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\begin{document}

\title{The Role of Normal Nasal Morphological Variations from Race and Gender
Differences on Respiratory Physiology}



\author[1]{Reanna Shah}%
\author[1]{Dennis O. Frank-Ito}%
\affil[1]{Duke University School of Medicine}%


\vspace{-1em}



  
  \date{May 27, 2024}


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\selectlanguage{english}
\begin{abstract}
Objectives: To identify anatomical and airflow-induced relationships
based on nasal morphological variations due to inter- and intra-racial
differences and gender. Design: Subject-specific reconstruction of the
nasal airway anatomy was created from computed tomography images in 16
subjects: 4 subjects from each ethnic group (Black, East Asian,
Caucasian, and Latino) comprising of 2 males and 2 females. Volume,
surface area, nasal index, airflow rate, and nasal resistance were
measured to determine the role of normal nasal morphological variations
due to race and gender differences on these variables. Results:
Bilateral nasal airspace surface area (p=0.0499) and volume (p=0.0281)
were significantly greater in male subjects than in females. Median
(Interquartile Range; IQR) surface area was 218.83cm\selectlanguage{ngerman}² (IQR=29.42 cm²)
for males and 190.08cm² (IQR=19.77cm²) for females, and 20.88cm³
(IQR=3.72 cm³) versus 18.02cm³ (IQR=3.06cm³) for males and female's
nasal volumes, respectively. Nasal volume was greatest in East Asians
(Median=20.38cm3, IQR=4.58cm3), while Latinos had the greatest surface
area (Median=219.70cm2, IQR=29.56cm2). East Asian and Black females had
a larger average nasal index than their male counterparts, while Latino
and Caucasian males had a larger average nasal index than their female
counterparts. Caucasians had the highest median pressure at 12.55Pa
(IQR=6.19Pa) and highest median nasal resistance at 0.050Pa.s/ml
(IQR=0.025Pa.s/ml), while East Asians had the lowest for both variables.
Conclusions: Our findings indicate that there exist anatomical
variabilities based on race and gender. However, these variabilities may
not significantly influence nasal respiratory functions.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\emph{ABSTRACT}

\textbf{Objectives:} To identify anatomical and airflow-induced
relationships based on nasal morphological variations due to inter- and
intra-racial differences and gender.

\textbf{Design:} Subject-specific reconstruction of the nasal airway
anatomy was created from computed tomography images in 16 subjects: 4
subjects from each ethnic group (Black, East Asian, Caucasian, and
Latino) comprising of 2 males and 2 females. Volume, surface area, nasal
index, airflow rate, and nasal resistance were measured to determine the
role of normal nasal morphological variations due to race and gender
differences on these variables.

\textbf{Results:} Bilateral nasal airspace surface area (p=0.0499) and
volume (p=0.0281) were significantly greater in male subjects than in
females. Median (Interquartile Range; IQR) surface area was 218.83cm\selectlanguage{ngerman}²
(IQR=29.42 cm²) for males and 190.08cm² (IQR=19.77cm²) for females, and
20.88cm³ (IQR=3.72 cm³) versus 18.02cm³ (IQR=3.06cm³) for males and
female's nasal volumes, respectively. Nasal volume was greatest in East
Asians (Median=20.38cm\textsuperscript{\textbf{3}} ,
IQR=4.58cm\textsuperscript{\textbf{3}} ), while Latinos had the greatest
surface area (Median=219.70cm\textsuperscript{\textbf{2}} ,
IQR=29.56cm\textsuperscript{\textbf{2}} ). East Asian and Black females
had a larger average nasal index than their male counterparts, while
Latino and Caucasian males had a larger average nasal index than their
female counterparts. Caucasians had the highest median pressure at
12.55Pa (IQR=6.19Pa) and highest median nasal resistance at 0.050Pa.s/ml
(IQR=0.025Pa.s/ml), while East Asians had the lowest for both variables.

\textbf{Conclusions:} Our findings indicate that there exist anatomical
variabilities based on race and gender. However, these variabilities may
not significantly influence nasal respiratory functions.

