Neuroradiology/Head and Neck Imaging Original Research Shpilberg et al. CT of Paranasal Sinuses and Nasal Cavity Neuroradiology/Head and Neck Imaging Original Research Katya A. Shpilberg 1 Simon C. Daniel 1 Amish H. Doshi 1 William Lawson 2 Peter M. Som 1 Shpilberg KA, Daniel SC, Doshi AH, Lawson W, Som PM Keywords: anatomic variants, CT, functional endoscopic sinus surgery, paranasal sinuses, sinusitis DOI:10.2214/AJR.14.13762 Received September 5, 2014; accepted after revision October 14, 2014. 1 Department of Radiology, Icahn School of Medicine at Mount Sinai, One Gustave L Levy Pl, New York, NY 10029-6574. Address correspondence to K. A. Shpilberg (katyats@gmail.com). 2 Department of Otolaryngology, Icahn School of Medicine at Mount Sinai, New York, NY. This article is available for credit. AJR 2015; 204:1255 1260 0361 803X/15/2046 1255 American Roentgen Ray Society CT of Anatomic Variants of the Paranasal Sinuses and Nasal Cavity: Poor Correlation With Radiologically Significant Rhinosinusitis but Importance in Surgical Planning OBJECTIVE. The purpose of this study was to determine the incidence of sinonasal anatomic variants and to assess their relation to sinonasal mucosal disease. MATERIALS AND METHODS. A retrospective evaluation of 192 sinus CT examinations of patients with a clinical history of rhinosinusitis was conducted. The CT scans were evaluated for the presence of several anatomic variants of the sinonasal cavities, and the prevalence of each variant was calculated. Prevalences of all sinonasal anatomic variants were compared between patients who had minimal to no apparent imaging evidence of rhinosinusitis and those who had radiologic evidence of clinically significant rhinosinusitis. RESULTS. The most common normal variants were nasal septal deviation, Agger nasi cells, and extension of the sphenoid sinuses into the posterior nasal septum. We found no statistically significant difference in the prevalence of any of the studied anatomic variants between patients with minimal and those with clinically significant paranasal sinus or nasal cavity disease. CONCLUSION. Analysis of every routine CT scan of the paranasal sinuses obtained for sinusitis or rhinitis for the presence of different anatomic variants is of questionable value unless surgery is planned. N umerous sinonasal anatomic variants exist and are frequently seen on sinus CT scans. The most common ones are Agger nasi cells, infraorbital ethmoidal (Haller) cells, sphenoethmoidal (Onodi) cells, nasal septal deviation, and concha bullosa [1 10]. The Agger nasi cells are the most anterior ethmoidal air cells. Their location is anterior, lateral, and inferior to the frontal recess [1, 11]. Infraorbital ethmoidal (Haller) cells are ethmoidal cells that extend downward under the medial floor of the orbit adjacent to and above the maxillary sinus ostium lateral to the infundibulum [1, 7]. Sphenoethmoidal (Onodi) cells are posterior ethmoidal cells that extend laterally, superiorly, and posteriorly to the sphenoid sinus and are intimately associated with the optic nerve [1]. Nasal septal deviation is defined as any bending of the septal contour on coronal CT scans and is present in more than one half of the population [3 5, 12]. Concha bullosa is commonly defined as pneumatization of the middle turbinate involving its inferior bulbous portion and is usually bilateral [1, 5, 12]. Pneumatization of the lamina of the middle turbinate is usually not defined as a concha bullosa and occurs fairly frequently, as does pneumatization of the superior turbinates [2, 5, 13, 14]. A paradoxically bent middle turbinate is defined as a turbinate having a scroll convexity in the lateral rather than the medial aspect [3, 5, 8]. Less common anatomic variants of the paranasal sinuses include pneumatization of the uncinate process (or an uncinate bulla), large ethmoidal bullae, supraorbital cells, and pneumatized crista galli [2, 3, 5, 8, 15, 16]. A supraorbital ethmoidal air cell is located posterolateral to the frontal sinus, superior and lateral to the lamina papyracea, and anterior to the anterior ethmoidal artery and can be identified by the presence of a bony septum between the frontal and anterior ethmoidal sinuses on axial CT images [16]. Pneumatization of the crista galli originates from the frontal sinuses [15]. Some of the anatomic variants have been reported to be associated with chronic rhinosinusitis, possibly leading to inflammation by obstructing drainage pathways from the sinuses and nasal cavity [2 5, 10]. Specifically, large ethmoidal bullae correlated with maxillary sinusitis in one study [2], but another study [3] showed a correlation between AJR:204, June 2015 1255
