European Journal of Radiology 51 (2004) 241–245
Classification of the inferior turbinate bones: a computed tomography study Lokman Uzun a,∗ , Mehmet Birol Ugur a , Ahmet Savranlar b , Kamran Mahmutyazicioglu b , Huseyin Ozdemir b , Levent Bekir Beder a a
Department of Otorhinolaryngology, Head & Neck Surgery, Faculty of Medicine, Zonguldak Karaelmas University, Zonguldak, 67000, Turkey b Department of Radiology, Faculty of Medicine, Zonguldak Karaelmas University, Zonguldak 67000, Turkey Received 24 November 2003; received in revised form 17 February 2004; accepted 19 February 2004
Abstract Background: There are only few reports describing the texture of the inferior turbinate bone in normal and pathologic conditions. In this study, different types of human inferior turbinate bones were classified and radiological features of each type were defined. Methods: The shape, structure and density of the inferior turbinate bones were evaluated using paranasal sinus computed tomography images of 283 patients. The cross-sectional areas of the bony part of the inferior turbinate were measured in bone windows. Results: Human inferior turbinate bones were classified into four groups on the basis of different shape and structure as: Type I, lamellar; Type II, compact; Type III, combined type (compact with spongious component); Type IV, bullous. The distribution was as follows: 352 (62.19%) lamellar, 50 (8.83%) compact, 162 (28.63%) combined, and 2(0.35%) bullous type. Conclusion: Inferior turbinate bone is not in a uniform shape and structure. These diversities should be taken into consideration in radiological and clinical evaluation. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Inferior turbinate bone; Classification; Computed tomography
1. Introduction The lateral nasal wall of the nasal cavity has three conchae or turbinates named superior, middle and inferior according to their relative location. The superior and middle turbinates are part of the ethmoid bone while the inferior turbinate (IT) is a separate bone [1]. The anterior aspects of the middle and inferior turbinates project into the primary airflow pattern observed during inspiration and expiration. At inspiration, up to two-thirds of upper airway resistance is produced by the anterior tip of the inferior turbinate in the region of the internal nasal valve [7]. Even if a little variation of the soft tissue and/or bone of the inferior turbinate occurs, nasal airflow is effected by this alternation. According to the Poiseuille’s law, flow through a tube is proportional to the fourth power of the radius or to the square of the cross-sectional area of the tube [2]. Enlargement of the soft tissue and/or bone of the turbinate may cause ∗ Corresponding author. Tel.: +90-372-261-01-69; fax: +90-372-261-01-55. E-mail address:
[email protected] (L. Uzun).
nasal obstruction through decreasing the cross-sectional area of the nasal airway tube. Although the nasal obstruction due to turbinate hypertrophy is a frequently encountered and well known clinical situation, only a few reports describing the texture of the inferior turbinate bone in normal and pathologic conditions exist [3]. No previous attempts have been made in the literature to classify the IT bone. The purpose of our study was to classify IT bone according to radiological shape and structure. There is no previous comprehensive study in the literature on this subject. The presented classification may help both the otolaryngologist and the radiologist in assessing the role of the inferior turbinate bone in nasal obstruction. Secondly this information can be a useful guide for clinician in determining appropriate treatment strategies.
