Keywords mouth breathing - nasopharynx - diagnosis - comparative study
Palavras-chave respiração bucal - nasofaringe - diagnóstico - estudo comparativo
Introduction
The breathing process, which begins at the upper airway and culminates in gas exchange
inside the alveoli, is essential for the human organism to survive. When breathing
begins through the nose, the air is prepared in order to reach the lungs with the
ideal conditions, that is, warmed, moistened, and filtered, thus activating immunological
processes such as mucociliary transport and microbicidal activity that protect the
lower airway. When breathing begins through the mouth, despite air warming and moistening,
no filtering or immunological activity occurs[1 ].
When mouth breathing occurs in childhood, a period during which intense facial muscular
and skeletal growth occurs, it promotes a pathological adaptation of the structures
of the stomatognathic system, to the detriment of the usually harmonious morphological
and functional growth of these structures[2 ].
The main causes of mouth breathing in childhood are the hypertrophy of the pharyngeal
and/or palatine tonsil, nasal mucosa and turbinate edema, nasal septal deviation,
extended suction habits, and others[3 ].
Morphological adaptations in mouth-breathing children occur with the aim of facilitating
the necessary arrival of the air to the alveoli. Thus, it is possible to observe maxillary
hypoplasia and posterior mandibular demotion/rotation, which lead to dental occlusion
alterations, higher mandibular inclination, and a vertical facial growth pattern,
with alterations in normal facial proportions and hard palate elevation, head anteriorization,
and muscular deharmonization, occurring mainly in the nasofacial region. These adaptations
generate functional changes in the stomatognathic system, which are observed through
alterations in speech, chewing, and deglutition[4 ]
[6 ].
The complexity of the consequences of mouth breathing that are associated with various
etiologies justifies the participation of several professionals, including otorhinolaryngologists,
odontologists, phonoaudiologists, physiotherapists, pediatricians, among others, along
the different phases of the care of mouth-breathers, including the diagnosis, treatment,
rehabilitation, and the prevention of mouth breathing in childhood. Multidisciplinary
staff integration is essential, as it is desirable to use a uniform categorization
of mouth breathers, consisting of the same terminology and the same complementary
exams.
Accurate diagnosis of the cause of mouth breathing is essential to the effectiveness
of treatment. In phonoaudiology, the type of care that is used for mouth-breathing
patients is typically determined by the etiology of the altered respiratory mode.
Therefore, the accurate use of the available diagnostic options contributes to early
diagnosis, and will aid in the establishment of a multidisciplinary therapeutics that
are more appropriate to each case and minimize relapse during mouth breathing rehabilitation[7 ]
[8 ].
Most causes of mouth breathing are diagnosed through a disarmed otorhinolaryngologic
exam, except for the diagnosis of hyperplasia of the pharyngeal tonsils, which demands
that complementary exams be used[3 ].
In the diagnosis of pharyngeal hyperplasia, the exams that are typically requested
include cavum radiography and nasopharyngoscopy. Nasopharyngoscopy is a procedure
that is used to visualize the pharyngeal tonsil and its relation to other nasopharyngeal
structures, and is considered by many authors as the most reliable exam in the diagnosis
of nasopharyngeal obstruction[9 ]
[10 ]
[11 ]
[12 ]
[13 ]. Cephalometry is an exam that is similar to cavum radiography; however, it is carried
out through the use of a cephalostat, which enables the most appropriate patient positioning,
and provides data related to craniofacial growth and the myofunctional status of these
structures[14 ]. Since it is a noninvasive exam, it is more comfortable for the patient, and is
often more accepted by children. Moreover, is associated with a lower cost and greater
availability relative to nasopharyngoscopy.
With the aim of contributing to the accurate diagnosis of mouth breathing, this study
was carried out with the purpose of verifying the correlation between nasopharyngoscopy
and cephalometry in the diagnosis of hyperplasia of the pharyngeal tonsils.
Method
The preset study was approved by the Research Ethics Committee of the institution
of origin under the protocol number 220.0.243.000-8. The children agreed to take part
in the study and the Informed Consent forms were signed by their representatives.
The study sample consisted of children from 3 public schools who were evaluated from
September 2008 through December 2009. The inclusion criteria were included complaints
related to mouth breathing, such as night drooling, snoring, and restless sleep; the
group age ranged from 7.0 to 11.11 years. Children that presented evident neurological
disorders, craniofacial malformation, syndromes, or history of pharyngeal surgery
were excluded from the study. Sex differences were not taken into account.