Shpilberg et al. paradoxically bent middle turbinates, infraorbital ethmoidal cells, and chronic rhinosinusitis. A statistically significant association has been found between the presence of sinus mucosal disease and nasal septal deviation, bilateral concha bullosa, infraorbital ethmoidal (Haller) cells, hypertrophic ethmoidal bullae, and Agger nasi cells [5]. An association also has been found between Agger nasi cells and frontal sinusitis [4]. In one study [10], the presence of infraorbital ethmoidal (Haller) cells and narrow infundibula was associated with recurrent acute rhinosinusitis. However, a number of other studies [4, 6, 7, 17, 18] did not show a significant association between these anatomic variants and rhinosinusitis. Moreover, it has been reported that failure to recognize certain anatomic variants such as sphenoethmoidal (Onodi) cells, pneumatization of anterior clinoid processes, supraorbital cells, infraorbital ethmoidal (Haller) cells, pneumatization of the dorsum sella, and dehiscence of the lamina papyracea may lead to complications during surgery due to proximity of blood vessels, nerves, brain, and orbits [1, 8, 9, 11, 16, 19, 20]. The purposes of this study were to investigate the prevalence of a number of anatomic A Fig. 1 43-year-old man with chronic rhinosinusitis. Coronal unenhanced CT scan shows pneumatization from maxillary sinus of left inferior turbinate (arrow). Asterisk marks partially pneumatized left middle turbinate. variants of the sinonasal cavities and to determine their relation to sinonasal mucosal disease and their clinical relevance in general. Materials and Methods After obtaining institutional review board approval, we retrospectively examined images from 192 consecutive unenhanced sinus CT examinations of patients referred because of symptoms of active rhinosinusitis between May 7, 2013, and November 5, 2013. Patients who had previously undergone sinonasal surgery or had a sinonasal malignancy were excluded. The conditions of all patients were diagnosed as rhinosinusitis only on the basis of the major criteria of the Task Force on Chronic Rhinosinusitis [21]. The symptoms were facial pain, facial pressure, nasal obstruction, hyposmia, or purulent rhinorrhea. The studies were performed on a 64-MDCT (LightSpeed VCT 64 Channel or Discovery CT750 HD, both GE Healthcare) or a 40-MDCT (Somatom Definition AS, Siemens Healthcare) scanner with an FOV of 14 16 cm and a slice thickness of 0.625 mm. The axial plane was the inferior orbital meatal plane (anthropologic plane). Coronal and sagittal reconstructions were postprocessed. The CT scans were examined independently by two neuroradiologists who had B certificates of added qualification, one of whom had more than four decades of experience in interpreting head and neck images. Any differences in evaluations were resolved by consensus. The CT scans were evaluated for the presence of anatomic variants of the sinonasal cavities. The prevalence of each variant and the frequency of its bilaterality when applicable were calculated. The CT scans were also evaluated for degree of paranasal sinus and nasal cavity disease. The patients were divided into two categories: those who were considered have minimal to no apparent paranasal sinus disease or nasal passage obstruction (105 patients) and those who had evidence of clinically significant paranasal sinus disease or nasal passage obstruction (87 patients). We defined minimal disease as less than 1-mm mucosal thickening with no obstruction of the sinus drainage passages. The prevalence of anatomic variants of the paranasal sinuses and nasal cavity was calculated for each group, and the results for the two groups were compared by Fisher exact test. The proportion of bilateral anatomic variants was calculated for each of the two groups when applicable, and the results for the two groups were subsequently compared by Fisher exact test. For all comparisons conducted in this study, p < 0.05 was considered to be statistically significant. Results The patients ages ranged from 10 to 82 years (mean, 47.9 years); 86 (44.8%) were women, and 106 (55.2%) were men. Overall, the most common anatomic variant of the paranasal sinuses