2. Materials and methods We have retrospectively reviewed digitally recorded computed tomography (CT) images of 283 consecutive patients (99 women, 184 men); 4–90 years old (mean age: 36.4)
0720-048X/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2004.02.013
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in the radiology department of our institution. Images were taken for evaluation of headache of unknown origin. Patients who had undergone previous inferior turbinate surgery were excluded. The CT images were obtained using a spiral CT scanner (Secura; Philips; Best; Holland) at a voltage of 120 kV, current of 200 mA, X-ray beam width of 3 mm. The region extending from the frontal sinus to the sphenoid sinus was helically scanned to obtain contiguous coronal sections at 3 mm-intervals. The window width and level were controlled so as to allow visualization of the mucosal and ostial lesions. In all cases, 3 mm thick contiguous high-resolution coronal CT sections were analyzed with Easy Vision software (version 5.1.1.2 Philips Medical Systems). Boundary of the IT bone was outlined with mouse aiding on bone window (WW:1500, WL:300) CT images and the corresponding area was measured in square millimeters using Easy Vision 5.1.1.2 software (Fig. 1). The measurements were made at levels of anterior, middle and posterior third of the IT. For standardization purposes, anterior measurement was performed on the first image in which the IT bone could be entirely identified. Middle measurement was made on the section in which the uncinate process and maxillary sinus ostium is visualized and posterior measurement, on the last image in which the IT bone could be entirely identified. IT bone density was also measured for the corresponding sections. Human inferior turbinate bones were classified into four groups on the basis of different shape and structure evaluated in tomography sections. IT bone characterized by thin bony lamella was defined as lamellar type (Fig. 2A). IT bones
with bulky and compact bone mass were classified as compact type. (Fig. 2B). IT bones consisting of both compact and spongious components were described as combined type (Fig. 2C). This type presents with a bulky appearance like the compact type but is characterized by a prominent central spongy osseous layer. In the central zone of the turbinate bone the density is relatively lower than the compact periphery. Pneumatization of the turbinate bone is named as bullous type (Fig. 2D). All results were expressed as mean ± standard deviation. The data were analyzed with SPSS software, version 11.0 (copyright© SPSS Inc., 1989–2001). To compare the calculated ratios and bone density values, one-way ANOVA and Tukey multiple comparisons were performed. The probability value of P < 0.05 was considered statistically significant.
3. Results Frequency of inferior turbinate bone types with sex and age distribution were summarized in Table 1. Age and sex distribution of the types showed similar pattern except compact type displayed male preponderance. Lamellar type of IT bone was found to be most common type in this study and its cross-sectional area was the smallest among the all IT bone types. Bullous type IT bone is a rare clinical entity. In this study, only two IT bones in one patient were encountered and were excluded from statistical assessment. Mean values of the cross sectional areas of the IT bone were summarized in Table 2. Bony cross-sectional area was lower in anterior and middle segments in lamellar type compared with combined and compact types (P < 0.001). There was no statistically difference in cross-sectional area between combined and compact types (P > 0.05) (Fig. 3). The values of IT bone density were summarized in Table 3. In lamellar type, the mean values of bone density were lower than combined and compact types in all three segments (P < 0.01). Mean density of combined type was lower than compact type only in the anterior segment (P < 0.05) (Fig. 4).
4. Discussion
Fig. 1. Boundary of the IT bone were outlined by mouse aiding on bone window and the value of the density was marked at left inferior turbinate bone and right maxillary sinus.
The human inferior turbinate consists of a bony part covered by highly vascularized, erectile soft tissue and pseudostratified columnar epithelium. Each of these three components of the inferior turbinate may have distinctive role in turbinate hypertrophy. The anterior part of the inferior turbinate is in the vicinity of the narrowest part of the nose called as isthmus nasi. Changes in the skeleton of the turbinate or increase in the volume of the erectile soft tissue may influence the nasal patency [4]. Poiseuille’s law explains this relation between nasal airflow and turbinate volume. According to this law, a 10% increase in the
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Fig. 2. Different types of inferior turbinate bone: (A) lamellar type; (B) compact type; (C) combined type; and (D) bullous type turbinate bone.
Table 1 Frequency of inferior turbinate bone types with sex and age distribution Type
n
Lamellar Combined Compact Bullous
352 162 50 2
Total
566
Percent (%) (62.19) (28.63) (8.83) (0.35) (100)
Sex (M/F)
Age range
Mean ± S.D.
230/122 104/58 42/8 2/0
4–90 12–69 7–68 34
35.30 ± 16.1 38.76 ± 12.1 35.18 ± 12.5 34
368/198
4–90
36.40 ± 14.73
n: Number of turbinate; S.D.: standard deviation.
Table 2 The cross-sectional area of the inferior turbinate bone in three segments of each type [mean (in mm2 ) ± S.D.] Type
Anterior
Middle
Posterior
Lamellar Compact Combined
7.82 ± 3.57 10.49 ± 6.36 11.03 ± 6.02
14.19 ± 4.38 22.04 ± 11.36 22.9 ± 8.67
8.23 ± 3.01 9.28 ± 4.22 9.82 ± 3.39
S.D.: standard deviation.
