Retromaxillary Pneumatization of Posterior Ethmoid Air Cells

Abstract

Objective

Retromaxillary pneumatization of posterior ethmoid (PE) air cells is an area that is yet to have appropriate description in rhinologic literature.

Study Design

Case series with chart review.

Setting

Tertiary care hospital.

Subjects and Methods

First, 524 sides in 262 paranasal sinus computed tomography scans were analyzed: 350 normal sides were examined for PE pneumatization lateral to the sagittal plane of the medial wall of maxillary sinus posteriorly, and 174 diseased sides were similarly reviewed to check how pathology may affect identification and measurements. Following that, 153 operated sides in 84 cases prepared for revision endoscopic sinus surgery (ESS) were studied for residual diseased cells at different anatomic locations.

Results

Overall, retromaxillary PE pneumatization was identifiable in 416 of the 524 sides (79.4%). Lateral retromaxillary extension varied from 0.5 to 12.3 mm (mean ± SD, 4.8 ± 2.3 mm). This area of pneumatization is bounded anteroinferiorly by the junction between the posterior and superior walls of the maxillary sinus. Three cell types were described depending on the degree of lateral extension (type I, <3 mm; type II, 3-6 mm; type III, >6 mm). This cell, which we refer to as the Herzallah cell, was distinguishable from the anterior ethmoid Haller cell and was found to have residual disease in 50.3% of cases prepared for revision ESS.

Conclusion

Retromaxillary extension of PE air cells varies considerably and requires attention during ESS. Residual undissected retromaxillary cell is a common finding in revision ESS and can contribute to inadequate disease clearance.

Keywords

posterior ethmoids paranasal sinus anatomy variations anatomical classification lamina papyracea Haller cell ethmomaxillary sinus sphenomaxillary plate lateral sphenoid recess revision functional endoscopic sinus surgery prevention of residual disease chronic rhinosinusitis computed tomography imaging radiology nasal polyps allergic fungal sinusitis

Understanding endoscopic paranasal sinus (PNS) anatomy is the key for safe and effective endoscopic sinus surgery (ESS). Identification of anatomic variations is equally important in preoperative planning and intraoperative orientation. Therefore, rhinologic literature is rich with studies that describe endoscopic landmarks and the different anatomic scenarios that surgeons may encounter.^1-4

Endoscopic, radiologic, and anatomic studies that have helped surgeons better perform ESS are numerous. Examples include description of agger nasi and frontal sinus infundibular cells, providing surgeons with better orientation during the endonasal frontal sinus approach.^5-7 Description of Onodi and Haller cells was similarly valuable in helping appropriate and safer clearance of ethmoid air cells as well as proper sphenoid and maxillary sinusotomies, respectively.^8-10 For the same reason, we have maintained a focus on exploring the endoscopic anatomy in several projects over the past decade.^11-13

Despite these anatomic descriptions, residual disease after ESS continues to occur and is not uncommon.^14-16 A recent study showed that missed ethmoid cells over the lamina papyracea (LP) and skull base is one of the most common findings in revision sinus surgery.¹⁴

The recent classification of LP position in the endoscopic field was introduced to help surgeons address anterior ethmoid disease more safely and effectively.¹⁷ Retromaxillary pneumatization of posterior ethmoid (PE) cells is yet another endoscopically important area that seems to be poorly recognized and frequently missed during ESS, particularly for residents and surgeons with less experience. The lack of studies describing this anatomic location easily explains the paucity of knowledge to appropriately tackle this region. Therefore, we have conducted this extensive work to describe this pneumatization of PE air cells and to investigate its importance from the endoscopic perspective.

Subjects and Methods

Study Design

We conducted a retrospective analysis of PNS computed tomography (CT) scans that were obtained for adult patients as part of evaluation for their sinonasal or anatomically related disorders. Enrollment criteria included adult PNS CT scans performed at our institution, King Abdullah Medical City, between January 2013 and August 2015, at 1-mm section thickness and interval, with the exclusion of those with sinonasal neoplasms, invasive fungal sinusitis, or craniofacial abnormalities.

