|Year : 2020 | Volume
| Issue : 4 | Page : 464-469
The sagittal grooves of the middle nasal turbinate determine paradoxical curvatures and bifidities
MC Rusu1, N Măru1, CJ Sava2, A Motoc3, M Săndulescu4, D Dincă5
1 Division of Anatomy, Faculty of Dental Medicine, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania
2 Division of Anatomy, Faculty of Medicine, “Victor Babes” University of Medicine and Pharmacy, Timisoara, Romania
3 Department of Anatomy, “Victor Babes” University of Medicine and Pharmacy, Timisoara, Romania
4 Division of Oral Implantology, Faculty of Dental Medicine, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania
5 Department II of Surgical Clinical Divisions, Faculty of Medicine, “Ovidius” University, Constanta, Romania
|Date of Submission||29-Jan-2019|
|Date of Acceptance||14-Dec-2019|
|Date of Web Publication||4-Apr-2020|
Dr. N Măru
“Carol Davila” University of Medicine and Pharmacy, 8 Eroilor Sanitari Blvd., RO-050474, Bucharest
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Paradoxical curvature of the middle nasal turbinate (MT) is a common anatomic variant, usually found and reported on coronal CT slices. However, less attention has been paid to the sagittal groove (SG) which is determining it. Aim: The study aimed to determine paradoxical curvatures and bifidities in the sagittal groves of middle nasal turbinate. Material and Method: A retrospective CBCT study on the archived files of 52 adult patients was performed. Results: Different patterns of MT bifidity were found: (1) unilateral bifid MTs; (2) bifid and trifid MTs and “wandering” single SGs; (3) bilateral bifid middle turbinates and double SGs, (4) bilateral false bifid appearance due to middle and superior turbinates fusion and (5) bifid concha bullosa media. Digital “dissections” of patients' files allowed us to conclude that paradoxical curvature as well as bifidity of MTs relate to the placement and number of the SGs on the MTs. Such SGs were previously documented in prenatal MTs since the 14th week, as well as in pædiatric patients. Conclusions: It seems reasonable to speculate that paradoxical curvature, as well as bifidity of MT, this later being previously undocumented, are just adult vestiges of the primitive MT morphology. Nevertheless, documentation of the MT morphology should not rely exclusively on coronal CTs, as combined morphologies of that turbinate could occur.
Keywords: Bifid middle turbinate, computed tomography, nasal concha, nasal fossa, paradoxical turbinate
|How to cite this article:|
Rusu M C, Măru N, Sava C J, Motoc A, Săndulescu M, Dincă D. The sagittal grooves of the middle nasal turbinate determine paradoxical curvatures and bifidities. Niger J Clin Pract 2020;23:464-9
|How to cite this URL:|
Rusu M C, Măru N, Sava C J, Motoc A, Săndulescu M, Dincă D. The sagittal grooves of the middle nasal turbinate determine paradoxical curvatures and bifidities. Niger J Clin Pract [serial online] 2020 [cited 2020 Sep 28];23:464-9. Available from: http://www.njcponline.com/text.asp?2020/23/4/464/281935
| Introduction|| |
The nasal turbinates (conchae) adhere to the nasal fossa lateral and/or superior nasal walls. The inferior nasal turbinate (IT) is an independent bone. The middle turbinate (MT), the superior turbinate (ST), and the inconstant Santorini's supreme one are ethmoidal turbinates. A secondary MT (SMT) is a bony projection from the lateral wall of the middle meatus while an accessory middle turbinate (AMT) is a medially bent uncinate process, that is developmentally distinctive to the SMT. Anatomic variations of the MT are important in the pathogenesis of sinusitis. The nasal turbinates are used as landmarks during functional endoscopic surgery.
All nasal turbinates develop from the cartilaginous nasal capsule's ridges—the turbinals, the lowest being the maxilloturbinal and those above it being the ethmoturbinals (ET1-ET5)., These turbinals are separated by furrows or grooves., The first ethmoturbinal (ET1) does not form a nasal turbinate; it derives the agger nasi and the uncinate process., The middle turbinate results from ET2 and the superior turbinate derives from ET3.
