ORIGINAL ARTICLE

Infraorbital ethmoid (Haller) cells: a cone-beam computedtomographic study

Filiz Namdar Pekiner • M. Oguz Borahan •

Asım Dumlu • Semih Ozbayrak

Received: 25 September 2013 / Accepted: 19 January 2014

� Japanese Society for Oral and Maxillofacial Radiology and Springer Japan 2014

Abstract

Objective Infraorbital ethmoid (Haller) cells are exten-

sions of the anterior ethmoid sinus into the floor of the orbit

and superior aspect of the maxillary sinus. The aim of this

retrospective study was to evaluate the frequency, volume,

and surface area of infraorbital ethmoid cells on cone-beam

computed tomography (CBCT).

Methods In this retrospective study, 150 CBCT evalua-

tions were determined for infraorbital ethmoid cells. One

CBCT examination was carried out for each of the patients

and interpreted for the presence of infraorbital ethmoid

cells. Volumetric measurements were performed using

CBCT scans. All of the CBCT scans were assessed and

analyzed using MIMICS 14.0 software.

Results In the 150 CBCT evaluations, 65 (43.3 %) were

noted as having infraorbital ethmoid cells. In these patients,

47 (31.3 %) were unilateral and 18 (12 %) bilateral. The

majority of the cells were round in shape. The frequency of

unilocular infraorbital ethmoid cells occurring unilaterally

was highly significant. There were no significant differ-

ences in the volume and surface area of right and left

infraorbital ethmoid cells between males and females.

Conclusions Infraorbital ethmoid cells were well dem-

onstrated and the volume and surface area of infraorbital

ethmoid cell could be measured on CBCT scans. These

cells may provide useful differential diagnoses for patients

suffering from orofacial pain of sinus origin.

Keywords Cone-beam computed tomography �Infraorbital ethmoid cells � Volume � Surface area

Introduction

There are ethmoid air cells present at birth, and they con-

tinue to grow until late adolescence or until the sinus wall

attains compact bone. Pneumatization progresses in the

posterior direction, increasing the posterior cells until the

medial and lateral walls of the ethmoid sinuses are parallel.

The final stage of ethmoid pneumatization may create

convex, medial, and lateral walls with posterior cells that

are larger and fewer than the anterior cells. When the final

stage of pneumatization includes medial and inferior air

cell extensions, extramural air cells are formed, such as

agger nasi cells (area of the anterior attachment of the

middle concha), concha bullosa cells (when the extension

progresses in the inferomedial direction toward the medial

ethmoid cells), and infraorbital ethmoid cells (when the

pneumatization progresses in the inferolateral direction

toward the infraorbital portion) [1–4].

Infraorbital ethmoid cells were first identified by Albrect

von Haller (1708–1777) in 1765 and subsequently named

after him, i.e. Haller cells [5, 6]. Infraorbital ethmoid cells

are defined as air cells situated beneath the ethmoid bulla

along the roof of the maxillary sinus and the most inferior

portion of the lamina papyracea, including air cells located

within the ethmoid infundibulum [6–8]. The presence of

infraorbital ethmoid cells has been related to different

disease processes and symptoms, including sinusitis,

headaches, and mucoceles [4, 9].

Anatomic variants with potential impacts on surgical

safety occur frequently and need to be specifically sought

as part of preoperative evaluations [10, 11]. However, it is

F. N. Pekiner (&) � M. O. Borahan � A. Dumlu � S. Ozbayrak

Department of Oral Diagnosis and Radiology, Faculty of

Dentistry, Marmara University, Guzelbahce Buyukciftlik Sok.

No: 6, Nisantasi, 34365 Istanbul, Turkey

e-mail: fpekiner@gmail.com

123

Oral Radiol

DOI 10.1007/s11282-014-0167-3

well documented that some of the anatomical variations of

the paranasal sinuses can predispose to sinus pathology or

even complicate sinus surgery, and infraorbital ethmoid

cells are no exception. These cells are frequently seen as

incidental findings on computed tomography (CT) exam-

inations of paranasal sinuses [12, 13].