First, a total of 524 sides in 262 PNS CT scans were reviewed: 350 normal sides that had clear ethmoid sinuses on PNS imaging for different purposes (eg, headache, nasal septal deviation, preoperative evaluation for endoscopic dacryocystorhinostomy, or unilateral pathology on the other side) and 174 sides with different ethmoid pathologies, with the above exclusion criteria. Following that, we reviewed 153 operated sides in 84 patients who had their CT scans as part of their evaluation for persistent symptoms and preoperative preparation for revision ESS. The retrospective analysis was approved by the Institutional Review Board at King Abdullah Medical City before commencement of the study.

CT Examination and Analysis

All PNS CT scans reviewed at our institution were performed with a 64-slice Siemens Somatom Definition Scanner (Syngo CT 2012B; Siemens Healthcare, Forchheim, Germany). CT scans were obtained at 1-mm section thickness and interval, 120 to 320 mA, 120 kV, 1-second rotation time, and a 16- to 18-cm field of view.

CT examination protocol in normal sides

The coronal plane where PE air cells start was first identified behind the basal lamella of middle turbinate (MT) by following the MT attachment as it changes from vertical to horizontal. The LP forming the lateral boundary of PE air cells tends to slope laterally as it goes inferior to join the orbit floor. PE air cells follow the LP slope forming an inferolateral extension below the orbit and in relation to the posterosuperior corner of the maxillary sinus ( Figure 1 ). Here, a vertical line that passes along the medial wall of the maxillary sinus (MMS) posteriorly was drawn and termed the MMS line. The degree of lateral extension of PE cells beyond the MMS line was then measured. To ensure appropriate identification, examination of CT scans was carried out in the axial, sagittal, and coronal planes ( Figure 2 ).

Figure 1.

At posterior ethmoids (PEs), lamina papyracea (LP) slopes inferolaterally (white arrow). A line is drawn along the medial wall of maxillary sinus (MMS) posteriorly, and degree of retromaxillary lateral extension is measured (double-headed arrow). MS, maxillary sinus.

Figure 2.

Identification of the retromaxillary posterior ethmoid (RM.PE) in coronal, sagittal, and axial planes. MS, maxillary sinus; SS, sphenoid sinus.

Two otolaryngology residents among the study authors (F.A.S. and R.F.S.) independently performed CT scan examinations, and their results were compared to determine interrater reliability (detailed in the Statistical Analysis section). The final measurements were then reported by calculating the mean of the 2 examiners’ results.

Additionally, CT scans were reviewed for the presence of other related anatomic variations: PE extension into the roof of maxillary sinus (ethmomaxillary sinus),^18-20 anterior extension of the sphenoid sinus to the retromaxillary area, and infraorbital extension of anterior ethmoid air cells (Haller cells).

CT examination in diseased sides

The same analysis was performed on sides with different PNS pathologies to ensure that presence of disease did not interfere with appropriate identification and measurement. The 174 diseased sides included 51 sides with chronic rhinosinusitis without nasal polyps, 68 sides with bilateral allergic nasal polyps, and 55 sides with allergic fungal rhinosinusitis.

CT examination protocol in cases imaged for revision sinus surgery

The presence of residual undissected diseased ethmoid air cells was checked in 153 previously operated sides. Sixty-six sides were originally operated for allergic fungal rhinosinusitis, 60 for allergic nasal polyps, and 27 for chronic rhinosinusitis without nasal polyps. All cases had the new CT done as part of the routine preoperative preparation for revision surgery. The following ethmoid pneumatization areas were examined for residual disease: ethmoid cells over the skull base and LP, frontal recess cells, agger nasi cells, supraorbital ethmoid pneumatization, Onodi cells, and Haller cells. Retromaxillary pneumatization was also analyzed in this study.

Statistical Analysis

Statistical analyses were performed with SPSS 22.0 for Windows (IBM Corp, Armonk, New York). Interrater reliability was examined via the intraclass correlation coefficient (ICC) to determine the degree of agreement on measurements between the 2 observers. Measurements were also compared between right and left sides through paired-samples t test and between the normal and diseased sides through independent-samples t test. The significance level was set at P < .05.

