar et al. [61 documented an error rate of more than 35% when the accuracy of conventional radiographs was compared with that of sinus CT for diagnosing chronic sinusitis. Also, few of the earlier studies compared asthmatic patients with a control population, despite the CT findings of Havas et al. I 131 showing abnormalities in one or more of the paranasal sinuses in more than 40% of control subjects without a history of sinus disease. Like the report by Havas et al. [13]. our study shows a high incidence of sinus mucosal thickening in a random control population. As in the Havas et al. study, the control subjects in our study were randomly selected. No effort was made to exclude subjects with preexisting sinus disease, and five (8%) of the 62 control subjects had some upper respiratory symptoms. We believe that this group of unselected control subjects is representative of the general population at large and that some degree of mucosal thickening in the paranasal sinuses is AJR:173, July

(43/65 [66%]). Some degree of maxillary mucosal thickening may be unrelated to any pathologic process because this finding was so common and was not associated with any particular morbidity.

acute asthma. Practitioners should be aware, however, that maxillary sinus mucosal thickening alone may be clinically insignificant.

Historically, chronic infection by organisms such as Moraxella catarrhaiis and Haemophilus influenzae has been targeted as the cause of sinusitis.

4 Crater et al. a common finding. This hypothesis is especially true for the maxillary sinuses, because the incidence of maxillary mucosal thickening was at least as high in control subjects (45/62 [73%]) as in asthmatic patients (43/65 [66%]). Some degree of maxillary mucosal thickening may be unrelated to any pathologic process because this finding was so common and was not associated with any particular morbidity. It is currently not possible to explain the predominance of sinus disease in the ostiomeatal complexes and sphenoidal and ethmoidal sinuses as opposed to the maxillary sinuses among patients with acute asthma. Practitioners should be aware, however, that maxillary sinus mucosal thickening alone may be clinically insignificant. Therefore, it may be problematic in patients with suspected sinusitis to rely on conventional radiographs, which afford images of the maxillary sinuses and little else. Historically, chronic infection by organisms such as Moraxella catarrhaiis and Haemophilus influenzae has been targeted as the cause of sinusitis. However, abnormalities revealed on CT in this study may have been associated with factors other than bacterial infection of the paranasal sinuses. Community-acquired rhinovinis infection is a common asthma trigger that has been shown to affect the appearance of the nasal passages and paranasal sinuses on a CT scan [14, 15]. Alternatively, acute exposure to high levels of aeroallergens could possibly produce widespread mucosal swelling found on a CT scan. Although the investigations required to support these assertions are beyond the scope of this study, it is significant that 1 1 of the 13 subjects Fig. 5.-Scattergram shows that CT scores in subjects with extensive sinus disease (CT score, 12 points [dotted/mel) improved from mean of 17.5 ± 1.0 points at initial presentation (left) to 11.1 ± 1.5 points at follow-up (right), indicating significant improvement (Mann-Whitney test, p =.003). Fig year-old black woman with 5-day history of wheezing, headache, and rhinorrhea. Coronal CT scan shows absence of mucosal thickening in any paranasal sinuses. CT score = 0 points. Fig year-old white woman with 3-day history of wheezing, rhinorrhea, and frontal headache. Coronal CT scan shows mucosal thickening in both ostiomeatal complexes, mucosal thickening in antenor ethmoidal sinuses, and mild mucosal thickening in maxillary sinuses (not evident on this cut). CT score = 10 points. Fig year-old black woman with acute asthma. A, Coronal CT scan obtained at presentation to emergency department shows severe mucosal thickening in maxillary sinuses. Other cuts revealed severe thickening in anterior ethmoidal sinuses, sphenoidal sinus, and nasal cavity. CT score = 18 points. B, Follow-up coronal CT scan obtained 136 days later, with resolution of asthma symptoms, shows only mild thickening in left ostiomeatal complex (not evident on this cut) and maxillary sinus. CT score = 3 points O U) 18 C (l)ie U) 14 I ! 0 C., I- 06 Initial CT Follow-Up CT 130 AJR:173, July 1999

CT of the Sinuses in Acute Asthma with Widespread mucosal thickening (score, 12 points) showed improvement on follow-up CT without receiving additional specific therapy for sinusitis (Figs. 4 and 5).