\emph{}

\emph{Key Points}

\begin{enumerate}
\tightlist
\item
  Computational modeling was used to investigate race and gender
  differences on normal nasal physiology.
\item
  Our findings suggest that East Asians had the largest median nasal
  volume, while Caucasians had the smallest median nasal volume.
  However, Blacks demonstrated the largest variability in the
  distribution of nasal cavity volume.
\item
  As expected, males had a larger distribution of nasal cavity volume
  than females. Furthermore, Caucasian females had the smallest average
  nasal volume, whereas Black males had the largest average nasal
  volume.
\item
  Blacks had the largest median nasal index and Caucasians had the
  smallest median nasal index. In terms of gender differences, males had
  a slightly larger median nasal index than females.
\item
  Median nasal resistance was lowest for East Asians and highest among
  Caucasians; however, nasal resistance between both genders was not
  significantly different.
\end{enumerate}

\emph{Introduction}

The normal human nose is distinguished by common inter- and
intra-individual nasal morphological variations. These variations such
as nasal cycle, nasal vestibule phenotypes, and nasal index can
influence objective description of normal nasal airflow
profile.\textsuperscript{1-4} Briefly, the asymmetry of nasal airflow as
characterized by a random, reciprocal shift in nasal patency due to
temporal periods of congestion and decongestion of the mucosa in both
nasal passages is described as nasal cycle.\textsuperscript{1} Prior
studies reported between 21\% and 80\% of individuals experience some
aspect of nasal cycling.\textsuperscript{3, 5, 6}

Ramprasad and Frank-Ito\textsuperscript{7} identified another feature of
natural variation in the nasal anatomy based on nasal vestibule
morphological shapes, which were classified as Notched, Standard, and
Elongated. Reported findings suggest global airflow patterns and
resistance in the nasal cavity were unaffected by the different
morphological shapes, but local airflow resistance and air conditioning
performance were found to be greatly impacted by these morphological
variations.\textsuperscript{3, 7} Consequently, it was postulated that
the manifestation of these distinct normal nasal vestibule phenotypes
may be associated with the fact that the human nasal airway naturally
response to localized constrictions by inducing corresponding
physiological response on other regions of the airway in order to
maintain natural ventilation conditions.\textsuperscript{3, 7, 8}

Variations in nasal morphology is also thought to have been due to human
adaptation to diverse climatic environments.\textsuperscript{2,
9-11}Changes in nasal shape reflect the conditions for respiration in an
environment as adaptations were made in order to provide more efficient
conditions to maximize respiration.\textsuperscript{2, 9} These
differences in human noses due to geographic adaptations are often
characterized by nasal index.\textsuperscript{7, 12, 13} A systematic
review study performed by Leong and Eccles showed no consistent evidence
supporting the idea that differences in nasal shape and size based on
ethnic descent influence physiology.\textsuperscript{12}

Although the predicted link between race and nasal morphology is
supported by anthropological studies recording relationships between
climate and nasal function, more studies need to be done to understand
how gender differences within and between races influence nasal
physiology. Little is known on the associations of nasal anatomy and
function based on race and gender. Nonetheless, it has been established
that males exhibit larger nasal cavities volumes and longer and narrower
nasal floors than females of a similar body size.\textsuperscript{4, 14,
15}

Thus, the purpose of the present study is to use computational modeling
to investigate additional relationships between nasal morphological
variations due to inter- and intra-racial differences and gender.

\emph{Methods}

\emph{Ethical Considerations}

This retrospective study was approved by an Institutional Review Board
for Clinical Investigations under protocol Pro00102005. Consent from the
subjects were obtained on enrollment of the study in accordance with the
approval protocol.

\emph{Study Cohort}

Sixteen adult subjects with computed tomography (CT) images were
selected based on a search of university medical records. The subjects
are from four racial/ethnic groups: African Americans (Blacks); East
Asians; Caucasians; and Latin Americans. The study cohort is made up of
eight males and eight females, four subjects from each racial/ethnic
group comprising of two males and two females. Inclusion criteria were
normal nasal anatomy; high resolution spiral CT scan images; and no
clinical evidence of nasal and/or sinonasal disease. CT images were
examined by an attending radiologist and an otolaryngologist to ensure
the nasal cavities of all subjects selected for this work had
radiographic evidence of normal nasal cavity.

\emph{Nasal Reconstruction and Mesh Generation}

Computational modeling was used to generate the results. DICOM images of
each subject were de-identified and imported into the imaging analysis
and segmentation software, Avizo Lite 2019.3 (Thermo Fisher Scientific,
Waltham, Massachusetts). Three-dimensional (3D) reconstructions of each
subject's main nasal passage were digitally created, and the paranasal
sinuses excluded since this study focuses on the main nasal cavity.
Avizo Lite 2019.3 was also used to calculate the volume (V) and surface
area (SA) of each subject's nasal passage. The nasopharynx was excluded
from these calculations as it has been reported that perception of nasal
patency during respiration was more evident from nostrils to choana than
nostrils to posterior end of nasopharynx.\textsuperscript{16} The
surface area-to-volume ratio (SAV) was calculated by dividing the SA by
the V.