Results

The average ± SD age of the 262 patients (524 sides) was 38.6 ± 16.0 and 37.02 ± 14.9 years in the normal and diseased groups, respectively, with no significant difference between the 2 groups (P > .05; range, 18-88 and 18-79 years, respectively). Overall, 58.4% of patients were men and 41.6% women, again with no significant difference in sex distribution between groups (P > .05).

Findings in Normal Sides (350 Sides)

Pneumatization of PE air cells lateral to MMS line was identifiable in 275 of the 350 sides (78.6%). In these cases, lateral extension ranged from 0.5 to 12.3 mm (4.8 ± 2.4 mm). This retromaxillary pneumatization was bounded anteroinferiorly by the junction between the posterior and superior walls of the maxillary sinus ( Figure 2 , sagittal view). When the lateral extension was relatively shallow, this cell was related mainly to the lower part of the LP ( Figure 3A , left side). As the retromaxillary PEs extended more laterally, the inferior orbital wall gradually contributed to the superior wall of the retromaxillary cell ( Figure 3B , 3C ).

Figure 3.

Degrees of retromaxillary posterior ethmoid lateral extension: (A) type I, <3 mm; (B) type II, 3-6 mm; (C) type III, >6 mm. In panel A, on the patient’s right side, there is no retromaxillary pneumatization of posterior ethmoids.

For descriptive purposes, 3 types of retromaxillary pneumatization were described depending on the degree of lateral extension: type I, pneumatization of PE air cells lateral to MMS line is <3 mm; type II, 3-6 mm; and type III, >6 mm. In other words, type I is a relatively shallow pneumatization; type II is the median common degree of retromaxillary lateral extension; and type III is a deep retromaxillary cell ( Figure 3 ).

In the 275 sides with identifiable retromaxillary PE cells, 66 sides (24%) were of type I; 136 (49.5%), type II; and 73 (26.5%), type III. Twelve sides had ethmomaxillary sinus, all of which were of type III pneumatization.

In 59 of 350 sides (16.9%), retromaxillary pneumatization was not part of the PEs but was rather caused by anterior extension of the sphenoid into the retromaxillary area ( Figure 4 ). In the remaining 16 sides (4.6%), no retromaxillary pneumatization was identifiable, neither from the PEs nor from the sphenoid sinus ( Figure 3A , right side).

Figure 4.

Anterior extension (asterisk) of sphenoid sinus (SS) to the posterior wall of the maxillary sinus (MS). RM.PE, retromaxillary posterior ethmoid pneumatization: note relationship to lateral sphenoid extension (LS) and upper pterygopalatine fossa (PPF).

The retromaxillary PE air cell, which we also refer to as Herzallah cell, was distinguishable from the infraorbital anterior ethmoid pneumatization known as Haller cell, which is part of the anterior group of ethmoid cells and was identified in 26 (7.4%) of the examined normal sides ( Figure 5 ).

Figure 5.

Although retromaxillary posterior ethmoids (Herzallah [Hz] cells) are partly related to the inferior orbital wall, these should be differentiated from the infraorbital anterior ethmoid air cells (Haller [Ha] cells).

The ICC for measurements of PE retromaxillary lateral extension as taken by the 2 examiners was 0.88 (95% confidence interval: 0.86-0.91) at a P value <.001, indicating high interrater reliability with statistical significance. There was no statistically significant difference in measurements between right and left sides (P > .05).

Findings in Diseased Sides (174 Sides)

Pneumatization of PE air cells lateral to MMS line was identifiable in 141 of the 174 diseased sides (81%). In these cases, lateral extension ranged from 0.65 to 10.4 mm (4.8 ± 2.2 mm). In 25 of 174 sides (14.4%), retromaxillary pneumatization was formed by anterior extension of the sphenoid sinus, while in the remaining 8 sides (4.6%), no retromaxillary pneumatization was identifiable, neither from the PEs nor from the sphenoid sinus. In 6 of the 25 sides with retromaxillary sphenoid extension (24%), this area of pneumatization was spared of the disease that involves the PE air cells ( Figure 4 ).

In the 141 diseased sides with identifiable retromaxillary PE cells, 34 sides (24.1%) were of type I; 67 (47.5%), type II; and 40 (28.4%), type III. Five sides had ethmomaxillary sinus, all of which were of type III pneumatization.