The anatomy of the lateral nasal wall in the newborn is depicted in Scott-Brown's Otorhinolaryngology, Head and Neck Surgery (2008). All nasal turbinates are attached to that wall and a sagittal groove is observed on the septum-facing medial face of the middle turbinate; above that groove, a longitudinal torus (LT) is identified and indicated as occasionally persisting in adult. Thus, the MT in the newborn has a medial sagittal groove (SG) with an upper lip represented by the LT. Identical details are presented in a halftone drawing of Warren Davis (1918) of the lateral nasal wall in a 1-year-old child [Figure 1], but were not termed anatomically. Scott (1954) also presented a halftone drawing of the lateral nasal wall in a 4-year-old child in whom the MT had an SG which placed medially in the anterior part of the turbinate, but switched to an inferior placement in the middle third of the turbinate, thus appearing as a “wandering” SG.
|Figure 1: Specimen From a child of 1-year, 10-month, and 13-day old. Sagittal section showing lateral wall of the nasal cavity and the sinus sphenoidalis. [reprinted with permission from SAGE Publications (License Number: 4417010780950) from Davis (1918)]. The original abbreviations are: C.med., Concha media; C.sup., concha superior; C.supr. I, concha suprema I; C.supr, II, conchasuprema II; C.sph., concha sphenoidalis (ossiculum Bertini); S.sph., sinus sphenoidalis; Hypoph., hypophysis; Ton.phar., tonsilla pharyngea; Ost. tub.aud., ostium pharyngeum tubæ auditivæ; C.in., concha inferior; Lob., lobulus. A white arrow was added to indicate the sagittal groove of the middle turbinate|
Click here to view
In children, the most common anatomic variations of the lateral nasal wall are pneumatic variants, such as Haller, Onodi, agger nasi cells, and concha bullosa media, as well as paradoxical middle turbinate (PMT).,, The paradoxical curvature of the middle turbinate is defined as its convex surface facing the lateral nasal wall instead of the nasal septum. Rephrasing, the PMT has a septum-facing concave longitudinal area. Thus, such paradoxical curvatures of the middle turbinate could be equally viewed as MTs with fetal morphologies, with a medial SG bordered by a more or less protrusive LT on their medial (septal) surface.
The PMT is a common anatomic variation in adults, being usually identified, unilaterally or bilaterally, on CT coronal images.,,,,,,,, Because of the limitations of this imagistic method, the authors did not observe, or use, three-dimensional volumes, or other dimensions of the anatomical space, to check the longitudinal extent of concavities of those paradoxical curvatures.
On the other hand, turbinate bifidity was reported, although rarely, for the IT,,,, and the ST, but we did not find any report of bifid MTs (BMT). Therefore, we designed a retrospective cone-beam computed tomography (CBCT) study to assess the bifidity, or trifidity, of the MT, in association, or not, with other variations, such as concha bullosa media or paradoxical MT.
| Material and Method|| |
A retrospective CBCT study on the archived files of 52 patients (25 male, 27 female) was performed. All subjects had been scanned using an iCat CBCT machine (Imaging Sciences International) with the following settings: resolution 0.250, field of view 130, and image matrix size 640 × 640. The patients were positioned according to the manufacturer instructions. By using the iCatVision software, the CBCT data was exported as a single uncompressed DICOM file, which we further analyzed using the Planmeca Romexis Viewer 3.5.0.R software. We evaluated the bidimensional multiplanar reconstructions (MPRs) in the three anatomical planes, as well as the three-dimensional volume renderizations of specified areas by use of the Soft Tissue filter. Relevant anatomical features were exported as image files (*.tif). The patients have given written informed consent for all medical data (including radiographs, CBCT scans, and intraoral images) to be used for research and teaching purposes, provided the protection of the identity is maintained. The present study was tacitly approved by the authorities in the authors' institutions.
