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ORIGINAL ARTICLE

A comparative analysis of aerodynamic


and anatomic characteristics of upper
airway before and after mini-implant–
assisted rapid maxillary expansion
Hongyi Tang, Panpan Liu, Qiuping Xu, Yingyue Hou, and Jing Guo
Jinan, China

Introduction: The objective of this research was to observe changes in aerodynamics and anatomic character-
istics of the upper airway after mini-implants assisted rapid maxillary expansion and to evaluate the correlation
between the 2 changes of the upper airway in young adults. Methods: Thirty consecutive patients (mean age,
23.82 6 3.90 years; median, 24.5 years; 9 males, 21 females) were involved. Cone-beam computed tomography
was taken before activation and over 3 months. Three-dimensional models of the upper airway were
reconstructed on the basis of cone-beam computed tomography. The anatomic characteristics of the upper
airway, including volume, area, transverse, and sagittal diameter, were measured. The aerodynamic
characteristics of the upper airway were calculated on the basis of 3-dimensional models using computational
fluid dynamics. The correlation between the changes in aerodynamics and anatomic characteristics of the
upper airway was explored. Results: The enlargements of the volume of the total pharynx, nasopharynx, and
oropharynx were found (9.99%, 20.7%, and 8.84%, respectively). The minimum cross-sectional area
increased significantly (13.6%). The airway resistance (R) and maximum velocity (Vmax) decreased
significantly in both the inspiration and expiration phase (inspiration: R, 26.8%, Vmax, 15.7%; expiration: R,
24.7%, Vmax, 16.5%). The minimum wall shear stress reduced significantly only in the inspiration phase
( 26.3%). The correlations between decreased R and increased volume and minimum cross-sectional area
were observed. Conclusions: Mini-implants assisted rapid maxillary expansion is an effective device for
improving anatomic characteristics represented by the total volume of the upper airway and minimum cross-
sectional area, which contributed to the respiratory function depending on the favorable changes of
aerodynamic characteristics including resistance, velocity, and minimum wall shear stress. (Am J Orthod
Dentofacial Orthop 2021;159:e301-e310)

O
bstructive sleep apnea (OSA) is a breathing disor- clinical diseases.1-3 In addition, some studies reported
der during sleep characterized by recurrent apnea craniofacial disharmonies such as midface hypoplasia
and hypopnea, which is associated with narrow and narrow dentition were predisposing factors in the
upper airway, obesity, hypertension, and other adverse occurrence and progress of OSA, according to the
influence of upper airway and muscular function.4,5
OSA was a multifactor disease, and orthodontic treatment
From the Department of Orthodontics, School and Hospital of Stomatology, was only an effective method in treating OSA that was
Shandong University, Shandong Key Laboratory of Oral Tissue Regeneration,
and Shandong Engineering Laboratory for Dental Materials and Oral Tissue
mainly caused by structural stenosis of the upper airway
Regeneration, Jinan, Shandong, China. because of skeletal craniofacial disharmony. In contrast,
All authors have completed and submitted the ICMJE Form for Disclosure of the effects of orthodontic treatment were limited for
Potential Conflicts of Interest, and none were reported.
Address correspondence to: Jing Guo, Department of Orthodontics, School and
OSA caused by other factors such as heredity, overweight,
Hospital of Stomatology, Shandong University, Shandong Key Laboratory of Oral and dyslipidemia.
Tissue Regeneration, and Shandong Engineering Laboratory for Dental Materials Rapid maxillary expansion (RME) is a conventional
and Oral Tissue Regeneration, Number 44-1, Wenhua W Rd, Jinan, Shandong
250012, China; e-mail, guojing@sdu.edu.cn.
treatment method correcting transverse maxillary defi-
Submitted, September 2020; revised, November 2020; accepted, December ciency.6 Some studies have reported the effects of RME
2020. could increase the volume of the upper airway,7-9 and
0889-5406/$36.00
Ó 2021 by the American Association of Orthodontists. All rights reserved.
Cistulli et al10 first suggested RME could be a therapy
https://doi.org/10.1016/j.ajodo.2020.12.013 for patients with OSA in 1998. However, conventional
e301
e302 Tang et al

