ORIGINAL ARTICLE

Folia Morphol.

Vol. 82, No. 2, pp. 339–345

DOI: 10.5603/FM.a2022.0033

Copyright © 2023 Via Medica

ISSN 0015–5659

eISSN 1644–3284

journals.viamedica.pl

Morphometric variants of the paranasal sinuses in a Mexican population: expected changes according to age and gender

N.G. Jasso-Ramírez*1R.E. Elizondo-Omaña*1J.L. Treviño-González2A. Quiroga-Garza13I.A. Garza-Rico4K. Aguilar-Morales1G. Elizondo-Riojas4S. Guzmán-López1
1Universidad Autonoma de Nuevo Leon, School of Medicine, Human Anatomy Department, Monterrey, Nuevo Leon, Mexico
2Universidad Autonoma de Nuevo Leon, University Hospital “Dr. José Eleuterio González”, Otorhinolaryngology Department, Monterrey, Nuevo Leon, Mexico
3Intituto Mexicano del Seguro Social, Delegación de Nuevo León, General Sugery, Monterrey, Nuevo Leon, Mexico
4Universidad Autonoma de Nuevo Leon, University Hospital “Dr. José Eleuterio González”, Radiology and Imaging Department, Monterrey, Nuevo Leon, Mexico

[Received: 18 January 2022; Accepted: 12 March 2022; Early publication date: 29 March 2022]

Background: There are developmental variations in the paranasal sinuses. Our objective was to determine their dimensions and volume stratified by age and sex and define the expected growth pattern.
Materials and methods: A retrospective, observational study was performed including computed tomography (CT) of patients between 1 and 20 years of age. The volumes of the frontal, sphenoid, and maxillary sinuses were obtained.
Results: A total of 210 CT were included with a mean age of 10 ± 6.1 years, 106 (50.5%) were female. Groups were categorised in ranges of 5 years. Spearman correlation coefficients between the right and left sides were 0.843, 0.711, 0.916 for the frontal, sphenoid and maxillary sinuses. Post-hoc for the categorical age groups demonstrated statistically significant differences with values of p < 0.01, except between age groups 11–15 against ≥ 16 years of age (p = 0.8). Gender-related differences were evident with a higher air volume in girls in the 5–10-year-old group, while boys predominated in the rest of the groups.
Conclusions: Computed tomography is ideal for pre-surgical sinus assessment. The maximum volume of paranasal sinuses is reached at the age of 15. There is a clear volumetric difference between age and gender groups. There is a direct relationship between a volume and its contralateral counterpart. (Folia Morphol 2023; 82, 2: 339–345)
Key words: paranasal sinuses, paediatrics, morphology, age groups, gender

Address for correspondence: J.L. Treviño-González, MD, or S. Guzman-Lopez, MD, PhD, Departamento de Otorinolaringologia, Hospital Universitario “Dr. Jose E. Gonzalez”, Universidad Autónoma de Nuevo León, Francisco I. Madero and Jose E. Gonzalez sin número, Colonia Mitras Centro Monterrey, Nuevo León, México, 64460, tel: +52 8183332917, e-mail: jose.trevinog@uanl.mx or dr.santos.anato@gmail.com

*Both authors participated equally in the study, and are both in the position of first author.

This article is available in open access under Creative Common Attribution-Non-Commercial-No Derivatives 4.0 International (CC BY-NC-ND 4.0) license, allowing to download articles and share them with others as long as they credit the authors and the publisher, but without permission to change them in any way or use them commercially.

INTRODUCTION

The paranasal sinuses (PNS) are hollow cavities lodged inside the facial bones. The size of the sinuses is variable and depends particularly on the age and gender of the individual [28]. Their function is controversial [18]. Most believe the PNS support respiratory function and resonance, however, because they constitute the largest viscerocranial cavity, the air space it occupies is the most important anatomical feature [17, 19].

