Retromaxillary Pneumatization of Posterior Ethmoid Air … · ethmoid disease more safely and effectively. 17 Retromaxillary pneumatization of posterior ethmoid ... (Syngo CT 2012B;

Original Research—Sinonasal Disorders

Retromaxillary Pneumatization ofPosterior Ethmoid Air Cells: NovelDescription and Surgical Implications

Otolaryngology–Head and Neck Surgery2016, Vol. 155(2) 340–346� American Academy ofOtolaryngology—Head and NeckSurgery Foundation 2016Reprints and permission:sagepub.com/journalsPermissions.navDOI: 10.1177/0194599816639943http://otojournal.org

Islam R. Herzallah, MD, PhD1,2, Faisal A. Saati, MD2,3,Osama A. Marglani, MD, FRCSC2,4, and Rehab F. Simsim, MD2

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

Abstract

Objective. Retromaxillary pneumatization of posterior eth-moid (PE) air cells is an area that is yet to have appropriatedescription in rhinologic literature.

Study Design. Case series with chart review.

Setting. Tertiary care hospital.

Subjects and Methods. First, 524 sides in 262 paranasal sinuscomputed tomography scans were analyzed: 350 normalsides were examined for PE pneumatization lateral to thesagittal plane of the medial wall of maxillary sinus posteriorly,and 174 diseased sides were similarly reviewed to check howpathology may affect identification and measurements. Followingthat, 153 operated sides in 84 cases prepared for revision endo-scopic sinus surgery (ESS) were studied for residual diseasedcells at different anatomic locations.

Results. Overall, retromaxillary PE pneumatization was identi-fiable in 416 of the 524 sides (79.4%). Lateral retromaxillaryextension varied from 0.5 to 12.3 mm (mean 6 SD, 4.8 6

2.3 mm). This area of pneumatization is bounded anteroinfer-iorly by the junction between the posterior and superiorwalls of the maxillary sinus. Three cell types were describeddepending on the degree of lateral extension (type I, \3 mm;type II, 3-6 mm; type III, .6 mm). This cell, which we referto as the Herzallah cell, was distinguishable from the anteriorethmoid Haller cell and was found to have residual disease in50.3% of cases prepared for revision ESS.

Conclusion. Retromaxillary extension of PE air cells varies con-siderably and requires attention during ESS. Residual undis-sected retromaxillary cell is a common finding in revision ESSand can contribute to inadequate disease clearance.

Keywords

posterior ethmoids, paranasal sinus, anatomy variations, ana-tomical classification, lamina papyracea, Haller cell, ethmo-maxillary sinus, sphenomaxillary plate, lateral sphenoidrecess, revision functional endoscopic sinus surgery, preven-tion of residual disease, chronic rhinosinusitis, computed

tomography, imaging, radiology, nasal polyps, allergic fungalsinusitis

Received December 21, 2015; revised February 11, 2016; accepted

February 29, 2016.

Understanding endoscopic paranasal sinus (PNS) anat-

omy is the key for safe and effective endoscopic

sinus surgery (ESS). Identification of anatomic varia-

tions is equally important in preoperative planning and intrao-

perative orientation. Therefore, rhinologic literature is rich

with studies that describe endoscopic landmarks and the dif-

ferent 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 endo-

scopic 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

1Department of Otorhinolaryngology, Faculty of Medicine, Zagazig

University, Zagazig, Egypt2ENT Department, King Abdullah Medical City, Makkah, Saudi Arabia3Department of Otolaryngology, Al-Hada Armed Forces Hospital, Taif,

Saudi Arabia4Department of Otolaryngology, Umm Al-Qura University, Makkah, Saudi

Arabia

Corresponding Author:

Islam R. Herzallah, MD, PhD, Department of Otorhinolaryngology, Faculty

of Medicine, Zagazig University, Egypt.

Email: [email protected]

at SOCIEDADE BRASILEIRA DE CIRUR on August 5, 2016oto.sagepub.comDownloaded from

http://oto.sagepub.com/

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 recog-

nized and frequently missed during ESS, particularly for resi-

dents 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 pneumati-

zation 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 preo-

perative 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 attach-

ment 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).

Two otolaryngology residents among the study authors

(F.A.S. and R.F.S.) independently performed CT scan exam-

inations, and their results were compared to determine inter-

rater 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 per-

formed 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 sur-gery. 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 prepara-

tion for revision surgery. The following ethmoid pneumati-

zation 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,

Figure 1. At posterior ethmoids (PEs), lamina papyracea (LP)slopes inferolaterally (white arrow). A line is drawn along themedial wall of maxillary sinus (MMS) posteriorly, and degree of ret-romaxillary lateral extension is measured (double-headed arrow).MS, maxillary sinus.