There were recorded the details regarding the anatomic variation of the nasal turbinates: pneumatization, bi/trifidity, and paradoxical curvature. There were also recorded the cases with secondary and accessory middle turbinate. Following the retrospective CBCT study, we selected a 6-case series (case #1: female, 52 years, case #2: female, 49 years, case #3: male, 46 years, case #4: male, 39 years, case #5: female, 51 years, case #6: female, 42 years) to be reported here.
| Results|| |
I. Anatomic variations of the nasal turbinates
Santorini's turbinate was found in 5/52 cases (9.6%), was bilateral in 4 patients and unilateral in 1 patient. That turbinate was pneumatized in 2 patients with bilateral evidence.
The ST was found in all cases, and it was pneumatized in 19/52 cases (36.5%); the ST pneumatization was bilateral in 13 patients and unilateral in 6 patients. A paradoxical ST was found in 3/52 cases (5.7%), being bilateral in 2 patients and unilateral in one.
The middle turbinate was found either bifid or trifid in 6/52 cases which will be detailed in the following section. The MT pneumatization unassociated with other variable morphology was found in 39/52 cases (75%), being bilateral in 27 cases and unilateral in other 12 cases. The simple paradoxical curvature of the MT was recorded in 6/52 cases (11.5%), being bilateral in 2 cases and unilateral in 4 cases.
A SMT was found in 6/52 cases (11.5%), 5 bilateral and 1 unilateral. An AMT was found in 11/52 cases (21.1%), 9 bilateral and 2 unilateral.
II. Bi- and trifidity of the middle nasal turbinate
Unilateral bifid middle turbinates (cases #1 and #2)
In case #1, we found a right deviation of the nasal septum which was penetrated posteriorly by sphenoseptal recesses of both sphenoidal sinuses. On each side, three nasal turbinates were found, inferior, middle, and superior. The middle turbinates had minute lamellar pneumatizations. The right middle turbinate was compressed by a right septal spur and in its anterior, two-thirds presented a medial SG which determined its paradoxical curvature (result not presented) but in its posterior, third presented a different, lateral sagittal groove, which determined this turbinate bifidity [Figure 2]a, [Figure 2]b. The left middle turbinate had a short medial sagittal groove which determined a segmental paradoxical curvature (result not presented).
|Figure 2: Unilateral bifid middle turbinates. Cases # 1 (a, b) and #2 (c, d). Coronal multiplanar reconstructions (a, c) and three-dimensional volume renderizations (b, d, lateral views of sagittally cropped volumes). Normally, curved bifid middle turbinates, right (a, b, arrows) and left (c, d, arrowheads)|
Click here to view
In case #2, there was only a minor bifidity of the left middle turbinate, which was determined by a short infero-lateral sagittal groove [Figure 2]c, [Figure 2]d.
Bifid and trifid middle turbinates and “wandering” single sagittal grooves (case #3)
In case #3, we observed complex and asymmetrical morphologies of the middle turbinates which were determined by switched position of the respective sagittal grooves (“wandering grooves“) [Figure 3]. There were also found a right secondary middle turbinate and a left accessory middle turbinate, this later resulting from a medially bent uncinate process (results not presented). The right MT had an anterior paradoxical curvature determined by a medially placed sagittal groove which continued inferiorly in the posterior two-thirds of the turbinate and determined it a bifid morphology. The left MT was trifid in its middle portion, with a larger medial and thinner lateral inferior sagittal grooves and paradoxically curved posteriorly, due to the continuation of the medial inferior sagittal groove as a medial one.
|Figure 3: Wandering grooves of middle turbinates determine combined variations (case #3). Anterior-to-posterior coronal multiplanar reconstructions (a-c) and three-dimensional volume renderizations of the lateral nasal walls (medial views of sagittally cropped volumes), right (d) and left (e). Right paradoxically curved (white arrowheads) and bifid (white arrows) middle nasal turbinate. Left trifid (black arrows) and paradoxically curved (black arrowheads) middle nasal turbinate|
Click here to view
Bilateral bifid middle turbinates and double sagittal grooves (case #4)
In case #4, the MTs were equally paradoxical and bifid, but with different sagittal grooves determining those morphologies [Figure 4]. The right MT had a medial sagittal groove on almost its entire length, which determined an almost complete paradoxical curvature. On that MT, a second sagittal groove was placed inferiorly and determined its bifid appearance. The left MT hat an anterior medial sagittal groove leading to paradoxical curvature and a second sagittal groove which was placed inferiorly in the middle third of the turbinate determining its bifid appearance, but continued medially in the posterior part of the turbinate, to determine a second, different one, paradoxical curvature.