tooth anchored RME had dental side effects, such as


buccal tipping of maxillary first molars11 and the reduc-
tion of buccal attachment of alveolar bone, and was not
suitable for nongrowing patients whose midpalatal su-
ture had been fused.12
To reduce the undesirable side effects, mini-implants
assisted rapid maxillary expansion (MARME) was de-
signed to provide skeletal expansion guaranteed by 4
mini-implants and minimize the dental side effects
compared with RME.13,14 Some studies have pointed
out MARME could cause the enlargement of the upper
airway15,16 and be considered as an effective treatment Fig 1. MARME.
to alleviate the symptoms of OSA in adults.17
Computational fluid dynamics (CFD) is an engineering excluded because of loose mini-implants, and 3 patients
technique used to solve problems relating to fluid or were excluded because of the defection of CBCT data. Ul-
airflow by simulating the access that the fluid or airflow timately, 30 patients were involved in this study. (mean
is going through a specific tube.18 CFD has been widely age, 23.82 6 3.90 years; median, 24.5 years; 9 males,
used to simulate the airflow of the upper airway on the 21 females; range, 18-33 years). The study was approved
basis of 3-dimensional (3D) data from CBCT, which could by the relative ethical commission, and the informed con-
assess the respiratory function of patients.19-21 It could sent was signed by each patient.
provide quantitative parameters describing the flow The inclusion criteria for this study were shown as
process of air in the upper airway by exhibiting the followed: (1) aged .18 years; (2) maxillomandibular
contours of aerodynamics characteristics such as skeletal transverse discrepancy 3 mm or greater (Fig 1);
pressure drop, velocity, and wall shear stress. (3) no history of expansion treatment or orthognathic
The effects of MARME on the upper airway of 1 pa- surgery; and (4) no severe dentofacial anomalies such
tient using CFD analysis was reported.17,22 However, the as a cleft lip or palate.
changes of 1 patient might not illustrate the reliability Each patient was treated by maxillary skeletal expan-
and universality of the effects of MARME. In addition, sion type II (BioMaterials Korea, Seoul, Korea) developed
previous studies evaluated the changes of the upper by Brunetto et al23 at the University of California Los An-
airway after MARME on the basis of CBCT in the stand- geles, which consisted of 2 stainless steel arms soldered
ing position. Based on these studies, the changes in a to the bands on the maxillary first molars. After the
group of patients on the basis of CBCT in supine position bands were bonded to the maxillary first molars, 4
had not been analyzed. In the optional location of taking mini-implants (diameter, 1.5 mm; length, 11 mm;
CBCT, the supine position was the position that could Mplant Series, BioMaterials Korea) were placed along
describe the relatively narrow state of the upper airway, with guided slots in the midpalatal region under local
and the standing position was the position that could infiltration anesthesia (Fig 1). The jackscrew was orien-
describe the relatively unobstructed state of the upper tated on the midpalatal region generally, which was acti-
airway. Both positions were valuable positions for taking vated one sixth of a turn (0.13 mm) each day. The
CBCT. In our study, we have gathered a group of pa- amount of expansion was set depending on the severity
tients, including 30 subjects from which the CBCT data of each patient, which ranged from 40-60 turns, and the
were of subjects in the supine position. duration of expansion ranged from 40 to 60 days. The
This study aimed to assess the changes of anatomic retention after activation was 3 months, allowing bone
and aerodynamics characteristics of the group of pa- formation in the separated maxillary suture.
tients on the upper airway and to evaluate the correla- CBCT scans (5G; NewTom, Verona, Italy) were ob-
tion between aerodynamics characteristics calculated tained before activation (T0) and over 3 months (T1).
by CFD and the anatomy of the upper airway. The CBCT device was set at 110 kVp; 7.33 mA; 0.3-
mm voxel size; scan time, 4.8 seconds; and field of
view of 18 cm 3 16 mm. To assure the reliability of
MATERIAL AND METHODS
the measurements from the airway segmentation, we
From 2019 to 2020, patients who were diagnosed with checked the position of each patient when taking
transverse deficiency of maxillary and have undergone CBCT. Each patient was scanned in the supine position
MARME were consecutively enrolled in this retrospective in which the Frankfort horizontal plane (FHP) was
study. During the collection process, 2 patients were perpendicular to the floor, keeping the teeth in centric