Reconstructed models were exported in stereolithography format from
Avizo and into the CAD and mesh generating software package, ICEM-CFD
19.0 (ANSYS, Canonsburg, PA). Planar inlet surfaces near the nostrils
and an outlet surface at the nasopharynx were created. Next, roughly 4
million unstructured tetrahedral elements and three-layer prism elements
were generated in each model's computational domain. Mesh refinement
analysis was not done based on prior work based on prior work by our
group.\textsuperscript{17} Mesh quality analysis was performed to
confirm the aspect ratio for the hybrid mesh was properly smoothed to
prevent poor elements quality from impacting the accuracy of the
numerical simulation.

\emph{Numerical Simulation}

Steady-state, laminar inspiratory air\selectlanguage{english}flow was simulated in the nasal
cavities using the CFD software package Fluent 19.0 (ANSYS, Inc.,
Canonsburg, PA) to mimic physiologic inhalation conditions at 15L/min.
The no-slip, stationary wall boundary condition was imposed on the nasal
wall. A ``pressure-inlet'' condition at the nostrils with gauge pressure
set to zero. A ``mass-flow-rate'' condition at the outlet to target
0.000301kg/s (15L/min).

\emph{Computed Quantities of Interest}

To determine the patency of each nasal cavity, nasal resistance (NR) was
calculated as \selectlanguage{english}[?]P\selectlanguage{english}/Q (Pa.s/mL) where \selectlanguage{english}[?]P is bilateral pressure drop from
nostrils to choana, and Q is bilateral volumetric flow rate. In
addition, as described in Patki and Frank-Ito\textsuperscript{2}, nasal
index was calculated as \(100\times NW\div NH,\ \) where NWis
nasal width and NH is nasal height. Lastly, statistical
comparisons were made between the genders, using the nonparametric
Wilcoxon Rank Sum test and significance (alpha=0.05), to test that the
difference in their median values was zero.

\emph{Results}

Boxplots of bilaterally computed nasal airspace surface area (SA),
volume (V), and surface area-to-volume ratio (SAV) were compared across
East Asians, Blacks, Latinos, Caucasians, and between genders. Across
the races (Figure 1A), median (IQR=interquartile range) SA was greatest
among Latinos at 266.02cm2 (IQR=25.03cm2), while East Asians had the
smallest median SA at 187.50cm2 (IQR=23.33cm2). The median SA comparison
by gender presented in Figure 1B showed that males had a significantly
greater (p= 0.0499) SA than females; 218.83cm2 (IQR=29.42cm2) versus
190.08cm2 (IQR=19.77cm2).

With regards to nasal airway volume, East Asians and Caucasians had the
largest and smallest median volume, respectively; 20.38cm3 (IQR=4.58cm3)
for East Asians and 18.63cm3 (IQR=5.19cm3) for Caucasians (Figure 1C).
Interestingly, as evidenced by IQR values and whisker lengths in Figure
1C, Blacks demonstrated the largest variability (IQR=8.38cm3) in the
distribution of nasal cavity volume. Similar to Figure 1B, box plots in
Figure 1D showed that males had a significantly larger (p=0.0281)
distribution of nasal cavity volume than females; 20.88cm3 (IQR=3.72cm3)
versus 18.02cm3 (IQR=3.06cm3).

The median SAV for all four racial groups indicated (Figure 1E) that
Caucasians and Latinos had relatively larger SAV at
10.97cm\textsuperscript{-\textbf{1}}
(IQR=1.50cm\textsuperscript{\textbf{-1}} ) and
10.72cm\textsuperscript{-\textbf{1}}
(IQR=2.77cm\textsuperscript{\textbf{-1}} ), respectively, compared to
the respective median SAV for East Asians and Blacks;
9.12cm\textsuperscript{-\textbf{1}}
(IQR=3.01cm\textsuperscript{\textbf{-1}} ) and
9.40cm\textsuperscript{-\textbf{1}}
(IQR=3.26cm\textsuperscript{\textbf{-1}} ). Figure 1F showed females
with slightly larger median SAV than males at
10.85cm\textsuperscript{-\textbf{1}}
(IQR=2.44cm\textsuperscript{\textbf{-1}} ) and
9.74cm\textsuperscript{-\textbf{1}}
(IQR=2.82cm\textsuperscript{\textbf{-1}} ), respectively, albeit not
significantly larger than males (p=0.44).