|Figure 4: Bilateral double sagittal grooves of middle turbinates with combined paradoxical curvature and bifidity (case #4). Anterior-to-posterior series of coronal multiplanar reconstructions (a-f). Three-dimensional volume renderizations of the lateral nasal walls (medial views of sagittally cropped volumes), right (g) and left (h). The right middle turbinate has medial (white arrowheads) and inferior (white arrow) sagittal grooves. The left middle turbinate has a short medial (black arrowheads) and an inferior (black arrows) sagittal groove|
Click here to view
Bilateral false bifid appearance due to middle and superior turbinates posterior fusion (case #5)
In case #5 [Figure 5], the ST and MT on each side were fused posteriorly in a common insertion on the medial wall of the maxillary sinus, which determined on coronal cuts a false bifid appearance of the MTs. Due to that posterior fusion of turbinates, the superior nasal meatus could have been misjudged as a sagittal groove of the MT.
|Figure 5: False bifidities of middle turbinates (case #5). Anterior (a) and posterior (b) coronal multiplanar reconstructions. Three-dimensional volume renderization (c, coronal crop of the volume, posterior view). The superior (arrowheads) and middle (arrows) turbinates are fused at their common maxillary insertions (*). The superior meatus (c, diverging arrows) appears as a false turbinate bifidity|
Click here to view
Unilateral bifid concha bullosa media (case #6)
In case #6 [Figure 6], all three pairs of nasal turbinates were found. The left superior turbinate was pneumatized, as also were both the MTs. The right concha bullosa media also had a segmental bifidity in its middle third, due to a lateral sagittal groove.
|Figure 6: Bifid concha bullosa media (case #6). Coronal multiplanar reconstructions, posterior (a) and anterior (b). Three-dimensional volume renderizations, anterior view of the coronally croppedvolume (c) and medial view of the right lateral nasal wall (d). Left concha bullosa superior (double-headed arrow). Pneumatized (arrows) and bifid (arrowheads) right middle turbinate|
Click here to view
| Discussion|| |
The series of 6 cases we detailed here had either bifid, trifid, or paradoxical middle turbinates, all of these variant morphologies being determined by the specific placement of the sagittal groove. In our knowledge, a bifid concha bullosa media was not reported previously. Those variants were either unilateral or bilateral. We consider that a medial sagittal groove determines a paradoxical curvature of the MT, with the convexity oriented laterally, but an inferior sagittal groove determines a bifid MT [Figure 7]. A MT is associated with either a single sagittal groove, or with double sagittal grooves. If a single sagittal groove is present on a MT, it can be fixed, determining either paradoxical curvature or bifid appearance, or it could “wander,” thus switching from a medial placement to an inferior one; in such variant, that MT is equally paradoxical and bifid, but in different segments. If two sagittal grooves are present on the same MT, segmental MT trifidity or segmental combination of paradoxical curvature and bifidity could be encountered. As sagittal grooves were encountered in pediatric MTs,, this allows the paradoxical curvature and bifidity of MT to be regarded as persisting pediatric morphologies. The previous reports of paradoxical curvature seemingly overlooked the pediatric morphology and SG of the MT. Therefore, reports of paradoxical curvature of the MT ignored the sagittal placement of the SG and, from this point of view, are rather incomplete, as they do not indicate whether it is a sagitally complete paradoxical curvature, or a segmental one, or it evolved to bifidity in a different segment of that MT. A paradoxical curvature is defined by a laterally oriented convexity of the MT, but a MT bifidity occurs on a normally curved MT.