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Fig 2. Volume of the upper airway according to the 3 segments.

occlusion, the tongue in the position at the end of swal- generate tetrahedral volume mesh. According to the
lowing (against the palate), breathing smoothly, no complexity of the model of the upper airway, a typical
swallowing15 and the duration of the scan was about grid consisted of approximately 2 million tetrahedral
15 seconds which was not difficult for our patients to cells (Fig 5).
keep constant. We had tried our best to ensure the uni- After mesh generation, the 3D mesh was imported
formity of the head position and posture of our patients into software (FLUENT 16.0; ANSYS) for airflow simula-
during CBCT before and after the treatment. The unifor- tion. The steady-state Reynolds Averaged Navier-Stokes
mity assured the reliability of the measurements to the formulation together with the laminar model was used
greatest extent. The CBCT data were saved as Digital Im- to model aerodynamic characteristics of the upper
aging and Communications in Medicine format. airway. Second-order discretization schemes were
The Digital Imaging and Communications in Medi- used, and the coupling between velocity and pressure
cine data were imported into Dolphin Imaging software was achieved using the SIMPLE algorithm.24 The density
(version 11.8; Dolphin Imaging and Management Solu- and the viscosity of the air were set as 1.225 kg/m3 and
tions, Chatsworth, Calif). The images were reoriented 1.79 3 10 05 kg/m/s, respectively, which was acquies-
along the palatal suture, tangent to the nasal floor and cent in the software. An inlet volume flow rate of
parallel to the FHP. The upper airway was divided into 166 mL s 1 (10 l min 1) was set in the airflow simula-
3 segments: nasopharynx, oropharynx, and hypophar- tion, and the standard atmospheric pressure of 0 Pa
ynx, and all the descriptions and definitions of anatomic was set for the inlet.25 The air within the upper airway
parameters were shown in Figures 2 and 3 and Table I. was thought to be adiabatic.24 In the inspiration phase,
The CBCT data were imported into Mimics software the inlet boundary was set at the line passing through
(version 19.0; Materialise, Leuven, Belgium). The upper PNS and S, and the outlet boundary was set at the plane
airway was highlighted by setting the threshold between across the C4 point parallel to the FHP. Conversely, the
1024 and 360 Hounsfield Units. The anterior upper expiration phase was simulated by setting an inlet at
boundary was the line passing through PNS and S, the the plane across the C4 point parallel to the FHP and
upper boundary was the roof of the nasopharynx, and outlet at the line passing through PNS and S. The itera-
the lower boundary was the plane across the C4 point tion numbers were 400 steps.
(the most anterior inferior point of the fourth cervical Airway resistance (R) was calculated by the following
vertebra) parallel to the FHP. All 3D models were ex- formula: R 5 DP/Q. The total pressure drop between the
ported as stereolithography files (Fig 4). inlet and outlet of the upper airway (DP) was computed
All the models of the upper airway were loaded into by Pmax Pmin, and Q was the volume flow rate, which
software (ICEM 16.0; ANSYS, Canonsburg, Pa) to was a constant. All the parameters were measured again

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Fig 3. Anatomic measurements: A, CSAmin; B, transverse diameter of CSAmin; C, sagittal diameter of


CSAmin; D, cross-sectional area of interface1; E, transverse diameter of interface1; F, sagittal diameter
of interface1; G, cross-sectional area of interface2; H, transverse diameter of interface2; I, sagittal
diameter of interface2.

by 1 researcher (H.T.) after 1 week, and the average value distribution and the homogeneities of variances were
was applied in this study. checked by the Shapiro-Wilk test and the Levene test,
respectively. A paired t test was used for the comparison
Statistical analysis of normally distributed data between T0 and T1 and the
All the data were measured repeatedly after 1 week by Wilcoxon test for the comparison of nonnormally
1 operator (H.T.), and the intraclass correlation coeffi- distributed data. Pearson correlation test was used to
cient was 0.91-0.97, indicating repeat agreement analyze the correlation of normally distributed data,
regarding all measurements. and Spearman correlation test was used to assess the
Statistical analysis was performed with SPSS software correlation of nonnormally distributed data. A P
(version 21; SPSS Inc, Chicago, Ill). The normality of data value \0.05 was determined as a statistical significance.