5 CT of the Sinuses in Acute Asthma with Widespread mucosal thickening (score, 12 points) showed improvement on follow-up CT without receiving additional specific therapy for sinusitis (Figs. 4 and 5). Ofthe two subjects with no improvement shown on CT, one had been seen in the emergency department for acute asthma the day before the follow-up scan was obtained. These results suggest that sinus abnormalities in asthmatic patients may be an episodic part of the illness, with mucosal inflammation that waxes and wanes with respiratory symptoms. Thus, the pathogenesis of the observed mucosal thickening may be related to other inflammatory conditions, rhinovirus infection, or allergic rhinitis [10, 15]. Additional investigations will be required to confirm this hypothesis. This study is the first to show an association between extensive sinus mucosal thickening detected by CT and acute asthma. The identification of transient, acute sinus changes seen on CT differs from the previously published association between chronic sinusitis and asthma [10, 11]. However, the subjects in the earlier studies were selected from a pool of older patients referred to an otolaryngologist for evaluation of chronic severe sinus symptoms, and this group may not be typical ofmost adults with asthma. Furthermore, only one of the asthmatic patients in our study met the criteria for Samter s syndrome, which consists of severe asthma, chronic sinusitis with nasal polyposis, and sensitivity to aspirin (or related compounds) [ 16, 17]. These classic criteria have long been associated with severe adult-onset asthma; however, the mucosal changes seen on CT in this study are mostly unrelated to Samter s syndrome. because only one subject met the criteria (Fig. I). Even when polypoid tissue was identified using CT in the subjects in this study, the incidence of polypoid-appearing mucosa was not significantly higher in the a.sthmatic patients than in the control subjects (Table 3). This finding suggests that polypoid-appearing tissue seen on CT may be unrelated to asthma pathogenesis in most patients. However, the radiologist cannot say with certainty that polypoid-appearing tissue on CT is a polyp, because polyps are a histologic diagnosis. This study shows extensive sinus disease (CT score, 12 points) in almost one third of patients presenting with acute exacerbations of asthma. The sinus abnormalities found in the study subjects probably reflect either an acute or acute-on-chronic process rather than a purely chronic process, because in the patients who underwent CT a second time, the disease appeared to have abated significantly with time. If imaging of the paranasal sinuses is planned for patients with acute asthma, CT should be the preferred technique because CT can detect dinically significant disease in the nasal passages, ostiomeatal complex, and ethmoidal and sphenoidal sinuses. Disease in these areas, not in the maxillary sinuses, appears to be related to the pathogenesis of acute asthma. Unfortunately, CT scans cannot show what proportion of the disease is attributable to allergic inflammation, bacterial infection, or acute viral infection; additional clinical and laboratory investigations that are beyond the scope of this study may be required to identify the cause of sinus abnormalities in patients with acute asthma. References 1. Gouleib Mi. Relation ofintranasal disease in the pmduction ofbronchial asthma JAMA 1925;85:l Zimmerman B, Stringer D, Feanny S. et at. Prevalence ofabnormalities found by sinus x-rays in childhood asthma: lack ofrelation to severity of asthma. JAllergy Clin Immunol 19$7;80: Schwartz HJ, Thompson is, Sher TH, Ross Ri. Occult sinus abnormalities in the asthmatic patient.arrh Intern Med 1987:147: Rossi OVI, Pirila 1, Laitinen I, Huhti E. Sinus aspirates and radiographic abnormalities in severe attacks of asthma. In: Arch Allergy Immuno! 1994: 103: Burke IF, Guertler AT, Timmons JH. Comparison of sinus x-rays with computed tomograpy scans in acute sinusitis. AcadEmerg Med 1994:1: Lazar RH, Younis RT, Parvey LS. Comparison of plain radiographs. coronal CT, and intraoperative findings in children with chronic sinusitis. 0:0- laryngol HeadNeck Surg 1992:107: Zinreich SI. Imaging ofchronic sinusitis in adults: x-ray. computed tomography, and magnetic resonance imaging. J Allergy Clin Immunol 1992:90: Anonymous. Standardization of spirometry: 1987 update-statement of the American Thoracic Society. Am Rev Respir Dis 1987:136: Phillips CD. Current status and new developments in techniques for imaging the nose and sinuses. 0:o1ar,ngo! Clin NorthAm 1997:30: Hoover GE, Newman Li, Platts-Mills TAE, Phillips CD. Gross CW, Wheatley LM. Chronic sinusitis: risk factors for extensive disease. J Allergy C/in Immunol 1997:100: Newman U, Plans-Mills TAE, Phillips CD. Hazen KC. Gross CW. Chronic sinusitis: relationship of computed tomographic findings to allergy. asthma, and eosinophila. JAMA 1994:271: Evans KL. Diagnosis and management of sinusitis. BMJ 1994:309: Havas TE, Motbey ia. Gullane PJ. Prevalence of incidental abnormalities on computed tomographic scans of the paranasal sinuses. Arch 0:olaryngol HeadNeck Surg 1988:114: Johnston SL, Pattemore PK, Sanderson G, et al. A community study of the role of viral infections in exacerbations ofasthma in 9-11 year old children. BMJ 1995;3l0: Gwaltney IM, Phillips CD, Miller RD. Riker DK. Computed tomographic study of the common cold. N Engi J Med 1994;330: Samter M, Beers RF. Intolerance to aspirin: clinical studies and consideration of its pathogenesis. Ann Intern Med 1968;68: Zeitz Hi. Bronchial asthma, nasal polyps. and aspirin sensitivity: Samter s syndrome. C/in Chest Med 1988:9: AJR:173, July

Sinusitis in Thai Asthmatic Children

ORIGINAL ARTICLES Sinusitis in Thai Asthmatic Children Nualanong Visitsuntorn 1 Kampanad Balankura 1 Sriprapai Keorochana 2 Suprida Habanananda Pakit Vlchyanond 1 and Montri Tuchlnda 1 Sinusitis has been