Computed tomography has become the gold standard for

diagnostic imaging, as it provides sufficient spatial reso-

lution and its dataset can be used for computer-assisted

endoscopic sinus surgery. However, CT in general is

known to be responsible for most of the collective medical

radiation dose of the population in modern societies. Cone-

beam CT (CBCT) produces three-dimensional information

on the facial skeleton and teeth and is increasingly being

used in many dental specialties. It was primarily introduced

for orthodontic indications, because an alternative imaging

modality needs to have reasonable diagnostic value for

diagnosis of rhinosinusitis. According to the literature,

CBCT should have great advantages over CT with regard

to radiation exposure. Compared with previous single-

source sinus CT studies, the eye dosages of the proposed

protocols are lower by a factor of 19–23 in milliamperages

[14, 15]. Conventional multidetector CT scans of the sinus

expose the patient to 0.96–2.00 mSv of radiation, which is

equivalent to approximately 100 chest X-rays. An adult

sinus scan using CBCT can decrease this dose to

0.04–0.17 mSv. The lower radiation doses achievable with

CBCT technology are desirable to avoid unnecessary

radiation of radiosensitive organs such as the eye lens and

thyroid gland [16–19]. Preliminary evidence suggests that

CBCT may be suited to specific imaging tasks in the

context of bony structural evaluations, enabling low-dose

assessment of sinonasal anatomy [20].

The aim of this retrospective study was to evaluate the

frequency, volume, and surface area of infraorbital ethmoid

cells on CBCT scans.

Materials and methods

Patient data

The subjects for this retrospective study consisted of all

150 patients (75 females, 75 males; age range 20–68 years;

mean age 33.24 ± 11.89 years) who visited the Depart-

ment of Oral Diagnosis and Radiology at the Faculty of

Dentistry, Marmara University and underwent a single

CBCT examination picked up from the picture archiving

and communications system (PACS) from 2012 to 2013.

The CBCT examinations were performed using a ProMax

3D Mid machine (Planmeca Oy, Helsinki, Finland). The

ProMax 3D Mid CBCT machine was operated at 90 kVp

and 10 mA with a 16 9 16-cm field of view. Assessment

of CBCT scans was performed directly on a monitor screen

(Monitor 23-inch Acer 1920 9 1080 pixel HP Recon-

struction PC). Patients with a history of trauma and/or

surgery involving the maxillofacial region, systemic dis-

eases affecting growth and development, or clinical and/or

radiographic evidence of developmental anomalies/

pathologies affecting the maxillofacial region were exclu-

ded from the study. All digital images were viewed using

Romexis 2.92 software (Planmeca Oy). The data obtained

from the CBCT images were transferred to a network

computer workstation, where the volumetric changes of

infraorbital ethmoid cells were measured using MIMICS

14.0 software (Materialise Europe, World Headquarters,

Leuven, Belgium). For assessment of infraorbital ethmoid

cell volumes, coronal images were selected. The threshold

limits were applied with a minimum limit of -1024

Hounsfield units (HU) and a maximum of -300 HU. The

infraorbital ethmoid cells were cropped in the slice in

which their widest size was apparent (Fig. 1). Axial and

sagittal views were also visualized and cropping was per-

formed (Fig. 2a, b). After any connections with the outer

anatomic landmarks were eliminated, three-dimensional

images of the left and right infraorbital ethmoid cells were

constructed and their volumes were calculated (Fig. 3).

The study protocol was approved by the Local Committee

of Research and Ethics of Yeditepe University.

Observer

One oral and maxillofacial radiologist (MOB) interpreted

all of the images. Recognition of infraorbital ethmoid cells

was made if an anatomical variation fulfilled the following

criteria suggested by Ahmad et al. [6]: (1) well-defined

round, oval, or teardrop shaped radiolucency, single or

multiple, unilocular or multilocular, with a smooth border,

which may or may not appear corticated; (2) located in the

medial to infraorbital foramen; (3) all or most of the border

of the entity visible on the CBCT image; and (4) inferior

border of the orbit lacked cortication or remained indis-

tinguishable in areas superimposed by the entity. In addi-

tion, we used criteria for defining infraorbital ethmoid cells

as air cells, of any size, located along the medial portion of

the orbital floor and/or the lamina papyracea inferior to the

bulla ethmoidalis, and continuous with the ethmoid cap-

sule. Continuity with the ethmoid capsule distinguishes

infraorbital ethmoid cells from an infraorbital recess of the

maxillary sinus [5].

Statistical analysis

The data were analyzed with Statistical Package for Social

Sciences (SPSS) for Windows 15.0 (SPSS Inc., Chicago, IL).

Descriptive statistical methods (mean, SD, and frequency)

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were used for evaluation of the data. The Chi square test was

used to evaluate comparisons between qualitative data. The

statistical significance of differences among quantitative

data was analyzed by the Mann–Whitney U test. Values of

p \ 0.05 were interpreted as significant.