After employing the inclusion and exclusion criteria, 55 children, including 25 males
and 30 females, with an average age 9.8 years were selected. These children underwent
otorhinolaryngologic assessment, as well as nasopharyngoscopy and cephalometry to
check for the presence or absence of nasopharyngeal obstruction. Any other causes
of obstruction of the upper airway, such as nasal septal deviation, primary hypertrophy
of the nasal turbinates, polyps, and malformations were not diagnosed in the study
sample. For the patients with bacterial rhinosinusitis and/or symptomatic allergic
rhinitis, appropriate treatments were prescribed and subsequent revaluation was carried
out during a period ranging from 30 to 60 days. After this period was completed, the
nasopharyn-goscopy and cephalometry exams were performed.
Otorhinolaryngologic evaluation was carried out in the presence of and with the help
of the parents or sponsors. After a general and specific otorhinolaryngologic anamnesis
was conducted, giving emphasis to the aspects related to mouth/nasal breathing, a
physical exam consisting of otoscopy, anterior rhinoscopy, cervical palpation, and
nasoscopy was carried out. This evaluation allowed for the determination of whether
the patient had either an oral or mouth-breathing mode.
Immediately after the completion of the anamnesis and the otorhinolaryngologic clinical
exam, nasopharyngoscopy was carried out, always by the same assessor and in the same
environment, employing topical anesthesia (lidocaine 5%) and a nasal vasoconstrictor
(oxymetazoline 0.05%), with a flexible nasofibroscope (3.2mm Mashida® brand, microcamera Asap® ), and recorded on DVD. Through this exam, apart from studying the size and the relation
of the pharyngeal tonsil to the nasopharynx, the nasal septum positioning, turbinate
size, upper pole of the palatine tonsils, presence of secretions, and other kinds
of lesions in the nasal cavity and hypopharynx were assessed.
When using nasopharyngoscopy to determine the level of hyperplasia of the pharyngeal
tonsils, we used a graded scale in which the relation of the pharyngeal tonsils to
the other structures that are present in the nasopharynx was assessed[15 ], as follows:
Grade 1–tonsil without contact with the nasopharyngeal structures ([Figure 1 ]);
Grade 2–tonsil in contact with the torus tubarius ([Figure 2 ]);
Grade 3–tonsil in contact with the torus tubarius and vomer ([Figure 3 ]);
Grade 4–tonsil in contact with the torus tubarius, vomer, and the soft palate at rest
([Figure 4 ]).
Figure 1. Grade 1 hyperplasia of the pharyngeal tonsils by nasofibropharyngoscopy and cephalometry
(cephalometric analysis).
Figure 2. Grade 2 hyperplasia of the pharyngeal tonsils by nasofibropharyngoscopy and cephalometry
(cephalometric analysis).
Figure 3. Grade 3 hyperplasia of the pharyngeal tonsils by nasofibropharyngoscopy and cephalometry
(cephalometric analysis).
Figure 4. Grade 4 hyperplasia of the pharyngeal tonsils by nasofibropharyngoscopy and cephalometry
(cephalometric analysis)
Subsequently, children were referred to the odontological radiology service center
to undergo a cephalometric assessment, through which it was possible to obtain a left
profile cranium teleradiograph by using the cephalostat for positioning the patient
at a distance of 1.5 meters. For the standard lateral radiography assessment, computerized
cephalometric tracing was performed with Cef X software (a computerized cephalometry
system version 2.4.0.0 from CDT software for informatics consulting, development,
and training). The exam was carried out with the same equipment in each patient, and
was analyzed by the same professional expert in odontological radiology.
When using cephalometric analysis, in order to determine the level of hyperplasia
of the pharyngeal tonsils, we used a graded scale in which the airway between the
palate pharynx border and the point that was most proximal to the pharynx was measured
in millimeters[16 ], as follows:
Grade 1–nasopharyngeal space larger than 6 mm ([Figure 1 ]);
Grade 2–nasopharyngeal space between 4.1 and 6 mm ([Figure 2 ]);
Grade 3–nasopharyngeal space between 2.1 and 4 mm ([Figure 3 ]);
Grade 4–nasopharyngeal space between 0 and 2 mm ([Figure 4 ]).
In order to verify the correlation between the nasopharyngoscopy and cephalometry
examinations, the Spearman's rank correlation test was performed at a significance
level of 5%. The test results in a correlation coefficient ranging from -1 to +1,
with zero indicating that there is no correlation, -1 indicating a perfect negative
correlation, and +1 denoting a perfect positive correlation; the closer to 1 or +1,
the greater the correlation between the variables that are being tested. The possible
results for a positive correlation are[17 ]:
0 when there is no correlation;
Between 0 and 0.3 - poor correlation;
Between 0.3 and 0.6 - regular correlation;
Between 0.6 and 0.9 - a very strong correlation;
Equal to 1–a perfect correlation between the data.
For calculating the sensitivity, specificity, the positive predictive value, and the
negative predictive value of radiologic exams, nasopharyngoscopy was considered to
be the reference exam (the gold standard). It was also necessary to establish limit
values in order to determine whether the exams that were studied were either positive
or negative. Therefore, the grade 1 and 2 nasopharyngoscopic and cephalometric exams
were considered to be negative, and the grade 3 and 4 exams were considered to be
positive.