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L. Uzun et al. / European Journal of Radiology 51 (2004) 241–245 Table 4 Reported bullous inferior turbinate cases in the literature
Fig. 3. Cross-sectional area of turbinate bone in anterior, middle, and posterior segments for lamellar, compact, and combined types. Bony cross-sectional area was lower in anterior and middle segments in lamellar type compared with combined and compact types (P < 0.001). There was no statistically difference in cross-sectional area between combined and compact types (P > 0.05). Table 3 The values of bone density of inferior turbinate in three segments of lamellar, each type (Mean ± S.D.) Type
Anterior
Middle
Posterior
Lamellar Compact Combined
260.20 ± 97.37 361.03 ± 117.43 318.63 ± 109.38
241.69 ± 70.43 314.62 ± 80.72 295.73 ± 70.65
194.95 ± 63.82 226.07 ± 84.99 230.07 ± 81.99
S.D.: standard deviation.
cross-sectional area of the nasal passage would result in 21% increase in airflow through the nose [2]. Histological and histopathological structure of the mucosa and submucosa of the human inferior turbinate is well documented [1,5]. On the other hand, there is no detailed data concerning shape and structure of the IT bone. Various terms have been used to describe the shape of IT bone such as “two elongated shell-like laminae of bone” [6], “thin semicircular bone” [7], “spongy trabecular appearance” [3], “scroll of bone” [8]. “Bifid” IT, is also described as an additional rare variant of shape [9,10]. But, each of them describes a
Authors
Unilateral
Bilateral
Dawlaty (1999) [11] Dogru et al. (1999) [12] Aydin et al. (2001) [13] Cankaya et al. (2001) [14] Ozcan et al. (2002) [8] Unlu et al. (2002) [15] Braun and Stammberger (2003) [16] Ingram and Richardson (2003) [17] Our case
1 1 1 1 – 2 1 1 –
1 – 1 – 1 – – – 1
Total
8
4
uniform IT bone shape without defining subtypes. Additionally, a few cases of pneumatized IT has been reported in the literature as an exceptional structural variation. Until now, 11 cases have been reported (Table 4) [8,11–17]. We add a new case to them, with bilateral involvement (Fig. 2D). Skeletal or mucosal enlargement of the inferior turbinates is one of the most common causes of nasal airway obstruction. Surgical procedures such as total inferior turbinectomy, partial inferior turbinectomy, turbinoplasty, cryosurgery, submucosal diathermy, laser turbinectomy, and radiofrequency surgery of the inferior turbinate can be performed for relieving nasal obstruction, when medical treatment modalities fail [2,18–22]. Thus, proper treatment is of great importance to patients with nasal obstruction [21–23]. Different surgical methods are applied to the hypertrophic turbinates without objective evaluation and without classification of the type of disturbance as skeletal or mucosal [4]. Indications for turbinate surgery are based on empiric criteria and may result in either extensive, unnecessary or insufficient surgery [4,24]. In the evaluation of patients with nasal obstruction due to IT hypertrophy, relative contribution of the elements of the IT must be thoroughly assessed. In the histopathological evaluation of Berger on compensatory hypertrophic turbinate patients, bone thickness was found to be a significant factor [3]. Accordingly we detected that, the cross-sectional area of the IT bone is relatively large in compact and combined types compared with lamellar type. In the management of such patients surgical intervention should not be focused on merely the mucosal and submucosal layers but the bone must be taken into consideration as well. In selected nasal obstruction cases in patients with compact or combined IT types, bone resection in anterior and middle segments may help in improving the nasal airway passage. In contrast, cases with lamellar type IT, may not benefit too much from such bone resection.
5. Conclusion Fig. 4. Bone density values of turbinate bone in anterior, middle and posterior segments for lamellar, compact, and combined types. In lamellar type, the mean values of bone density were lower than combined and compact types in all three segments (P < 0.01). Mean density of combined type was lower than compact type only in the anterior segment (P < 0.05).
In our series of patients, IT bone was not uniform in shape. Furthermore different varieties in appearance were identified and categorized in four groups. This classification
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