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Table I. The descriptions and definitions of relative parameters


Parameters Descriptions and definitions
CSAmin The minimum cross-sectional area of the upper airway
Transverse diameter of CSAmin The transverse line on the greatest transverse dimension at CSAmin
Sagittal diameter of CSAmin The sagittal line on the greatest sagittal dimension at CSAmin
Total volume The anterior border is the line passing through PNS and S; the inferior border
is the line parallel to the FHP passing through C4 (the anterior and inferior
point of the fourth cervical vertebra), and the posterior border is the
pharyngeal posterior wall
Superior boundary The line passing through PNS and S
Nasopharyngeal volume The anterior border is the line passing through PNS and S, the inferior border
is the line parallel to the FHP passing through PNS, and the posterior
border is the pharyngeal posterior wall
Interface1 The line parallel to the FHP passing through PNS
Transverse diameter of interface1 The transverse line on the greatest transverse dimension at interface1
Sagittal diameter of interface1 The sagittal line on the greatest sagittal dimension at interface1
Oropharyngeal volume The superior border is the line parallel to the FHP passing through PNS, the
inferior border is the line parallel to the FHP passing through the top of the
epiglottis, and the posterior border is the pharyngeal posterior wall
Interface2 The line parallel to the FHP passing through the top of the epiglottis
Transverse diameter of interface2 The transverse line on the greatest transverse dimension at interface2
Sagittal diameter of interface2 The sagittal line on the greatest sagittal dimension at interface2
Hypopharyngeal volume The superior border is the line parallel to the FHP passing through the top of
the epiglottis, the inferior border is the line parallel to the FHP passing
through C4 (the anterior and inferior point of the fourth cervical vertebra),
and the posterior border is the pharyngeal posterior wall
Inferior boundary The line parallel to the FHP passing through C4 (the anterior and inferior
point of the fourth cervical vertebra)

RESULTS diameter and sagittal diameter of CSAmin were found.


We observed significant changes in both anatomic The 3 segments of the upper airway, volume, cross-
and aerodynamics characteristics. sectional area, and transverse diameter of nasopharynx
The changes of anatomic parameters of the upper displayed significant increases from T0 to T1
airway between T0 and T1 were shown in Table II. Sig- (P \0.01). In addition, the volume of the oropharynx
nificant increases in total volume (VTot), minimum showed a significant increase (P 5 0.043), and other pa-
cross-sectional area (CSAmin) along with the transverse rameters of the 3 segments of the upper airway did not
reveal significant changes.
The contours of pressure, minimum wall shear stress,
and the streamline of velocity during both inspiration
and expiration phase were shown in Figures 6 and 7.
The aerodynamic characteristics within the upper airway
between T0 and T1 were shown in Table III. Airway resis-
tance and maximum velocity during both inspiration
and expiration phase (Rin, Rex, Vmaxin, Vmaxex) showed
significant decreases by the comparison between T0
and T1 (Rin, P \0.001; Rex, P 5 0.001; Vmaxin,
P \0.01; Vmaxex, P \0.01; rate of changes: 26.8%,
24.7%, 15.7%, 16.5%, respectively). In terms of
minimum wall shear stress, minimum wall shear stress
decreased only in the inspiration phase (P \0.05; the
rate of changes, 26.3%).
Reduction of Rin, Rex, Vmaxin, and Vmaxex showed a
negative correlation with enlargement of VTot and CSAmin.
Decreases of Vmaxin and Vmaxex displayed a negative
Fig 4. 3D reconstructed model. correlation with increases of transverse diameter and

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Fig 5. Generated mesh of the upper airway.