and nasal cavity was nasal septal deviation. It was present to some extent in 189 of 192 patients (98.4%) but was considered to be more than minimal (> 1 mm) in 118 of 192 patients (61.4%). The second most common variant was Agger nasi cells, which were present in 160 of 192 patients (83.3%). The third most common variant, noted in 146 of 192 patients (76.0%), was extension of the sphenoid sinuses into the posterior nasal septum (Table 1). Fig. 2 Sinusitis. A, Coronal unenhanced CT of 50-year-old woman with chronic sinusitis shows pneumatization of crista galli (arrow), which occurs as diverticulum of frontal sinus. Left supraorbital ethmoidal cell pneumatizing roof of orbit (SE) also is evident. B, Axial unenhanced CT scan of 47-year-old man with sinusitis shows bilateral supraorbital cells (E) located behind frontal sinuses (F). Bony plate is evident between frontal and supraorbital cells on each side. 1256 AJR:204, June 2015
CT of Paranasal Sinuses and Nasal Cavity TABLE 1: Sinonasal Anatomic Variants Observed and Their Prevalence (%) Anatomic Variant Prevalence Bilateral Nasal septal deviation 98.4 (61.4 > 1 mm) NA Agger nasi cell 83.3 70.6 Sphenoid sinus extension into posterior nasal septum 76.0 4.1 Pneumatization posterior to floor of sella turcica 68.8 NA Prominent ethmoidal bulla 44.8 44.2 Infraorbital ethmoidal (Haller) cell 39.1 41.3 Partially pneumatized middle turbinates 37.0 62.0 Nasal septal spur 32.3 NA Supraorbital cell 28.1 39.0 Pneumatized pterygoid process 27.1 36.5 Pneumatized superior turbinate 26.0 54.0 Concha bullosa 26.0 38.0 Pneumatized anterior clinoid process 16.7 37.5 Paradoxically bent middle turbinate 15.6 16.7 Pneumatized hard palate 14.6 78.6 Uncinate cells 13.5 23.1 Sphenoethmoidal (Onodi) cells 12.0 4.4 Pneumatized crista galli 9.9 NA Pneumatized inferior turbinate 1.0 0 Dehiscent lamina papyracea 0.5 0 Note NA = not applicable. TABLE 2: Prevalence (%) of Anatomic Variants in the Minimal and Significant Sinonasal Groups Anatomic Variant Minimal Significant Nasal septal deviation 98.1 (62.0 > 1 mm) 98.8 (60.9 > 1 mm) 1.0000 Agger nasi cell 83.8 82.8 0.8485 Sphenoid sinus extension into posterior nasal septum 79.0 71.3 0.2399 Pneumatization posterior to floor of sella turcica 64.8 63.6 0.2130 Prominent ethmoidal bulla 46.7 42.5 0.6620 Infraorbital ethmoidal (Haller) cell 36.2 42.5 0.3775 Partially pneumatized middle turbinate 40.0 33.3 0.3701 Nasal septal spur 33.3 31.0 0.7587 Supraorbital cell 23.8 33.3 0.1509 Pneumatized pterygoid process 25.7 28.7 0.7445 Pneumatized superior turbinate 30.5 20.7 0.1393 Concha bullosa 23.8 28.7 0.3233 Pneumatized anterior clinoid process 13.3 20.7 0.1804 Paradoxically bent middle turbinate 14.3 17.2 0.6903 Pneumatized hard palate 13.3 16.1 0.6824 Uncinate cell 17.1 9.2 0.1388 Sphenoethmoidal (Onodi) cell 10.5 13.8 0.5101 Pneumatized crista galli 9.5 10.3 1.0000 Pneumatized inferior turbinate 1.0 1.2 1.0000 p The most frequent bilateral paranasal sinus and nasal cavity anatomic variants were a pneumatized hard palate (22/28 [78.6%]), Agger nasi cells (113/160 [70.6%]), and partial pneumatization of the middle turbinates (44/71 or 62.0%) (Table 1). There was no statistically significant difference in the prevalence of any of the studied anatomic variants between the minimal and clinically significant paranasal sinus or nasal cavity disease groups (p = 0.1388 1.0) (Table 2). There was no statistically significant difference in the proportion of bilateral anatomic variants between the minimal and significant disease groups (p = 0.2436 1.0) (Table 3). Several anatomic variants, including the least common ones, are illustrated in Figures 1 7. Discussion In our study, the most common anatomic variant of the sinonasal cavities was deviation of the nasal septum, which was present in 98.4% of the patients but was considered to be more than minimal in 61.4%. Although our overall prevalence of nasal septal deviation is much higher than that reported in the literature, the prevalence of more than minimal nasal septal deviation falls within the previously reported range of 19.4 79% [3 5, 12, 17]. Approximately one third of our cases of nasal septal deviation were associated with a bony nasal septal spur. The second most common variant was Agger nasi cells, which were present in 83.3% of patients, falling within the wide range of 3 100% reported in previous studies [1 7]. Agger nasi cells were also the second most common variant that