Results

Of the 150 patients, 74 (49.3 %) were aged 20–29 years,

34 (22.7 %) were 30–39 years, 23 (15.3 %) were

40–49 years, and 19 (12.7 %) were C50 years. In the 150

Fig. 1 Cropped images of infraorbital ethmoid cells. The defined borders are clearly seen in the coronal, sagittal, and axial views

Fig. 2 Axial (a) and sagittal (b) views of infraorbital ethmoid cells

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CBCT evaluations, 65 (43.3 %) were interpreted as having

infraorbital ethmoid cells. Bilateral infraorbital ethmoid

cells were present in 18 (12.0 %) CBCT images (Fig. 4a),

while 47 (31.3 %) had unilateral infraorbital ethmoid cells

(Fig. 4b). Thus, a total of 65 cases with infraorbital ethmoid

cells were identified, of which 18 (27.7 %) had cells on the

right side, 29 (44.6 %) had cells on the left side, and 18

(27.7 %) had cells on both sides. There was a highly sig-

nificant difference in the frequency of infraorbital ethmoid

cells between the right side (n = 36; 55.3 %) and the left

side (n = 47; 72.3 %). There were no significant differences

in the frequency of infraorbital ethmoid cells between males

and females and in the frequency of infraorbital ethmoid

cells according to age groups (Table 1). No significant dif-

ferences were observed in the distribution of infraorbital

ethmoid cells between males and females (Table 2).

Of the total infraorbital ethmoid cells, 50 (76.9 %) had a

round shape and 15 (23.1 %) had an ovoid shape. Among

the female patients with infraorbital ethmoid cells, 22

(75.9 %) had a round shape and 7 (24.1 %) had an ovoid

shape. In the male patients with infraorbital ethmoid cells,

28 (77.8 %) had a round shape and 8 (22.2 %) had an

ovoid shape. There were no significant differences in the

distribution of infraorbital ethmoid cells with respect to sex

and age according to shape (Table 3; Fig. 5a, b).

No significant differences in the volume and surface

area of the right and left infraorbital ethmoid cells were

found between males and females (Table 4).

Discussion

Several researchers have studied the prevalence of infra-

orbital ethmoid cells using CT images. In these studies, the

wide range of prevalence (4.7–45.1 %) probably arose

from the different protocols used for image acquisition as

well as differences in the populations studied [21–24].

Raina et al. [3] examined panoramic radiographs, and their

observed prevalence (16 %) was within the range of the

previous studies. Meanwhile, Ahmad et al. [6] evaluated

images according to a sole panoramic radiographic study

on infraorbital ethmoid cells and cited a much higher

prevalence of 38.2 %. Raina et al. [3] explained that this

lack of coordination could have resulted from variations in

the populations, sample sizes, and subjective judgments

pertaining to the presence or absence of infraorbital eth-

moid cells. In the present study examining CBCT images,

the prevalence (43.3 %) was within the range of the pre-

vious studies. Mathew et al. [20] observed that the preva-

lence of infraorbital ethmoid cells was relatively high

(60 %). These authors explained that small-sized infraor-

bital ethmoid cells could easily be missed in the interslice

intervals involved in multislice CT scans.

Unilateral occurrence of infraorbital ethmoid cells was

found to be highly significant. Similar to other studies

[6, 21, 24, 25], unilateral infraorbital ethmoid cells were

seen in a larger number of cases than bilateral infraorbital

Fig. 4 Coronal CBCT images showing bilateral (a) and unilateral (b) infraorbital ethmoid cells

Fig. 3 Three-dimensional model of infraorbital ethmoid cells

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ethmoid cells. The presence of bilateral infraorbital eth-

moid cells was reported to vary from 26 to 50 % [6, 21, 24,

25]. According to our study, the prevalence of bilateral

infraorbital ethmoid cells (12 %) fell below the range of

these previous studies.

Raina et al. [3] found no significant difference in the

occurrence of infraorbital ethmoid cells on the right and

left sides on panoramic radiographs. Moreover, they clas-

sified the shapes of the infraorbital ethmoid cells as round,

ovoid, or teardrop and concluded that the majority of the

infraorbital ethmoid cells were round or ovoid [3]. Ahmad

et al. [6] found equal distributions on the right and left

sides on panoramic radiographs. There was a highly sig-

nificant difference in the frequency of infraorbital ethmoid

cells between the right side (n = 36; 55.3 %) and the left

side (n = 47; 72.3 %) in the present study. In addition, the

majority of the infraorbital ethmoid cells were round in

shape (76.9 %), while fewer infraorbital ethmoid cells

were ovoid in shape (23.1 %). The variety of the results

compared with other studies may have arisen from dis-

crepancies in the radiological techniques, ethnicities of

populations, and sample sizes.

