ORIGINAL ARTICLE

Computed Tomographic Analysis of Frontal Sinus Drainage Pathway Variations and Frontal Rhinosinusitis Abdullah Soydan Mahmutoğlu, MD,* Irfan Çelebi, MD,* Burhan Akdana, MD,* Müjdat Bankaoğlu, MD,* Emin Çakmakçi, MD,† Mehmet Mazhar Çelikoyar,‡ and Muzaffer Başak, MD*

Objective: The objective of this study was to radiologically determine frontal sinus drainage pathway variations with respect to superior attachment of uncinate process (SAUP) and their effect on prevalence of frontal rhinosinusitis. Design: This was a retrospective cohort study. Methods: Computed tomography scans of the 919 frontal sinus sides of 460 patients (252 female, 208 male; mean age, 35.1 ± 10.5 years) who were candidates for endoscopic sinus surgery were evaluated retrospectively between August 2012 and January 2013 by 3 radiologists to determine the SAUP types and the presence of frontal rhinosinusitis. Results: The frontal sinus outflow tract was localized medial to the SAUP in 651 frontal sinus sides and lateral to the SAUP in 268 sides. We determined 3 types (types 7, 8, and 9) of SAUP in addition to 6 types defined in literature. The most common type of SAUP was type 3 (n = 332, 36.1%) followed by type 2 (n = 256, 27.8%) and type 7 (n = 160, 17.4%). Of the evaluated sides, 316 (34.3%) had frontal rhinosinusitis. Frontal rhinosinusitis was more common in the sides where the frontal sinus outflow tract was localized medial to the SAUP than those localized lateral (37.2% vs 27.6%, P = 0.006). Conclusions: Endoscopic approach to frontal recess usually requires uncinectomy, and it is necessary to know SAUP to prevent postoperative retained superior portion of the uncinate process. The location of frontal sinus outflow tract on the SAUP affects the prevalence of frontal rhinosinusitis as well. Frontal rhinosinusitis is significantly more common when the frontal sinus outflow tract was localized medial rather than lateral to the SAUP. Level of evidence: 2b. Key Words: Rhinosinusitis, frontal sinus, anatomy, computed tomography (J Craniofac Surg 2015;26: 87–90) From the *Radiology Clinic, Şişli Hamidiye Etfal Training and Research Hospital, Istanbul; †Radiology Clinic, Dr. Sami Ulus Pediatric Training and Research Hospital, Ankara; and ‡Otorhinolaryngology Clinic, Istanbul Cerrahi Hospital, Istanbul, Turkey. Received May 1, 2014. Accepted for publication July 23, 2014. Address correspondence and reprint requests to Abdullah Soydan Mahmutoğlu, MD, Şişli Hamidiye Etfal Eğitim ve Araştirma Hastanesi Halaskargazi Cad. Etfal Sk. 34371 Şişli/Istanbul, Turkey; E-mail: [email protected] The study had no financial support or funding. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001244

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espite recent advances in imaging tools, antibiotic therapy, and surgical techniques, frontal rhinosinusitis remains clinically challenging for physicians because it is the most common source of intracranial complications of infections of all sinuses.1–3 Although incidence of frontal rhinosinusitis complications decreased because of increase in antibiotic use,4 there is still significant degree of morbidity and mortality associated with these complications.1 Therefore, evaluation of risk factors for frontal rhinosinusitis and complications, correct and timely diagnosis, and intervention are vital to avoid and treat chronic frontal rhinosinusitis and its complications. Mucosal inflammatory processes and anatomic variations in the frontal recess are proposed etiologic factors for frontal rhinosinusitis.2 The uncinate process (UP) is the most important structure along with agger nasi cell in frontal recess anatomy and surgery.5 The superior attachment of the UP (SAUP) is a landmark for the location of the frontal sinus drainage pathway, and its variations affect the dimensions of the frontal sinus ostium and the size of the frontal beak.6 There is a variable relationship between the UP and frontal recess, and the direction of frontal recess drainage into the middle meatus is determined by the SAUP.7,8 The anterior portion of the UP forms the lateral wall of the frontal recess when it attaches to the lamina papyracea or the agger nasi; thus, frontal recess drainage channels directly into the middle meatus, and the ethmoid infundibulum ends as a blind-ending recess, which is called the recessus terminalis. The UP forms the medial wall of the frontal recess when it attaches to the skull base or the middle turbinate, and in this case, secretions are directed into the ethmoid infundibulum prior to passage into the middle meatus. Medially displaced UP is one of the most common causes of obstruction at the frontal recess level, in patients without previous surgery. This happens when the UP is displaced medially by the disease in the recessus terminalis causing it to lie close to or even against the middle turbinate. Sometimes, there can be a fusion between the UP and middle turbinate. Of the patients undergoing revision functional endoscopic sinus surgery, 37% were reported to have retained UP as surgeons occasionally ignore the SAUP. When a medialized UP is left behind during endoscopic sinus surgery, the frontal recess will not surprisingly have a tendency to restenose after the surgery. The UP is best identified on coronal computed tomography (CT) images, which allow to clearly demonstrate its relationship to the frontal recess and the surrounding structures.7,8 There are limited studies in the literature evaluating the effects of the frontal sinus drainage pathway and frontal recess anatomy on the presence of frontal rhinosinusitis.9–12 These otorhinolaryngologic studies reported conflicting results on the relation between presence of frontal cells and frontal rhinosinusitis.7,8 In a CT-assisted anatomical and clinical study, Turgut et al11 evaluated 486 frontal sinus sides of 243 patients and reported significantly higher rate of frontal rhinosinusitis when the frontal sinus outflow tract is located medial to the superior attachment.