Sadler reports the frontal sinus does not develop before the age of 3, but reaches its maximum development between the ages of 4 and 8 years and continues its growth until 14–16 years [29]. The ethmoidal sinus has a faster development in the anterior ethmoid region and a complete development around 12 years of age with increased convexity of its lateral and middle walls in the last phases [34]. The sphenoid sinus begins to be pneumatized around the age of 2, progresses anterior-posteriorly around the age of 5, and completes its development at the age of 15 in half of the cases, with the other half continuing until the age of 30 [43]. The maxillary sinus initially grows in a transverse pattern (> 2 years of age) and then vertically (0–2 years and 7–10 years) reaching the level of the nasal passages, the nasolacrimal duct, and the zygomatic recess at the age of 12 [33, 43]. All sinuses are usually asymmetrical to their contralateral pair [29].

Knowledge of the variations in the development of the PNS is a clinically relevant issue [37]. Genetic diseases, environmental conditions, and infections can affect its structure and variations [6, 10, 35, 40]. Understanding age-related changes in their dimensions and volume can aid in radiographs and computed tomography (CT) assessment for the identification of pathology [20, 21, 35]. Examples include hypoplasia (incomplete development) and sinus atelectasis (known as silent sinus syndrome, which is a rare finding in general but found in the majority of patients with orbital floor fracture [38], usually seen on CT as an opacified sinus with retraction of its walls towards light and associated loss of volume [31]. For these instances, it is helpful to have normal range values and clinical morphometric parameters in the diagnostic approach of pathologies such as sinusitis or sinus dysmorphism [3]. Morphometric parameters are also important in the preoperative evaluation for functional endoscopic sinus surgery (FESS) as this procedure can jeopardize the anatomical variations of vital structures adjacent to the sinuses [3, 27].

Currently, nasosinusal endoscopic surgery has become the surgical procedure of choice to resolve chronic and recurrent nasosinusal inflammatory pathologies that do not respond to medical treatment. These minimally invasive techniques allow clear visualization of the sinuses and successful surgical treatment [11, 12, 42].

Previous studies have calculated PNS volume using dry skulls [1], cadaveric specimens [39], CT images [32, 44], and magnetic resonance imaging [21]. The use of CT scan instead of simple radiography for PNS evaluation was introduced by Zinreich et al. [44] in 1987.

Due to the craniofacial variations between populations, our objective is to establish morphometric parameters stratified by age and gender in our population as a guide for endoscopic surgery and a reference for a specific pathology approach.

MATERIALS AND METHODS

A retrospective, descriptive, observational, and cross-sectional study was performed. PNS morphometrics were obtained from CTs of patients between 0 and 20 years of age, from the database of the Radiology and Imaging Department of the University Hospital. Exclusion criteria included those patients with injury or pathology of the PNS or a history of PNS surgery. CTs with poor technical quality were eliminated.

The images were acquired using a helical tomography (Light Speed Plus CT, GE Medical Systems) with collimation of 0.625 mm, a table speed of 15.0 mm per second, a cutting interval of 1.25 mm parallel to the temporal bone with 50 mA and 120 kV and a 512 × 512 matrix. Volume operations were performed with multiplanar reformatting using Centricity Universal Viewer. The studies were assessed separately by two expert head and neck radiologists.

Bilateral measurements were made for frontal, sphenoid, and maxillary sinuses’ volume (Figs. 1–3). Data were registered in a database and stratified by age, gender, and laterality. Age groups were categorised in ranges of 5 years of age. Patients less than 1-year-old were included quantifiable as 0 years.

Figure 1. Three-dimensional reconstruction of aerial structures of the skull of a 4-year-old patient. Scale with marks for each centimetre.
Figure 2. Three-dimensional reconstruction of paranasal sinuses of a 10-year-old patient; A. Lateral view in a sagittal slice; B. Frontal view with a coronal slice; C. Superior view in a transverse slice. Scale with marks for each centimetre.
Figure 3. Aerial reconstruction of paranasal sinuses; A. Frontal sinuses; B. Sphenoidal sinuses; C. Maxillary sinuses; D. Lateral view of frontal, ethmoidal cells and sphenoidal sinuses (left to right); E. Anterior view of frontal sinuses, ethmoidal cells, maxillary sinuses, and nasal turbinates. All images correspond to a fully grown young woman of 18 years of age. Scale with marks for each centimetre.
Statistical analysis

The database was analysed using the SPSS statistical package version 20 programme (IBM, Armonk, NY, USA), for Windows 7. Normality tests were applied with Kolmogorov-Smirnoff and for each of the groups, the mean ± standard deviation for each measurement parameter was determined independently. The Mann-Whitney U test was used to determine the significance of the differences between men and women for each morphometric parameter. Kruskal-Wallis tests were performed to compare the results of each measurement parameter for the different age groups, interpreting a value of p ≤ 0.05 as significant. The results are presented in Tables 1 and 2.