|Figure 7: Diagrams of normal (N), paradoxical (P), and bifid (B) middle turbinates. Depending on the placement of the sagittal groove on the inner surface of the turbinate (connectors), it will result either a paradoxical curvature (the medial sagittal groove), or a bifid morphology (the inferior sagittal groove). The upper lip of the groove of (P) corresponds to the medial lip of the groove of (B) and both correspond to the torus of the fetal middle turbinate|
Click here to view
The SG of the MT is, seemingly, not a postnatal morphological possibility in humans. We observed the evidence presented in a study of de Arreola et al. (1996) of human lateral nasal wall morphogenesis in embryos and fetuses; at 7 weeks, there were no grooves on the MT bud, but at 14 weeks, both MTs presented a medial epithelial SG corresponding to a medial chondral one, and there were also distinctive inferior chondral grooves which were giving a bifid appearance to the cartilaginous MT scaffolds. SGs were also found in an older human fetus (63 mm HL, CRL unknown) by Maier and Ruf (2014). On successive anterior-to-posterior cuts, an SG of the cartilaginous MT was inferior and generated a bifid appearance in the middle part of the turbinate, but posteriorly there was an SG located on the convex surface of the fetal MT which was “pushing” a spur on the opposite concave surface. It could not be established whether or not these are different SGs or segments of the same one. The reader is encouraged to observe these details of that clearly documented article, details which support the reasonable speculation that paradoxical curvature and bifidity of MT are prenatal features which could be conserved, or could disappear in adult.
When the MT is approached, identification of an SG, thus a prenatal morphology, should be determined by the surgeon to evaluate whether it is a segmental groove, or a “wandering” one which can alter the usual landmarks in endoscopic surgery. This because the MT is a key piece allowing and guiding the access to the ostiomeatal complex in the middle meatus, being described a long time ago by Loeb (1907) as “the most important surgical landmark of the nose” which “should more properly be called the inferior ethmoidal turbinate.“ Evaluation of individual anatomic variations of patients in CT is a prerequisite, especially in patients with chronic rhinosinusitis, as anatomical variations could increase the risk of mucosal disease. The significance of anatomic variations, such as is the paradoxical MT, in the pathogenesis of rhinosinusitis is, however, in debate or was defeated.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interests
The authors declare that they have no conflict of interest.
| References|| |
Sava CJ, Rusu MC, Sandulescu M, Dinca D. Vertical and sagittal combinations of concha bullosa media and paradoxical middle turbinate. Surg Radiol Anat 2018;40:847-53.
Maru N, Rusu MC, Sandulescu M. Variant anatomy of nasal turbinates: Supreme, superior and middle conchae bullosae, paradoxical superior and inferior turbinates, and middle accessory turbinate. Rom J Morphol Embryol 2015;56:1223-6.
Rusu MC, Sandulescu M, Sava CJ, Dinca D. Bifid and secondary superior nasal turbinates. Folia Morphol (Warsz) 2019;78:199-203.
Felix V, Veerasigamani N. Unilateral absence of ethmoid sinus and nasal turbinates: A rare case report. J Clin Diagn Res 2017;11:MD01-2.
Gotlib T, Kuzminska M, Sokolowski J, Dziedzic T, Niemczyk K. The supreme turbinate and the drainage of the posterior ethmoids: A computed tomographic study. Folia Morphol (Warsz) 2018;77:110-5.
Gleeson MJ, Clarke RC. Scott-Brown's Otorhinolaryngology: Head and Neck Surgery 7Ed: 3 volume set. Hodder Arnold (London): CRC Press; 2008.
Davis WB. LV. Anatomy of the nasal accessory sinuses in infancy and childhood. Ann Otol Rhinol Laryngol 1918;27:940-67.
Scott JH. The growth of the human face. Proc R Soc Med 1954;47:91-100.
Kim HJ, Jung Cho M, Lee JW, Tae Kim Y, Kahng H, Sung Kim H, et al
. The relationship between anatomic variations of paranasal sinuses and chronic sinusitis in children. Acta Otolaryngol 2006;126:1067-72.