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FIGURE 1. Symmetrical illustrations (A, C) and CT images (B, D) of types 1/2, 3, and 5 SAUP (arrows). The area of SAUP is lamina papyracea in types 1/2; lamina papyracea and the junction of the middle turbinate with cribriform plate in type 3; skull base in type 5. u Indicates UP.

In this study, we aimed to investigate the SAUP radiologically and determine frontal sinus drainage pathway variations with respect to these types and the effect of these variations on the prevalence on frontal rhinosinusitis.

defined by Landsberg and Friedman,8 and following studies in literature, we defined 9 SAUP types (types 7, 8, and 9) in the present study. The types of SAUP in our study were as follows: type 1/2: lamina papyracea, type 3: lamina papyracea and the junction of the middle turbinate with cribriform plate, type 4: the junction of the middle turbinate with cribriform plate, type 5: skull base, type 6: middle turbinate, type 7: lamina papyracea and base of skull, type 8: lamina papyracea and interfrontal septum, and type 9: lamina papyracea and middle turbinate (Figs. 1–4). Frontal sinus outflow tract localization was classified as medial (to the middle meatus) or lateral (to ethmoid infundibulum) with respect to the SAUP.

Statistical Analysis Study data were summarized using descriptive statistics (mean, SD, frequency, percentage). Categorical data of study groups were compared with χ2 test. Statistical analyses were performed using a computer software (Statistical Package for Social Sciences, version 20.0; SPSS Inc, Chicago, IL). The level of statistical significance was set to P < 0.05.

MATERIALS AND METHODS Study Design and Patients This was a retrospective, descriptive study that included chronic rhinosinusitis patients who were resistant to medical therapy and candidates for endoscopic sinus surgery and who were given treatment and under follow-up between August 2012 and January 2013. The exclusion criteria were as follows: prior sinus surgery, massive nasal polyposis, invasive fungal rhinosinusitis, tumoral disease, and trauma. The hospital files of the patients were reviewed, and the basic demographic and clinical data were recorded. The study was approved by ınstitutional review board and conducted in accordance with the ethical guidelines of the Helsinki Declaration. The informed consent was waived for the retrospective nature of the study.

Radiological Evaluation of Frontal Sinuses Multidetector CT scans of the frontal sinuses of patients were evaluated separately on the coronal reformatted images to determine the superior attachment type of UP and the presence of frontal rhinosinusitis on each side by magnification and appropriate window setting. Multidetector CT (Philips Brilliance ICT 256; Medical Systems, Best, the Netherlands) was performed without using intravenous contrast material. The CT acquisition parameters consisted of a 251-mAs tube current, 120 kV, 64  0.625 detector collimation, 0.5-second rotation time, table speed of 1 mm/rotation (pitch, 0.391), 0.67-mm slice thickness, 4.9-second scan time, field of view of 294, and matrix of 1024  1024. Nasal vasoconstrictors were not administered. All patients were referred for CT owing to a clinical symptom presumably referable to the sinonasal region. The other surrounding structures (eg, agger nasi cell, sinus terminalis, bulla ethmoidalis, types of frontal recess cells) except UP and patient histories were not taken into account. The scans were interpreted retrospectively by 3 expert radiologists, and any differences in opinions were resolved by consensus. The left and right sides of each of the frontal sinuses were assessed separately for the presence of mucosal disease. This disease was evaluated as either being present or absent. The criteria for frontal rhinosinusitis were as follows: opacification, air-fluid level, and/or mucosal thickening greater than 3 mm in the frontal sinus. Although 6 types of SAUP were