Table 1. Paranasal sinuses morphometrics stratified by laterality and gender

Volume [cm3]

Mean

Total (n = 210)

P-value

Males (n = 104)

Females (n = 106)

P-value

Frontal

Right

7.460

6.77 ± 6.70

0.0843

7.76 ± 7.49

5.80 ± 5.71

0.096

Left

8.14 ± 10.82

8.81 ± 10.08

7.50 ± 11.52

0.243

Sphenoid

Right

8.796

8.38 ± 7.08

0.711

8.52 ± 7.39

8.25 ± 6.8

0.832

Left

9.21 ± 8.58

9.81 ± 8.41

8.62 ± 8.74

0.181

Maxillary

Right

27.572

27.24 ± 13.79

0.916

28.73 ± 14.37

25.78 ± 13.11

0.179

Left

27.90 ± 10.20

28.50 ± 14.62

27.31 ± 13.83

0.716

Table 2. Difference between categorical age between the parameters of volume and length of the paranasal sinuses

Volume [cm3]

Categorical age

< 5 (n = 60, 28.6%)

6–10 (n = 50, 23.8%)

11–15 (n = 50, 23.8%)

> 16 (n = 50, 23.8%)

Frontal

Right

0.79 ± 1.41

3.94 ± 3.30

10.18 ± 4.96

13.38 ± 6.75

Left

1.14 ± 2.26

4.59 ± 4.37

12.22 ± 6.52

16.05 ± 16.68

Sphenoid

Right

2.65 ± 4.19

6.29 ± 4.69

11.19 ± 6.67

14.54 ± 5.93

Left

2.84 ± 3.25

7.08 ± 5.84

13.34 ± 10.01

14.87 ± 7.91

Maxillary

Right

12.33 ± 7.66

23.88 ± 8.27

35.95 ± 9.50

39.80 ± 7.76

Left

12.74 ± 7.84

23.82 ± 7.07

35.51 ± 9.09

42.57 ± 8.79

Ethical considerations

The study was previously reviewed and approved by the University’s Ethics and Research Committees, receiving the registration number AH16-00005, making sure it adheres to the Helsinki declaration and national and international standards of research. The authors declare no financial or commercial gain for the realisation of this study. Also, the authors declare no conflict of interest. None of the imaging studies were performed for the purposes of this study.

RESULTS

A total of 210 axial head and neck CT scans were included, with similar distribution in gender (104 [49.5%] male, 106 [50.5%] female). The mean age was 10 ± 6.06 years.

The mean volumes and lengths stratified by gender are reported in Table 1 and by age in Table 2. In the post-hoc analysis for non-parametric tests for categorical age groups, all groups were statistically significant with values of p < 0.01, with the exception of the group aged 11 to 15 years with the group over 16 years of age. Significance among the volume means groups having a value of p > 0.8 in all the variables compared between the groups.

DISCUSSION

There has been a continued interest in the sinuses and nasal passages to correlate with the ideal approach for paranasal sinus surgery and surgical approach of associated structures. Computed tomographies are considered the gold standard for the evaluation of PNS due to the invasiveness of an endoscopic approach and its possible complications such as infection, bleeding, perforation, among others [15].

Although a higher time consumption was involved, for this study, manual segmentation was used to create three-dimensional models based on the aerial reconstruction of the PNS, to better identify and delimit each structure. This allows non-invasive visualisation, simulation, and precise quantitative measurements of internal body structures. The PNS volumes are the most important index due to the large differences shown between the individuals [15].