occurred bilaterally in our study. The third most common variant was extension of the sphenoid sinuses into the posterior nasal septum resulting in some degree of pneumatization of the posterior nasal septum (76.0%). The fourth most common variant was sphenoid sinus pneumatization extending posterior to the floor of the sella turcica (68.8%), which was defined as air extending more than halfway beyond the middle of the sellar floor toward the dorsum sella. In one study [11], extensive sellar floor pneumatization was present in 77% of the patients. It reached the middle of the sella in 54.7%, exhibited a significant postsellar component in 22.3%, and extended to the dorsum sella in 13.4%. The prevalence of prominent ethmoidal bullae in our study was 44.8%, which is higher than the 4 32.8% reported in the literature [2, 5]. This may be because we did not use objective criteria when evaluating the size of the eth- AJR:204, June 2015 1257
Shpilberg et al. TABLE 3: Prevalence (%) of Bilateral Variants in the Minimal and Significant Sinonasal Groups Anatomic Variant moidal bullae, such as measuring them. Another anatomic variant that had a higher than previously reported prevalence in our study was uncinate cells at 13.5%, which according to the literature occur in 0.4 9% of patients [2, 3, 5]. The prevalence of infraorbital ethmoidal (Haller) cells in our study (39.1%) was within the 10 62% reported range [1 5, 8, 10], as was the prevalence of supraorbital cells at 28.1% (5 65% previously reported) [16], sphenoethmoidal (Onodi) cells at 12% (1.3 65.3% previously reported) [1, 2, 4, 5, 8, 9], and a pneumatized crista galli at 9.9% (2.4 13% previously reported) [5, 15]. The prevalence of pneumatization of the anterior clinoid process in our study was 16.7%, which is commensurate with the prevalence of 4 29.3% described in the literature [8, 19, 22]. Pneumatization of the pterygoid processes was found in 27.1% of patients in our study, which is slightly lower than the previously reported prevalence of 29 43.6% [22]. Pneumatization of the hard palate was defined as medial extension of the maxillary sinuses into the palatal process of the maxilla and was present in 14.6% of patients in our study. It was also the most common variant to be bilateral. The significance and incidence of this entity are not known. The prevalences of concha bullosa at 26.0% in our study (14 67.5% previously reported) [3 5, 8, 10, 12, 13, 17], pneumatized lamina of the middle turbinate at 37.0% (9.6 46.2% previously reported) [2, 5, 13], and paradoxically bent middle turbinates at 15.6% (0.7 40% previously reported) [3, 5, 8] were similar to those described in the literature. Minimal Significant Sphenoid sinus extension into posterior nasal septum 3.6 4.8 1.0000 Pneumatized anterior clinoid processes 28.6 44.4 0.4709 Pneumatized pterygoid processes 33.3 40.0 0.7743 Pneumatized hard palate 71.4 85.7 0.6483 Agger nasi cell 69.3 72.2 0.7296 Infraorbital ethmoidal (Haller) cells 36.8 50.0 0.4861 Uncinate cells 16.7 37.5 0.3301 Prominent ethmoidal bullae 49.0 37.8 0.3817 Supraorbital cells 36.0 41.4 0.7827 Pneumatized superior turbinates 50.0 61.1 0.5587 Paradoxically bent middle turbinates 13.3 20.0 1.0000 Partially pneumatized middle turbinates 61.9 62.1 1.0000 Concha bullosa 48.0 28.0 0.2436 Less than one half of cases of concha bullosa (38.0%) in our study were bilateral. Pneumatization of the superior turbinates was found in 26.0% of patients in our study, which is slightly lower than the previously reported prevalence of 27 57% [2, 13, 14]. Only two patients had pneumatized inferior turbinates, which is consistent with the previously reported observation that it is a very rare entity with at least 10 reported cases [13]. Another very rare finding with only one case (0.5%) in our study was congenital dehiscence of the lamina papyracea; this prevalence is slightly lower than previously the reported 0.76 10% [20]. Fig. 3 22-year-old woman with chronic sinusitis. Coronal unenhanced CT scan shows right-sided sphenoethmoidal (Onodi) cell (O) in upper lateral sphenoid sinus (S). Projection of optic nerve canal into sphenoethmoidal (Onodi) cell (arrow) is evident. p We did not find a statistically significant difference in the prevalence of any of the paranasal sinus or nasal cavity anatomic variants between the minimal and significant disease groups. Like our study, a number of other studies did not show a significant association