Table II. Anatomic characteristics of the upper airway before (T0) and after (T1) MARME
Parameters T0 T1 P value
Total volume 25,518.43 6 6756.68 28,068.69 6 7142.77 0.007*
CSAmin 164.36 6 68.43 186.71 6 72.3 0.03*
Transverse diameter of CSAmin 21.55 6 5.22 23.69 6 5.40 0.007*
Sagittal diameter of CSAmin 8.66 6 3.04 9.86 6 2.69 0.003*
Nasopharyngeal volume 6463.86 6 1459.17 7806.69 6 1806.87 \0.001*
Cross-sectional area of interface1 434.71 6 113.83 481.95 6 132.88 0.003*
Transverse diameter of interface1 27.29 6 3.50 28.52 6 3.90 0.002*
Sagittal diameter of interface1 19.73 6 4.13 20.23 6 3.73 0.166
Oropharyngeal volume 10,886.67 6 3382.94 11,849.28 6 4306.25 0.043*
Cross-sectional area of interface2 240.53 6 104.08 256.46 6 104.94 0.364
Transverse diameter of interface2 27.09 6 5.86 28.4 6 5.03 0.213
Transverse diameter of interface2 11.72 6 3.55 12.36 6 3.34 0.276
Hypopharyngeal volume 8542.31 6 3426.18 8307.14 6 3237.12 0.387

*P \0.05.

sagittal diameter of CSAmin (P \ 0.01). In addition, the whose growth was slow, the interval assured growth,
increased volume of the nasopharynx, volume of the and the changes in body mass index were very slight,
oropharynx, and transverse diameter of the nasopharynx and there was no need to set a control group without
correlated negatively with the decreases of Rin and Rex treatment. After MARME, we observed favorable effects
(P \0.01) (Table IV). in both aerodynamic and anatomic characteristics.
In our study, the total volume of the upper airway
DISCUSSION increased significantly after MARME. In published
The retrospective study focused on the changes of studies, there were different results concerning the
anatomic and aerodynamic characteristics of the upper changes in total airway volume. Kim et al16 reported sig-
airway after MARME. In this study, 30 young adults nificant increases in total airway volume after MARME.
were involved consecutively, and the mean age was Another study indicated that although the effects of
23.82 6 3.90 years (range, 18-33 years). The interval be- bone-borne RME were more obvious than tooth-borne
tween T0 and T1 ranged from 4.3 to 5.6 months, which RME, both tooth-borne RME and bone-borne RME
assured the radiation exposure would not influence the could increase the total volume of the upper airway.26
patients. Because all of the subjects were young adults However, Yi et al27 found no significant changes in the

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Fig 6. Aerodynamic characteristics during inspiration: A, pressure drop; B, velocity; C, wall shear
stress.

Fig 7. Aerodynamic characteristics during expiration: A, pressure drop; B, velocity; C, wall shear
stress.

total upper airway after the same treatment, and the airway. That might be 1 of the factors why the effects of
study explained the negative result might be due to bone-borne RME on the upper airway were more
elongation of posterior teeth, which caused mandibular obvious than tooth-borne RME as well.
clockwise rotation. Therefore, vertical control guaran- Significant increases of CSAmin in the upper airway
teed by 4 mini-implants in the midpalatal region, which were observed after MARME. A systemic review relating
could avoid mandibular clockwise rotation, might be an to OSA have pointed out CSAmin was the most relevant
important factor to assure the enlargement of the upper factor in assessing the severity of obstruction of the

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we simulated the airflow of the upper airway of our pa-