On average, nasal cavity SA for females in each race/ethnicity was
smaller than their respective male counterparts (Figure 2A); however,
average SA for Black females (195.67cm2) was marginally smaller than
Black males (197.60cm2). With a difference of 29.56cm2, the Caucasian
race had the largest difference between average SA for females and
males. The group with the smallest average SA, across all races and
genders, was East Asian females (172.74cm2), while the largest average
SA was Caucasian males (227.36cm2).

Average nasal cavity volume (Figure 2B) largely followed a similar
pattern as SA (Figure 2A), with the exception of Latinos where females
had a larger average nasal volume than their male counterpart. Overall,
Caucasian females had the smallest average nasal volume at 16.58cm3,
while Black males had the largest (26.40cm3; Figure 2B). Results for SAV
were completely reversed from those of nasal volume -- except for
Latinos, average SAV values among females of the other races/ethnicities
were respectively larger than their male counterparts (Figure 2C).
Caucasian females and Latino males overall had the largest SAV at
11.93cm\textsuperscript{\textbf{-1}} and
12.28cm\textsuperscript{\textbf{-1}} , while Black males had the
smallest (7.48 cm\textsuperscript{\textbf{-1}} ).

Blacks had the largest median nasal index of 95.82 (IQR=3.08), whereas
Caucasians had the smallest median nasal index of 72.46 (IQR=0.89;
Figure 3A). Latinos and East Asians followed with a median of 82.59
(IQR=8.84) and 78.33 (IQR=6.62), respectively. In Figure 3B, males had a
slightly larger nasal index than females with respective median values
of 80.98 (IQR=13.86) and 79.25 (IQR=20.12).

Figure 3C described comparisons between race and gender for nasal index.
East Asian and Black females had a larger average nasal index than their
male counterparts, while Latino and Caucasian males observed the
opposite trend. It should be noted that the difference in average nasal
index between Caucasian males and females may be considered negligible.
Overall, Black females had the largest average nasal index (97.05) and
Caucasian females had the smallest average nasal index (72.24).

Among the races, Caucasians had the greatest median nasal airflow
pressure of 12.55Pa (IQR=6.19Pa), followed by Blacks at 11.47Pa
(IQR=7.79Pa); while East Asians had the smallest median nasal airflow
pressure of 5.65Pa (IQR=7.45Pa; Figure 4A). For nasal airflow pressure
comparison by gender, males and females had approximately the same
median nasal airflow pressure values (males=10.88Pa, females=10.11Pa, p=
0.7984); nonetheless, males had larger variability with an IQR of
9.21Pa, compared to females (IQR = 5.14Pa; Figure 4B).

Median nasal resistance was highest among Caucasians at 0.050Pa.s/ml
(IQR=0.025Pa.s/ml; Figure 4C). Blacks and Latinos followed with nearly
identical median nasal resistance of 0.046Pa.s/ml (IQR=0.032Pa.s/ml) and
0.043Pa.s/ml (IQR=0.016Pa.s/ml), respectively. East Asians had the
lowest nasal resistance (median=0.023Pa.s/ml, IQR=0.030Pa.s/ml). Next,
nasal resistance between males and females were not significant
difference (p=0.7984). Both genders had nearly identical median nasal
resistance values of 0.044Pa.s/ml (IQR=0.04Pa.s/ml) for males and
0.041Pa.s/ml (IQR=0.02Pa.s/ml) for females (Figure 4D).

Additionally, average pressure for males was larger than females of
their respective race in all races except for East Asians (Figure 5A).
Caucasian and East Asian females had very similar pressure values around
12.50Pa. East Asian females had a much greater pressure than East Asian
males with a difference of 6.95Pa. Across all races and genders, Black
males had the largest pressure at 14.65Pa, while East Asian males had
the smallest pressure at 5.64Pa.

Similar to Figure 4, Figure 5 revealed that nasal airflow pressure and
nasal resistance generally followed identical patterns, except among
Blacks where females on average had lower nasal airflow pressure (Figure
5A) but higher nasal resistance (Figure 5B) than their male
counterparts. Latino males, East Asian females, and both Caucasian
genders had nearly similar nasal airflow pressure of about 13Pa (Figure
5A), and nasal resistance value around 0.05Pa.s/ml (Figure 5B). Across
all races and genders, Caucasian males had the largest nasal resistance
at 0.052Pa.s/ml and East Asian males had the smallest nasal resistance
at 0.023Pa.s/ml (Figure 5B).

\emph{Discussion}

The present study focused on relationships between nasal morphological
variations due to inter- and intra-racial differences and gender, which
differs from previously published studies by our group investigating
nasal morphological variations.\textsuperscript{2, 18} Unlike this study
that categorizes nasal index by subjects' race/ethnicity with gender,
and gender separately; Patki and Frank-Ito\textsuperscript{2} explored
the relationship between nasal index and CFD simulated airflow-related
variables, such as nasal resistance, wall shear stress, and heat flux.