Al-Qudah M. The relationship between anatomical variations of the sino-nasal region and chronic sinusitis extension in children. Int J Pediatr Otorhinolaryngol 2008;72:817-21.
Rusu MC, Sava CJ, Ilie AC, Sandulescu M, Dinca D. Agger nasi cells versus lacrimal cells and uncinate bullae in cone-beam computed tomography. Ear Nose Throat J 2019;98:334-9.
Wani AA, Kanotra S, Lateef M, Ahmad R, Qazi SM, Ahmad S. CT scan evaluation of the anatomical variations of the ostiomeatal complex. Indian J Otolaryngol Head Neck Surg 2009;61:163-8.
Shahizon AM, Suraya A, Rozmnan Z, Aini AA, Gendeh BS. Correlation of computed tomography and nasal endoscopic findings in chronic rhinosinusitis. Med J Malaysia 2008;63:211-5.
Ozcan KM, Selcuk A, Ozcan I, Akdogan O, Dere H. Anatomical variations of nasal turbinates. J Craniofac Surg 2008;19:1678-82.
Mendiratta V, Baisakhiya N, Singh D, Datta G, Mittal A, Mendiratta P. Sinonasal anatomical variants: CT and endoscopy study and its correlation with extent of disease. Indian J Otolaryngol Head Neck Surg 2016;68:352-8.
Maru YK, Gupta V. Anatomic variations of the bone in sinonasal C.T. Indian J Otolaryngol Head Neck Surg 2001;53:123-8.
Arslan H, Aydinlioglu A, Bozkurt M, Egeli E. Anatomic variations of the paranasal sinuses: CT examination for endoscopic sinus surgery. Auris Nasus Larynx 1999;26:39-48.
Beale TJ, Madani G, Morley SJ. Imaging of the paranasal sinuses and nasal cavity: Normal anatomy and clinically relevant anatomical variants. Semin Ultrasound CT MR 2009;30:2-16.
Bandyopadhyay R, Biswas R, Bhattacherjee S, Pandit N, Ghosh S. Osteomeatal complex: A study of its anatomical variation among patients attending North Bengal Medical College and Hospital. Indian J Otolaryngol Head Neck Surg 2015;67:281-6.
Çalışkan A, Sumer AP, Bulut E. Evaluation of anatomical variations of the nasal cavity and ethmoidal complex on cone-beam computed tomography. Oral Radiol 2017;33:51-9.
Rusu MC, Maru N, Sandulescu M, Sava CJ. Rare anatomic variation: True bifid inferior turbinate. Surg Radiol Anat 2018;40:217-20.
Al-Qudah MA. Extra middle turbinate lamellas: A suggested new classification. Surg Radiol Anat 2015;37:941-5.
Aksungur EH, Bicakci K, Inal M, Akgul E, Binokay F, Aydogan B, et al
. CT demonstration of accessory nasal turbinates: Secondary middle turbinate and bifid inferior turbinate. Eur J Radiol 1999;31:174-6.
Yilmaz MS, Guven M, Akidil O, Kayabasoglu G. Bifid inferior turbinate: A report of two cases. Kulak Burun Bogaz Ihtis Derg 2014;24:357-60.
Arredondo de Arreola G, Lopez Serna N, de Hoyos Parra R, Arreola Salinas MA. Morphogenesis of the lateral nasal wall from 6 to 36 weeks. Otolaryngol Head Neck Surg 1996;114:54-60.
Maier W, Ruf I. Morphology of the nasal capsule of primates--with special reference to Daubentonia and Homo. Anat Rec (Hoboken) 2014;297:1985-2006.
Loeb HW. The anatomy of the middle turbinate, with special reference to its topographic and surgical relations. JAMA 1907;48:2098-105.
Azila A, Irfan M, Rohaizan Y, Shamim AK. The prevalence of anatomical variations in osteomeatal unit in patients with chronic rhinosinusitis. Med J Malaysia 2011;66:191-4.
Lloyd GA. CT of the paranasal sinuses: Study of a control series in relation to endoscopic sinus surgery. J Laryngol Otol 1990;104:477-81.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]