between the presence of anatomic variants and imaging evidence of rhinosinusitis. Two studies [4, 17] showed no increased incidence of paranasal sinus disease in patients with concha bullosa or nasal septal deviation. One study [6] showed no significant association between Agger nasi cells and frontal sinus disease. There was no significant association between infraorbital ethmoidal (Haller) cells and maxillary sinusitis in another study [7]. No significant relation was found between sinusitis and multiple anatomic variants in pediatric patients [18]. Patients may have symptoms of some of the anatomic variants without imaging evidence of clinically significant rhinosinusitis. For example, contact between a massively pneumatized turbinate and nasal mucosa can cause headache even in the absence of sinonasal inflammation [1]. Identification of some anatomic variants is crucial in the planning of functional endoscopic sinus or other skull base surgery, because the presence of these variants may influence the surgical approach. Most notably, the presence of sphenoethmoidal (Onodi) cells is associated with increased risk of injury to the optic nerves or carotid arteries during functional endoscop- Fig. 4 38-year-old man with chronic sinusitis. Coronal unenhanced CT scan shows right-sided uncinate cell (arrow). This cell comes from main ethmoidal cell complex. M = middle turbinate, I = inferior turbinate. 1258 AJR:204, June 2015
CT of Paranasal Sinuses and Nasal Cavity Fig. 5 Coronal unenhanced CT scan of sinuses in 34-year-old woman with sinusitis shows bilateral pneumatization of hard palate (arrows), representing pneumatization from maxillary sinus into palatal process of maxilla. M = middle turbinate, I = inferior turbinate. Fig. 6 49-year-old man with chronic sinusitis. Coronal unenhanced CT scan of sinuses shows bilateral paradoxically bent middle turbinates (arrows). I = inferior turbinate. ic sinus surgery and with other transsphenoidal and skull base procedures [1, 8, 9]. Pneumatization of the anterior clinoid processes increases the incidence of CSF rhinorrhea after skull base surgery, such as for access to cavernous sinus lesions requiring anterior clinoidectomy [19]. However, there is no significant association between anterior clinoid pneumatization and spontaneous CSF leaks [19]. Pneumatization of the anterior clinoid process also increases the risk of injury to the optic nerve during endoscopic sinus surgery [8]. To avoid accidental injury to the carotid artery and optic nerves, it is important to be aware of the midline of a highly pneumatized sphenoid sinus when opening the sella via a trans sphe noid al approach [11]. Postsellar pneumatization from the sphenoid sinus, particularly pneumatization of the dorsum sella, may result in penetration of the posterior wall of the sphenoid with resultant CSF leak during transsphenoidal pituitary surgery [11]. The presence of infraorbital ethmoidal (Haller) cells can increase the risk of orbital injury during ethmoidectomy [8]. The presence of supraorbital cells can increase the risk of orbital damage during endoscopic sinus surgery and may jeopardize sterility in anterior cranial fossa approaches to the orbit [8]. Failure to recognize a supraorbital cell with the anterior ethmoidal artery as a landmark during surgery increases the risk of skull base injury because CSF leaks and retraction of a lacerated anterior ethmoidal artery into the orbit can occur [16]. Dehiscence of the lamina papyracea can lead to prolapse of orbital contents into the ethmoidal sinuses and puts the patient at risk of hemorrhage or damage to the orbit during endoscopic intranasal ethmoidectomy [20]. All 192 patients in our study had at least one anatomic variant of the paranasal sinuses or nasal cavity. With the exception of one patient whose only variant consisted of nasal septal deviation, all of the patients had at least two anatomic variants. The association of different anatomic variants with one another was not analyzed in this study, which may be a limitation. We did, however, analyze the proportion of different variants that were bilateral and found no significant difference in proportion of bilateral variants between the minimal and clinically significant rhinosinusitis groups. Another possible limitation of our study was that we analyzed only the prevalence of pneumatization of the uncinate process, although several other variations in the uncinate process