The ICC for measurements of PE retromaxillary lateral extension as taken by the 2 examiners was 0.87 (95% confidence interval: 0.82-0.90) at a P value <.001, indicating high interrater reliability with statistical significance. Additionally, there was no statistically significant difference in the measurements between the normal and diseased sides (P = .94), indicating that the presence of pathology did not interfere with proper identification and measurement.

Findings in All Examined Sides Combined (524 Sides)

Overall, retromaxillary PE pneumatization was identifiable in 416 of the 524 examined sides (79.4%). Lateral retromaxillary extension varied from 0.5 to 12.3 mm (4.8 ± 2.3 mm). In 84 of 524 sides (16%), retromaxillary pneumatization was formed by anterior extension of the sphenoid sinus. In the remaining 24 of 524 sides (4.6%), no retromaxillary pneumatization was identifiable, neither from the PEs nor from the sphenoid sinus.

In the 416 sides with identifiable retromaxillary PE cells, 100 sides (24%) were categorized as type I, 203 (48.8%) as type II, and 113 (27.2%) as type III. Seventeen sides had ethmomaxillary sinus, all of which were of type III pneumatization. Haller cells were identifiable in 36 of the 524 examined sides (6.9%).

Findings in Operated Sides Prepared for Revision ESS (153 Sides)

The average age of the 84 patients was 34.4 ± 14.0 years. Forty-eight patients (57.1%) were men and 36 (42.9%) women. The highest prevalence of residual undissected cells was in the anterior ethmoid air cells along the LP (97 sides, 63.4%), anterior ethmoid cells along the skull base (61.4%), PE cells along the LP (60.8%), PE cells along the skull base (57.5%), frontal recess cells (56.2%), agger nasi cells (54.2%), and PE retromaxillary cells in 77 sides (50.3%).

Pneumatization of PE air cells lateral to MMS line was identifiable in 119 of the 153 sides (77.8%). In these cases, 33 sides (27.7%) were of type I PE retromaxillary pneumatization; 54 (45.4%), type II; and 32 (26.9%), type III. Residual PE retromaxillary cells were found in 20 sides (60.6%) of type I pneumatization, 35 (64.8%) of type II, and 22 (68.8%) of type III. No statistically significant difference was found in the prevalence of residual cells among the 3 categories of PE retromaxillary pneumatization (P > .05).

Other, less common ethmoid pneumatization areas that had residual disease included Onodi cells (16.3%), supraorbital ethmoid pneumatization (9.8%), and Haller cells (5.2%). Retromaxillary sphenoid extension had residual disease in 10.5% of the examined sides.

Discussion

Residual ethmoid disease continues to be one of the common findings in revision ESS.^14-16 This fact needs to be acknowledged and should alert us that further understanding of the endoscopic ethmoid anatomy is necessary to help the training of less experienced surgeons. Fortunately, the current progress in sinonasal imaging and the increasing use of intraoperative navigation are continuously helping us in the 3-dimensional understanding of the endoscopic anatomy. Figure 6 demonstrates intraoperative identification of the retromaxillary PE cell along with CT navigation in different planes. Video 1 (at www.otojournal.org/supplemental) also demonstrates intraoperative dissection of a retromaxillary PE cell along with other closely related landmarks.

Figure 6.

Intraoperative identification of retromaxillary posterior ethmoids. MS, maxillary sinus; SS, sphenoid sinus opening.

Retromaxillary PE pneumatization is an area that has received poor attention in the rhinologic literature as compared with other anatomic variations. In fact, one could hardly find any article that specifically addresses this pneumatization or describes its different anatomic scenarios. Yet, Haller cells—or infraorbital pneumatization of the anterior ethmoids in the region of the ostiomeatal complex—have been extensively described before, with a prevalence that usually lies in the range of 3% to 18%.^21-24 Although retromaxillary PEs are also partly located in relation to the orbit floor, these should be differentiated from Haller cells given the different anatomic location that makes each of them of particular importance during ESS. However, we have come across studies on sinonasal anatomic variations in which retromaxillary PEs were misinterpreted as Haller cells.^25,26 This can be explained by the lack of appropriate description and has guided us to use the term Herzallah cell to distinguish them from their Haller counterpart ( Figure 5 ).