Several authors (Table 3) have categorized their population using different age groups. Karakas and Kavakli [16] divided their population into 5-year age groups (total five groups) starting at the age of 5 years. Wolf et al. [43] evaluated the development of the sinuses in 102 cadaverous specimens and divided them into four age groups: newborn, 1 to 4 years old, 4 to 8 years old, and 8 to 12 years old. In this study ventrodorsal, cephalocaudal, and mediolateral length measurements were performed, however without differentiating between genders. The group of newborns showed anterior and posterior ethmoid cells almost completely developed in number and a spherical or pyramidal shape for the maxillary sinus. Lorkiewicz-Muszyńska et al. [21] studied their population individually by age and also reported the maxillary sinus was present at birth. They observed the ethmoidal and maxillary region expanding rapidly in the first few years, and similar to our results, they identified frontal and sphenoid sinuses pneumatisation. Sadler described, frontal sinuses are always absent at birth, but evident in boys by the age of 2, and until the age of 4 in girls [29].

Table 3. Differences in paranasal sinuses volume between populations

Author, Year, Reference, Country

Imaging method

Sample size (men, women)

Gender

Age groups

Mean volume [cm3] (men, women)

Maxillary

Frontal

Sphenoid

Ariji et al., 1993 [2]

Japan

CT

230 (116, 114)

116

4–84

4.56

114

6–96

4.76

Barghouth et al., 2002 [3]

Switzerland

MRI

179 (103, 76)

< 1

0.14

0.01

2

1.6

0.17

4

4.1

0.57

8

10.1

1,77

12

17.1

3.44

16

25.9

5.82

Jun et al., 2005 [14]

Korea

CT

173 (84, 89)

15 (11, 4)

0–10

8.94, 4.23

26 (17, 9)

11–20

19.45, 9.06

22 (8, 14)

21–30

2.40, 15.85

25 (14, 11)

31–40

22.28, 13.97

35 (15, 20)

41–50

18.39, 11.94

17 (8, 9)

51–60

19.42, 13.32

22 (9, 13)

61–70

14.29, 13.69

11 (2, 9)

71–80

20.26, 12.03

Karakas and Kavakli, 2005 [16]

Turkey

CT

91 (47, 44)

18 (9, 9)

5–10

6.02, 6.81

1.19, 1.23

2.96, 3.14

19 (10, 9)

11–15

11.17, 9.8

4.20, 1.75

5.40, 4.85

17 (8, 8)

16–20

14.64, 14.03

7.57, 3.54

7.50, 5.43

18 (10, 9)

21–25

15.98, 10.90

8.83, 3.51

9.68, 8.71

19 (10, 9)

> 25

15.50, 11.33

8.41, 3.50

7.88, 1.14

Emirzeoglu et al., 2007 [9]

Turkey

CT

77 (39, 38)

39

18–72

19.8

7.5

7.7

38

16.0

4.1

6.1

Sahlstrand-Johnson et al., 2011 [30]

Sweden

CT

60 (28, 32)

20

18–32

14.4

20

33–49

16.6

20

50–65

15.2

Masri et al., 2013 [23]

Malaysia

CT

144

0–6

1.81, 2.81

7–12

10.2, 9.26

13–20

17.3, 13.5

21–30

19.75, 14.5

Degermenci et al., 2016 [7]

Turkey

CT*

361 (18, 180)

100 (50, 50)

< 5

3.23, 2.89

100 (50, 50)

6–10

3.61, 7.18

101 (51, 50)

11–15

11.03, 10.40

60 (30, 30)

> 16

14.46, 12.58

Lorkiewicz-Muszyńska et al., 2015 [21]

Poland

CT

170

40

0–4

1.97, 2.25

30

4–8

5.48, 4.92

100

8–17

12.15, 11.35

Marino et al., 2016 [22]

USA

CT

20 (6, 14)

6,14

28–66

27.99

5.61

9.33

Cohen et al., 2018 [5]

Israel

CT

201 (101, 100)

100 (50, 50)

25–64

15.7, 13.9

4.9, 3.7

3.7, 2.4

100 (51, 50)

> 65

13.1, 10.5

3.8, 2.4

3.9, 2.5

Özer et al., 2018 [26]

Turkey

CT

144 (89, 55)

10.24, 8.33

Jasso-Ramirez et al., 2020

Mexico

CT

210 (104, 106)

59 (28, 31)

< 5

14.12, 11.04

1.38, 0.56

3.59, 1.95

51 (25, 26)