exist with a reported incidence between 15.9% and 65% [5]. Other variations in the uncinate process include medial deflection, which has been described in 3 22.8% of cases, and lateral deflection, observed in 21.4% of cases [5]. Medial deviation of the uncinate process was associated with sinusitis in one study [5]. We also did not analyze the prevalence of different types of frontal cells, which were found to be not associated with frontal sinusitis in two studies [6, 23]. It has been reported that patients with clinically significant sinusitis may have no or minimal evidence of sinusitis, such as mucosal thickening, at imaging. In one study [24], 35% of patients with symptomatic chronic rhinosinusitis had completely normal scan findings, and another 10% had minimally abnormal findings. In another study [25], 40% of patients with symptomatic chronic rhinosinusitis had normal sinus CT findings. Patients with normal CT findings were younger than those with abnormal findings, were more likely to be have symptoms, and had more severe symptoms. In our study, we divided the patients into minimal and clinically significant disease groups based on imaging findings rather than clinical data, which was a limitation. Moreover, it is possible that patients with CT scans showing no or minimal evidence of sinus inflammation may have had significant sinusitis on previous CT scans that improved or resolved even though they continued to experience sinusitis symptoms. Radiologists should assume that all patients undergoing CT for chronic rhinosinusitis will be undergoing surgery and include the presence of anatomic variants including sphenoethmoidal (Onodi) cells, pneumatization of anterior clinoid processes, supraorbital cells, infraorbital ethmoidal (Haller) cells, pneumatization of the dorsum sella, and dehiscence of the lamina papyracea in their reports. Although surgical complications occur for a variety of reasons, failure to recognize certain anatomic variants is an important factor, and radiologists have a responsibility to comment on the presence of certain anatomic variants to minimize the likelihood of surgical complications. The results of our study and several previous studies show that an association between sinonasal anatomic variants and rhinosinusitis may be an urban myth. Conclusion There are a multitude of anatomic variants of the sinonasal cavities, some of which are so common that they are most likely found in the majority of the population. We found no significant difference in the prevalence of any of the paranasal sinus or nasal cavity variants between patients with minimal and patients with clinically significant radiologic evidence of rhinosinusitis. Therefore, analysis of every routine AJR:204, June 2015 1259
Shpilberg et al. A Fig. 7 Chronic rhinosinusitis and sinusitis. A, Coronal unenhanced CT scan of 37-year-old woman with chronic rhinosinusitis shows pneumatization of both superior turbinates (thin arrows). Right-sided nasal septal spur (thick arrow) is present at junction of perpendicular plate of ethmoid bone (E) and vomer (V). B, Coronal unenhanced CT scan of 29-year-old woman with sinusitis shows prominent left ethmoidal bulla cell (B), which may encroach on infundibulum (arrow). CT scan of the paranasal sinuses obtained for sinusitis or rhinitis for the presence of different anatomic variants is of questionable value unless surgery is planned. For patients who are planning to undergo functional endoscopic or other skull base surgery, however, it is important to be aware of certain anatomic variants, such as sphenoethmoidal (Onodi) cells, pneumatization of anterior clinoid processes, supraorbital cells, infraorbital ethmoidal (Haller) cells, pneumatization of the dorsum sella, and dehiscence of the lamina papyracea. Failure to recognize these variants is associated with a higher rate of surgical complications. References 1. Kantarci M, Karasen RM, Alper F, et al. Remarkable anatomic variations in paranasal sinus region and their clinical importance. Eur J Radiol 2004; 50:296 302 2. Sivasli E, Sirikçi A, Bayazýt YA, et al. Anatomic variations of the paranasal sinus area in pediatric patients with chronic sinusitis. Surg Radiol Anat 2003; 24:400 405 3. Azila A, Irfan M, Rohaizan Y, et al. The prevalence of anatomical variations in osteomeatal unit in patients with chronic rhinosinusitis. Med J Malaysia 2011; 66:191 194 4. 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