Although Keeler et al.\textsuperscript{18} modeled deposition patterns
of individuals across the same four race/ethnic groups as the present
study, as well as briefly reported results of SAV ratio, nasal
resistance and nasal index across races/ethnicities; the present student
conducted an in-depth analysis of both anatomical and airflow-related
variables in the same race/ethnic groups with gender as a factor.
Additionally, Keeler et al.\textsuperscript{18} included the paranasal
sinuses in their CFD models while the present study excluded the
paranasal sinuses are they have negligible effects on physiological
functions pertaining to the main nasal cavities.

Nasal index results are in agreement with reports on climate-related
variation in human nose, suggesting that individuals that evolved from
colder and drier climates tended to have smaller nasal index than
individuals from warmer and more humid climates.\textsuperscript{2, 12,
18, 19} Results in this study pertaining to nasal index and gender are
consistent with those previously reported by Ravichandran et
al.\textsuperscript{20} In their paper, Ravichandran and colleagues
found that nasal index is a reliable parameter for the estimation of
gender difference, noting that the average value of nasal indices of
South Indian males was greater than South Indian
females.\textsuperscript{20} Additionally, in a study examining the
nasal index of the Kosovo Albanian population, males had a significantly
higher nasal index than females (p \textless{}
0.001).\textsuperscript{21} While similar conclusions can be made with
the Caucasian population from the present study, it should be noted that
the difference in median nasal index between Caucasian males and females
was 0.66. Additionally, when comparing nasal index and gender by race,
East Asian and Black females had larger average nasal index than their
male counterparts.

The current literature is sparse regarding the relationship between
nasal resistance and race/ethnicity. Keeler et
al.\textsuperscript{18}reported that average nasal resistance for
African Americans and Caucasians were lowest and highest, respectively.
Other studies have reported no significant differences in nasal
resistance between African descents and Caucasians.\textsuperscript{19,
22, 23} Babatola measured nasal resistance of African descents from
Nigeria and concluded that nasal resistance in this population was
similar to those of Caucasians and Asians.\textsuperscript{22} Calhoun
et al. and Ohki et al.\textsuperscript{19, 23} also arrived at similar
conclusions in their studies. Our results suggest that median nasal
resistance was highest among Caucasians, followed by Blacks before
Latinos, and East Asians had the lowest median nasal resistance values.
Nonetheless, it should be noted that the IQR values for Blacks and East
Asians were particularly larger than those of Caucasians and Latinos,
implying there could be possible overlap among the groups, which may
indicate non-significant differences among groups.

Our findings indicate females have a larger nasal resistance than males.
This trend was seen within every race except for Caucasians when
comparing between nasal resistance and race and gender. A study
conducted by Warren et al.\textsuperscript{24} revealed no significant
difference in resistances for males and females with normal nasal
anatomy. However, Ren et al.\textsuperscript{25} reported that mean
nasal resistance in males were significantly lower than females among a
cohort of healthy subjects in China.

The main limitation from the present study pertains to our relatively
small sample size. Although there were 16 subjects, each race had 4
subjects, and after further stratification by race and gender, there
were 2 subjects per group. In conclusion, this study investigated the
relationships between normal nasal morphological variations due to
inter- and intra-racial and gender differences in subject-specific nasal
airway models from 16 subjects across 4 racial groups. Findings from the
present work indicate that there is an association between normal nasal
anatomical variabilities across race and gender. However, these
variabilities may not discriminate proper functioning of the nasal
cavity across race and gender.

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\textbf{Figure Legend}

\textbf{Figure 1:} Nasal cavity surface area by (A) Race and (B) Gender.
Nasal cavity volume by (C) Race and (D) Gender. Nasal cavity surface
area-to-volume ratio by (E) Race and (F) Gender.

\textbf{Figure 2:} Nasal cavity quantification by race and gender for
(A) Surface area, (B) Volume, and (C) Surface Area-to-Volume Ratio.

\textbf{Figure 3:} Nasal index quantification by (A) Race, (B) Gender,
and (C) Race and gender.

\textbf{Figure 4:} Nasal pressure by (A) Race and (B) Gender. Nasal
resistance by (C) Race and (D) Gender.

\textbf{Figure 5:} Nasal cavity results by race and gender for (A)
Pressure, and (B) Resistance.\selectlanguage{english}
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\includegraphics[width=0.70\columnwidth]{figures/PR-R-Bar-Figure5/PR-R-Bar-Figure5}

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