As far as the maxillary sinuses are concerned, there are

very few studies related to their size in general [26–28],

and to our knowledge, this is the first report to describe

evaluations of the volume and surface area of infraorbital

ethmoid cells. In the present study, we observed that there

were no significant differences in the volume and surface

area of the right and left infraorbital ethmoid cells between

males and females.

Several published reports have indicated the clinical

significance of infraorbital ethmoid cells. Even if infra-

orbital ethmoid cells are not diseased, their presence may

narrow the ethmoid infundibulum or the ostium of the

maxillary sinus. Such anatomical limitations may result

in persistent rhinosinusitis [6]. A case study reported

headache that was attributed to the presence of infraor-

bital ethmoid cells [21]. Mathew et al. [20] suggest that

the role of infraorbital ethmoid cells in sinus disease

should be evaluated on an individual basis depending on

the size of infraorbital ethmoid cells and clinical evi-

dence of sinus inflammation. A limitation of our study is

that we did not investigate the association between

infraorbital ethmoid cells and maxillary sinusitis in our

patients.

In conclusion, the results of the present study indicate

that CBCT can provide a clear illustration of infraorbital

ethmoid cells in a considerable number of cases. The

present study attempted to explore the characteristics of

infraorbital ethmoid cells on CBCT images. A description

of infraorbital ethmoid cells on CBCT images may prove

vital in counting the differential diagnoses for patients with

orofacial pain. Further CBCT evaluation of subjects with

definitive maxillary sinusitis is strongly recommended to

Table 1 Distributions of infraorbital ethmoid cells with respect to

sex and age (numbers of patients)

Infraorbital ethmoid cells p

Present (n = 65) Absent (n = 85)

n (%) n (%)

Sex

Male 36 (48.0) 39 (52.0) 0.249

Female 29 (38.7) 46 (61.3)

Age (year)

20–29 32 (43.2) 42 (56.8) 0.416

30–39 18 (52.9) 16 (47.1)

40–49 7 (30.4) 16 (69.6)

C50 8 (42.1) 11 (57.9)

Data were compared by the Chi square test

Table 2 Distributions of infraorbital ethmoid cells with respect to

sex and age according to sides

Infraorbital ethmoid cells p

Unilateral

(n = 47)

Bilateral

(n = 18)

Absent

(n = 85)

n (%) n (%) n (%)

Sex

Male 25 (33.3) 11 (14.7) 39 (52.0) 0.437

Female 22 (29.3) 7 (9.3) 46 (61.3)

Age (year)

20–29 20 (27.0) 12 (16.2) 42 (56.8) 0.283

30–39 16 (47.1) 2 (5.9) 16 (47.1)

40–49 5 (21.7) 2 (8.7) 16 (69.6)

C50 6 (31.6) 2 (10.5) 11 (57.9)

Data were compared by the Chi square test

Table 3 Distributions of infraorbital ethmoid cells with respect to

sex and age according to shapes

Infraorbital ethmoid cells p

Round (n = 50) Ovoid (n = 15)

n (%) n (%)

Sex

Male 28 (77.8) 8 (22.2) 0.855

Female 22 (75.9) 7 (24.1)

Age (year)

20–29 24 (75.0) 8 (25.0) 0.777

30–39 13 (72.2) 5 (27.8)

40–49 6 (85.7) 1 (14.3)

C50 7 (87.5) 1 (12.5)

Data were compared by the Chi square test

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assess the association between infraorbital ethmoid cells

and maxillary sinusitis.

Acknowledgments This study was presented at the 19th European

Congress of Dentomaxillofacial Radiology held from 22–27 June

2013 in Bergen, Norway. It was supported by the Marmara University

Scientific Research Project Council (Project no: SAG-D-100413-

0121).

Conflict of interest Filiz Namdar Pekiner, M. Oguz Borahan, AsımDumlu, and Semih Ozbayrak declare that they have no conflict of

interest.

Human rights statements and informed consent All procedures

followed were in accordance with the ethical standards of the

responsible committee on human experimentation (institutional and

national) and with the Helsinki Declaration of 1975, as revised in

2008 (5). Informed consent was obtained from all patients for being

included in the study.

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