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RESULTS Study Population A total of 919 frontal sinus sides of 460 patients (252 female [54.8%], 208 male [45.2%]; mean age, 35.1 ± 10.5 years; age range, 8–68 years) were evaluated in this study. Of these cases, 1 had 1 frontal sinus (unilateral aplasia). The frontal sinus outflow tract was localized medial to the SAUP in 651 frontal sinus sides and lateral to the SAUP in 268 frontal sinus sides (Fig. 5). The most common type of SAUP was type 3 (n = 332, 36.1%) followed by type 2 (n = 256, 27.8%) and type 7 (n = 160, 17.4%) (Table 1).

Frontal Rhinosinusitis Of the evaluated sides, 316 (34.3%) were diagnosed as frontal rhinosinusitis. Frontal rhinosinusitis was more common among the sides where the frontal sinus outflow tract was localized medial to the SAUP than those localized lateral to the SAUP (37.2% vs 27.6%, P = 0.006). Among the SAUP types, frontal rhinosinusitis was most frequently detected in types 6 and 2. Almost half of the patients with type 2 attachment had frontal rhinosinusitis (Table 2).

DISCUSSION Among all the paranasal sinuses, the frontal sinus has the most complex and variable drainage pathway.13 These variations and complexity produce a challenge for the radiologist; however,

FIGURE 2. Symmetrical illustrations (A, C) and CT images (B, D) of types 3, 4, and 5 SAUP (arrows). The area of SAUP is lamina papyracea and the junction of the middle turbinate with cribriform plate in type 3; the junction of the middle turbinate with cribriform plate in type 4; skull base in type 5. u Indicates UP.

© 2014 Mutaz B. Habal, MD

Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

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FIGURE 3. Symmetrical illustrations (A, C) and CT images (B, D) of types 6 and 7 SAUP (arrows). The area of SAUP is middle turbinate in type 6; lamina papyracea and base of skull in type 7. u Indicates UP.

recent use of multiplanar CT reformations provided clearer anatomic view of the nasofrontal region and evaluation of diversities of frontal sinus drainage pathways.6 These images improved depiction and anatomy of the frontal sinus and recess, which is particularly important for defining appropriate surgical technique.14 Radiological display of frontal sinus drainage pathway for subjects with chronic rhinosinusitis is important for both evaluation of etiology of rhinosinusitis and planning of surgery. The course of UP is also of great importance for preoperative planning. A surgeon needs to have 2 situations distinguished15: (1) ıf the UP is attached to the lateral nasal wall, the lamina papyracea, or the agger nasi cells, the frontal recess is reached between the UP and bulla lamella; and (2) ıf the UP is attached cranially to the anterior skull base or middle turbinate, it blocks the access to the frontal recess. In this situation, the frontal recess is opened by resection of the UP. Under such circumstances, care must be taken by the operating surgeon not to apply undue force while performing uncinectomy, as this may lead to cerebrospinal fluid rhinorrhea or damage to the anterior cranial fossa and orbital contents. In the current retrospective reconstructed volumetric CT survey of 919 frontal sinus sides of 460 chronic rhinosinusitis patients who were resistant to medical therapy and candidates for endoscopic sinus surgery, we found that frontal rhinosinusitis was present in 34.3% of evaluated sides. Frontal rhinosinusitis was more common among the sides where the frontal sinus outflow tract was localized medial to the SAUP (651 sides) than those localized lateral (268 sides) to the SAUP. There are limited studies in the literature evaluating the relation between the frontal rhinosinusitis and frontal recess anatomy.9–12 Lien et al9 reported that frontal rhinosinusitis is associated with the presence of suprabullar cells, supraorbital ethmoid cells, frontal bullar cells, and recessus terminalis. On the other hand, del Gaudio et al10 found no relation between presence of frontal cells and frontal rhinosinusitis. Similar to the findings in our study, Turgut et al11 found frontal sinusitis in 35% of 361 sides. They also

CT of Frontal Sinus Drainage Pathways

FIGURE 5. Computed tomography images (figures on right side) and symmetrical illustrations (figures on left side) show that the frontal sinus (F) outflow tract (arrows) was localized lateral to the SAUP in 268 frontal sinus sides (A, B) and medial to the SAUP in 651 frontal sinus sides (C, D).