Herzallah et al 341



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 relia-

bility was examined via the intraclass correlation coefficient

(ICC) to determine the degree of agreement on measure-

ments 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 6 SD age of the 262 patients (524 sides) was

38.6 6 16.0 and 37.02 6 14.9 years in the normal and dis-

eased 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 6 2.4

mm). This retromaxillary pneumatization was bounded ante-

roinferiorly by the junction between the posterior and super-

ior 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 later-

ally, the inferior orbital wall gradually contributed to the

superior wall of the retromaxillary cell (Figure 3B, 3C).

For descriptive purposes, 3 types of retromaxillary pneumati-

zation were described depending on the degree of lateral exten-

sion: 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

Figure 2. Identification of the retromaxillary posterior ethmoid (RM.PE) in coronal, sagittal, and axial planes. MS, maxillary sinus; SS, sphe-noid sinus.

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. Inpanel A, on the patient’s right side, there is no retromaxillary pneumatization of posterior ethmoids.

342 Otolaryngology–Head and Neck Surgery 155(2)



(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 pneumatiza-

tion was not part of the PEs but was rather caused by ante-

rior extension of the sphenoid into the retromaxillary area

(Figure 4). In the remaining 16 sides (4.6%), no retromax-

illary pneumatization was identifiable, neither from the PEs

nor from the sphenoid sinus (Figure 3A, right side).

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).

The ICC for measurements of PE retromaxillary lateral

extension as taken by the 2 examiners was 0.88 (95% confi-

dence 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 identi-

fiable in 141 of the 174 diseased sides (81%). In these cases,

lateral extension ranged from 0.65 to 10.4 mm (4.8 6 2.2

mm). In 25 of 174 sides (14.4%), retromaxillary pneumatiza-

tion was formed by anterior extension of the sphenoid sinus,

while in the remaining 8 sides (4.6%), no retromaxillary pneu-

matization was identifiable, neither from the PEs nor from the

sphenoid sinus. In 6 of the 25 sides with retromaxillary sphe-

noid 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% confi-

dence 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

Figure 5. Although retromaxillary posterior ethmoids (Herzallah [Hz] cells) are partly related to the inferior orbital wall, these should bedifferentiated from the infraorbital anterior ethmoid air cells (Haller [Ha] cells).

Figure 4. Anterior extension (asterisk) of sphenoid sinus (SS) to the posterior wall of the maxillary sinus (MS). RM.PE, retromaxillary pos-terior ethmoid pneumatization: note relationship to lateral sphenoid extension (LS) and upper pterygopalatine fossa (PPF).

Herzallah et al 343



measurements between the normal and diseased sides (P =

.94), indicating that the presence of pathology did not inter-

fere 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 retromax-

illary extension varied from 0.5 to 12.3 mm (4.8 6 2.3

mm). In 84 of 524 sides (16%), retromaxillary pneumatiza-

tion 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 pneuma-

tization. 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 6 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 pneumati-

zation; 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 dif-

ference 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%), supraor-

bital ethmoid pneumatization (9.8%), and Haller cells

(5.2%). Retromaxillary sphenoid extension had residual dis-

ease 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 cur-

rent 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 com-

pared with other anatomic variations. In fact, one could

hardly find any article that specifically addresses this pneu-

matization 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 retro-

maxillary 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 ret-

romaxillary 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 distin-

guish them from their Haller counterpart (Figure 5).

Anterior extension of the sphenoid sinus to form retro-

maxillary 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 signifi-

cantly 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 6 0.5 SD

and thus constitutes the most common category that sur-

geons 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 intrao-

perative 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 eth-

moid cells. Since retromaxillary PE cells are in direct rela-

tionship 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 retromaxil-

lary 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 ret-

romaxillary PE pneumatization. Residual undissected retro-

maxillary 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.

Acknowledgments

We thank Mr Ammar Alwaheib, RT, and the staff at Radiodiagnosis

Department in King Abdullah Medical City for their conscientious

assistance and help.

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 analy-

sis, 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.

Herzallah et al 345



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Documents

Retromaxillary Pneumatization of Posterior Ethmoid Air … · ethmoid disease more safely and effectively. 17 Retromaxillary pneumatization of posterior ethmoid ... (Syngo CT 2012B;