Table III. Aerodynamic characteristics of the upper
tients on the basis of CBCT data in the supine position us-
airway before (T0) and after (T1) MARME
ing CFD analysis. What needed to be mentioned was that
P the whole respiratory cycle was a very complex physio-
Parameter T0 T1 value logical process. Although CFD was a novel method for
Airway resistance during 0.97 6 0.48 0.71 6 0.46 \0.001* the simulation of the airflow of the upper airway, it could
inspiration (Pa/L/min)
Maximum velocity during 2.16 6 0.73 1.82 6 0.76 0.003*
not simulate the airflow state of the upper airway
inspiration (ms 1) completely because of the effects of physiological regu-
Minimum wall shear stress 2.78 6 1.22 2.05 6 1.17 0.01* lation of respiration during the breathing phase.
during inspiration (Pa) Airway resistance was calculated by the formulation
Airway resistance during 0.73 6 0.37 0.55 6 0.35 0.001* based on CFD calculations, and published studies have
expiration (Pa/L/min)
Maximum velocity during 2.18 6 0.87 1.82 6 0.76 0.002*
indicated maximum velocity could reveal the most
expiration (ms 1) obstructive degree of the upper airway, which were
Minimum wall shear stress 2.28 6 0.92 1.90 6 0.85 0.053 both reliable parameters evaluating the respiratory func-
during expiration (Pa) tion of patients.32 In this study, airway resistance and
*P \0.05. maximum velocity reduced significantly in both inspira-
tion phase and expiration phase, in agreement with
some previous studies (Rin, from 0.97 to 0.71 Pa/L/
upper airway.28 Therefore, the changes of CSAmin in our min; Rex, from 0.73 to 0.55 Pa/L/min; Vin, from 2.16
study indicated MARME might be an effective method to to 1.82 m/s 1; and Vex, from 2.18 to 1.82 m/s 1). Hur
mitigate the obstruction of the upper airway. et al17 evaluated the effects of MARME on the upper
Dividing the upper airway into 3 segments, we found airway of 1 adult patient diagnosed with OSA using
the changes in the upper airway occurred in the naso- CFD analysis and reported MARME was an effective
pharynx and oropharynx. The increase in the volume of method for adult patients with moderate OSA. Zhao
the nasopharynx and oropharynx is probably due to et al22 reported a significant reduction of airway resis-
changes in craniofacial structure and the surrounding tance and velocity of 1 adult patient with transverse
soft tissues generated by MARME. Some previous studies maxillary deficiency after MARME.
have pointed out the shape and position of soft tissue, Previous studies reported the aerodynamics charac-
such as soft palate and tongue, were important factors teristics of the upper airway on the basis of CBCT in
influencing the volume of the upper airway.15,29 In addi- standing position. In our study, we observed significant
tion, we could also find that the increases in the upper changes in aerodynamics characteristics of the upper
airway occurred mostly in the nasopharynx, less in the airway based on CBCT in the supine position, which
oropharynx, and scarcely in the hypopharynx. This was another important position of taking CBCT. In addi-
finding is probably due to MARME acting directly on tion, the reliability and universality of the results were
the nasomaxillary complex, closing to the nasopharynx. better demonstrated by a group of 30 patients compared
In addition, the changes of oropharynx and hypopharynx with previous studies.
were limited by the surrounding hard and soft tissues. In addition, minimum wall shear stress decreased
Many studies stated clearly that CFD analysis was a significantly in the inspiration phase. Previous studies
convenient, effective, and reliable engineering tool for pointed out immoderate minimum wall shear stress
simulating the airflow of the upper airway, which could derived from the high speed of airflow might have a
evaluate the respiratory function of patients more pre- disadvantageous impact on the function of epithelial
cisely compared with anatomy.19-21,30,31 In our study, cells in the upper airway.33 Thus, in this study, the

Table IV. Correlation between changes of aerodynamic and anatomic characteristics


Parameter Total volume CSAmin Nasopharyngeal volume Oropharyngeal volume
Airway resistance during inspiration (Pa/L/min) 0.549* 0.583* 0.510* 0.498*
Maximum velocity during inspiration (ms 1) 0.767* 0.814* 0.309 0.499*
Minimum wall shear stress during inspiration (Pa) 0.373 0.324 0.469* 0.263
Airway resistance during expiration (Pa/L/min) 0.638* 0.662* 0.525* 0.510
Maximum velocity during expiration (ms 1) 0.751* 0.818* 0.350 0.535

*P \0.05.

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reduction of minimum wall shear stress after MARME scientific research of school of stomatology, Shandong
indicated MARME had a positive effect on the function University [2019QNJJ02].
of epithelial cells of the upper airway.
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