reported similar rates of frontal rhinosinusitis for frontal sinus outflow tract located medial and lateral to the SAUP (41% and 23%, respectively; P < 0.001). These rates were also comparable to the rates in our study, which were 37.2% and 27.6%, respectively. In the previous studies, up to 6 types of SAUP were recognized.11–17 Landsberg and Friedman8 defined 6 types of the SAUP. Ercan et al16 and Turgut et al11 modified this classification by combining types 1 and 2. Liu et al17 further modified the classification of Landsberg and Friedman by combining types 4 and 6. In this CT evaluation study of 264 sides of 132 patients from Taiwan, Liu et al17 reported that the most common superior attachment side of the UP is the lamina papyracea (70.4%) followed by middle turbinate (10.2%), lamina papyracea and skull base (7.6%), and skull base (6.1%). The superior attachment side of the UP also shows variations with respect to ethnicity.17 Although the most common superior attachment side of the UP is lamina papyracea in studies from different ethnic groups, its rate ranges widely between 33% and 70.4%.11–17 In a study of 361 subjects from Turkey, Ercan et al16 reported that the superior attachment side of the UP is lamina papyracea in 62.6% of the subjects, middle turbinate in 19.9% of the subjects, and skull base in 14.4% of the subjects. In our study, different from the previous reports, we detected 9 types of SAUP. In the current study, the most common type of SAUP was type 3 (36.1%), where the SAUP is attached both to lamina papyracea and the junction of the middle turbinate with cribriform plate. The second and third most common types of SAUP were type 2 (27.8%), where SAUP is attached to lamina papyracea, and type 7 (17.4%), where it is attached both to lamina papyracea and base of skull. As shown by previous studies,14,18–20 we showed that reformatted CT imaging is useful in the radiological evaluation of

TABLE 1. Localization of Frontal Sinus Outflow Tract and SAUP Types of Frontal Sinus Sides Evaluated Frontal Sinus Sides, % n = 919

FIGURE 4. Symmetrical illustrations (A, C) and CT images (B, D) of types 8 and 9 SAUP (arrows). The area of SAUP is lamina papyracea and interfrontal septum in type 8; lamina papyracea and middle turbinate in type 9. u Indicates UP.

Localization of frontal sinus outflow tract Medial to the SAUP (group 1) Lateral to the SAUP (group 2) Attachment types Types 1/2 Type 3 Type 4 Type 5 Type 6 Type 7

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651 (70.8%) 268 (29.1%) 260 332 38 8 6 160

(28.2%) (36.1%) (4.1%) (0.9%) (0.7%) (17.4%)

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TABLE 2. Frontal Sinusitis Prevalence in SAUP Types SAUP Types Types 1/2 Type 3

Type 4 Type Type Type Type Type

5 6 7 8 9

Attachments Area

Frontal Sinusitis, no. sides (%)

Lamina papyracea Lamina papyracea and the juction of the middle turbinate with cribriform plate The junction of the middle turbinate with cribriform plate Skull base Middle turbinate Lamina papyracea and base of skull Lamina papyracea interfrontal septum Lamina papyracea and middle turbinate

104 (40.6%) 124 (37.3%)

5 (13.2%) 0 3 44 12 24

(0.0%) (50.0%) (27.5%) (23.1%) (37.5%)

frontal sinus outflow tract. In all coronal images evaluated, we were able to depict the SAUP. Thus, coronal plane for UP courses and sagittal plane for frontoethmoid recess are informative for surgeons particularly if evaluated by experienced radiologists. The study population in this study was formed of the individuals who were referred to CT because of a specific symptom most likely to be related to a probable disease of sinonasal region. Hence, the statistical inference of outcomes of this study can be related only to a symptomatic group of people, and no conclusions about general population can be made.

CONCLUSIONS The location of frontal sinus outflow tract on the SAUP is among the factors affecting the presence of frontal rhinosinusitis. The insertion of frontal sinus outflow tract to the SAUP is medial more than lateral. Frontal rhinosinusitis is significantly more common when the frontal sinus outflow tract was localized medial rather than lateral to the SAUP. The variations in nasofrontal anatomy and location of frontal sinus outflow tract affect the development of frontal rhinosinusitis and are important for preoperative evaluation of patients. Pathophysiological basis and clinical implications of these findings need further studies.

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© 2014 Mutaz B. Habal, MD

Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

Computed tomographic analysis of frontal sinus drainage pathway variations and frontal rhinosinusitis.

The objective of this study was to radiologically determine frontal sinus drainage pathway variations with respect to superior attachment of uncinate ...
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