6–10

22.25, 25.45

3.55, 4.97

6.27, 7.08

50 (26, 24)

11–15

36.72, 34.64

12.76, 9.50

13.15, 11.30

50 (25, 25)

> 16

43.41, 38.95

16.21, 13.2

14.20, 15.18

Most studies focus on the maxillary sinuses, lacking data on the sphenoid and frontal sinuses. The sphenoid sinus is considered the most variable cavity in the human body and is of great relevance for optimal surgical access to the pituitary gland [36]. In addition, its’ pneumatisation may provide access to other parts of the skull base [41]. We report it present at birth, with a continued volume growth throughout all age groups. The degree and direction of pneumatisation play a crucial role in the planning of surgical procedures.

According to Wolf et al. [43] at 8 years, pneumatisation has progressed considerably and the nasal cavity and sinuses have almost completed their development and reached adult proportions. Karakas and Kavakli [16] reported the volume increased in both sexes up until the age of 25, then progressively decreased thereafter.

In the maxillary sinuses, we report maximum volumes reached at the age of 16–20, similar to that reported by Jun et al. [14] and Lorkiewicz-Muszyńska et al. [21]. Like the maxilla, the frontal sinus has also taken a tetrahedral shape and the sphenoid sinus has reached its permanent size, but its shape is still developing. We determine the greatest change in volume was between the ages of 11 and 15, a contrast to the results of Ariji et al. [2] who reported PNS volumes continued increasing until the age of 20 and then decreased. Similarly, Karakas and Kavakli [16] found the highest means for PNS volumes in the 21-to-25-year age group in men, and in the 16-to-20-year age group for the maxillary sinuses of women. Masri et al. [23] evaluated maxillary sinus and reported sizes and volume increased from birth until 30 years of age; men also exhibited larger maxillary sinus volume than women in 7–12 (p < 0.01) and 21–30 (p < 0.01) age groups. Size sexual dimorphism was evident in most age groups for the maxillary sinus.

Emirzeglou et al. [9] reported the PNS is typically larger in men than in women. Cohen et al. [5] also demonstrated larger sinus volumes for men. The means for adult PNS were 12.75cc, 4.00cc, and 2.92cc for the maxillary, sphenoid and frontal sinuses, respectively. These compare much smaller than our mean in a paediatric population with 27.57cc, 8.79cc, and 7.46cc, respectively for the same PNS (Table 3).

Laterality dysmorphism was not evident in the vertical, horizontal, and anteroposterior axes of our measurements. However, gender-related differences were evident in the 5-to-10-year-old group, in which girls had higher volumes than boys. Other studies observed no statistically significant correlation between the measured volumes with age, gender, or side [2, 7, 9, 30]. In our categorical age groups, boys tended to have higher air volumes, agreeing with Cohen et al. [5] that the difference noted could not be solely explained by the general difference in skull size between genders, which has also been demonstrated in other studies [8, 24–26]. Marino et al. [22] consider the postnatal development of the frontal and sphenoid sinuses as a predisposing factor for greater variation in its development and final volumes.

It’s important to evaluate the characteristics of the PNS, to correlate with rhinosinusitis diseases, and other bone defects [4, 6, 13]. Our study is the first to evaluate morphometrics in a Latino population, resulting in significantly higher volumes than other populations. However, it is limited by the lack of mastoid cells measurement due to the difficulty and inaccuracy when assessment.

CONCLUSIONS

The use of automated three-dimensional volume reconstructions is a precise tool for PNS morphometrics and accurate knowledge of their anatomy. The CT allows not only a full evaluation of the sinuses and the adjacent anatomical structures but also for the planning of the FESS.

Our results evidence higher volumes at a younger age, than reported in other populations. There is a clear volumetric difference with respect to categorized age groups and gender. The correlation between a volume and its contralateral counterpart is also demonstrated. Head and neck surgeons must consider the PNS differences in size and shape in paediatric patients, from those found in adults. It is important to understand that each age has a specific anatomical characteristic directly related to the development of the facial part of the skull and teething. The size and the disparity in the location of the floor of the nose and the floor of the maxillary sinus in children predispose them to more complications than expected in adults.

Conflict of interest: None declared

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