Anterior extension of the sphenoid sinus to form retromaxillary pneumatization has been described.^21,22,26,27 In such cases, the intervening wall between the maxillary and sphenoid sinuses was termed the sphenomaxillary plate, and this variation was reported in 11% to 15% of cases.^21,22 However, the current study shows that retromaxillary PE pneumatization is, by far, more common the sphenoid one (79.4% vs 16%). This differentiation is important, since sphenoid retromaxillary extension can be spared in cases of PE disease, an observation that was reported in 24% of the diseased sides with sphenoid retromaxillary extension in our series ( Figure 4 ). We have to mention that retromaxillary pneumatization should also be differentiated from the lateral sphenoid recess, which is rather a pneumatization in the pterygoid base behind the upper part of the pterygopalatine fossa ( Figure 4 ).

In this study, we have demonstrated different lateral extension degrees of the retromaxillary PEs and typed them accordingly. Although an ethmomaxillary sinus has been described in about 2% of cases,^18-20 it has received limited citation, which may be explained by the lack of thorough analysis of this variation. Therefore, we believe the current description of retromaxillary PE pneumatization significantly clarifies the variations in this region.

For descriptive purposes, we have proposed to classify the depth of retromaxillary cell lateral extension for easier comparison among sides. The middle group (3-6 mm) was chosen since it roughly represents the mean depth ± 0.5 SD and thus constitutes the most common category that surgeons may encounter. The other 2 groups (<3 and >6 mm) represent relatively shallow and deep retromaxillary PE pneumatization, respectively. The categorization presented in this study is not meant to ask the surgeon to take intraoperative measurements but rather to appreciate the relative depth of retromaxillary PE pneumatization, to help him or her appropriately tackle this region. Note, however, that no statistically significant difference was cited in the prevalence of residual disease among the 3 types in revision cases.

In accordance with our results, several investigators have found residual undissected ethmoid air cells over the LP and skull base in >60% of patients undergoing revision ESS.^14-16 The current study shows that retromaxillary PE cells are as likely to be left undissected as other major ethmoid cells. Since retromaxillary PE cells are in direct relationship with the lower part of the LP, this would explain why missing this region would contribute to the frequent finding of residual disease over the LP. Proper orientation to and dissection of the retromaxillary PE cells would ensure proper clearance of the ethmoid disease over the LP. Furthermore, since this area of pneumatization is located anterior to the lateral sphenoid pneumatization, proper dissection of the retromaxillary cell would help in better exposure of the lateral sphenoid extension. Although no statistically significant difference was found in the rate of residual cells among the 3 degrees of PE retromaxillary extension, attention to the relative depth of the retromaxillary PE cell should help surgeons and residents perform the closely related endoscopic work more safely and effectively.

Conclusion

The current study introduces a novel description of the retromaxillary PE pneumatization. Residual undissected retromaxillary cell is a common finding in revision ESS. The recognition of this anatomic variation should help residents in training and would improve surgeons’ ability to perform better clearance of ethmoid air cells.

Author Contributions

Islam R. Herzallah, inventing and developing the research idea, reviewing literature, defining the study protocol and methodology, preparing Institutional Review Board forms, designing computed tomography (CT) analysis and measurement protocol, mentoring work implementation, thorough review and examination of CTs, performing statistical analysis, writing the manuscript and preparing figures; Faisal A. Saati, preparing a list of available CTs, performing CT measurements, data collection, contribution to manuscript writing, data interpretation, statistical analysis and figures preparation, and review and approval of the final manuscript; Osama A. Marglani, contribution to manuscript writing and data interpretation and analysis, assistance in preparing a list of available CTs, review and approval of the final manuscript; Rehab F. Simsim, performing CT measurements and data collection, contribution to manuscript writing, figures preparation, data interpretation and analysis, and review and approval of the final manuscript.

Disclosures

Competing interests: None.

Sponsorships: None.

Funding source: None.

Footnotes

Acknowledgements

We thank Mr Ammar Alwaheib, RT, and the staff at Radiodiagnosis Department in King Abdullah Medical City for their conscientious assistance and help.

No sponsorships or competing interests have been disclosed for this article.

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