Results
[Table 1 ] shows the results of the correlation analysis between the nasopharyngoscopy and
cephalometry examinations in diagnosing the grade of hyperplasia in the pharyngeal
tonsils.
Table 1.
Correlation between the nasopharyngoscopy and cephalometry examinations for the diagnosis
of the grade of hypertrophy of the pharyngeal tonsils.
Exam Obstruction
Nasopharyngoscopy
Cephalometry
Grade 1
n = 15
n = 32
27.27%
58.18%
Grade 2
n = 20
n = 15
R = 0.52
36.36%
27.27%
p = 0.000
Grade 3
n = 19
n = 5
34.54%
9.09%
Grade 4
n = 1
n = 3
1.83%
5.46%
N = number of children; p = significance level at 5%; R = Spearman's rank correlation
coefficient.
From the analysis of the results presented in [Table 1 ], it was possible to verify that the Spearman's rank correlation coefficient, Rho
(R), was equal to 0.52. This result indicates a significant regular and positive association
between the nasopharyngoscopy and cephalometry assessments (p = 0.000) at a significance
level of 5%.
[Table 2 ] describes the nasopharyngoscopy and cephalometry distribution results that were
used for assessing the diagnostic tests.
Table 2.
Distribution of children according to the results in nasopharyngeal and cephalometric
exams.
Cephalometry
Nasopharyngoscopy
Total
Positive
Negative
Positive
7
1
8
Negative
13
34
47
Total
20
35
55
In [Table 2 ], using nasopharyngoscopy as the gold standard for the diagnosis of hyperplasia of
the pharyngeal tonsils, it was possible to verify that the sensitivity of cephalometry
(determined by the proportion between the number of correct positive radiographic
cephalometry diagnoses and the total number of positive cases) was 35%. The negative
predictive value of cephalometry (determined by the proportion between the number
of correct negative diagnoses and the total number of negative cases) was 97%. The
positive predictive value of the cephalometric exam (determined by the ratio of the
number of correct positive cephalometric diagnoses and the total number of positive
cephalometric diagnoses) was found to be 87%. The negative predictive value (determined
by the ratio of the number of correct negative cephalometric diagnoses and the total
number of negative cephalometric diagnoses) was 72%.
Discussion
Hyperplasia of the pharyngeal tonsils is one of the main causes of upper airway obstruction.
For this reason, studies have been carried out with the objective of assessing the
reliability of the available diagnostic procedures that are used for the detection
of nasopharyngeal obstruction resulting from the increased size of the pharyngeal
tonsils. The most commonly used exams are cavum radiographs, flexible and rigid nasopharyngoscopy,
and cephalometry[11 ]
[13 ]
[18 ].
Reports in the literature indicate that there is concern regarding the best method
for diagnosing and treating children in which hyperplasia of pharyngeal tonsils is
suspected, which a frequently occurring situation in the otorhinolaryngological practice[13 ]
[19 ]. Therefore, this study aimed to establish a correlation between the nasopharyngoscopy
and cephalometry examinations in the diagnosis of hyperplasia of the pharyngeal tonsils,
while highlighting their main contributions.
The findings of this study demonstrated that it was possible to verify a regular and
positive correlation, R = 0.52; however, a perfect correlation between the exams was
not found. The results revealed that most of the children showed grade 2 and 3 hyperplasia
of the pharyngeal tonsils, followed by grade 1 in the nasopharyngoscopic exam, and
most of the children showed grade 1 hyperplasia of the pharyngeal tonsils, followed
by grade 2 in the cephalometric assessment ([Table 1 ]). After analyzing these results, it was possible to infer that cephalometry, as
compared to nasopharyngoscopy, presented a tendency to underestimate the pharyngeal
tonsil size in the nasopharynx.
The sensitivity of cephalometric exam, which indicates the probability of a positive
result when the patient presents with the condition in question, was 35%. The negative
predictive value, which expresses the probability that the individual does not present
with the condition in question when the exam result is negative, was 72%. These results
suggested that a negative cephalometric exam might not provide a proper assessment
of the nasopharynx when compared to the nasopharyngoscopic exam.
Similar results were obtained when cavum radiography and flexible nasopharyngoscopy
for the assessment of the grade of nasopharyngeal obstruction were compared in other
similar study[13 ]. The authors concluded that children with classical symptoms of respiratory obstruction,
in the absence of hypertrophy of the pharyngeal tonsils by a radiological exam, should
undergo flexible nasopharyngoscopy in order to achieve a more accurate diagnosis.
Several published studies consider nasopharyngoscopy to be the gold standard exam
for assessing the nasopharynx[12 ]
[13 ]
[20 ]
[21 ]
[22 ]. This is justified, among other reasons, by the dynamic and tridimensional nasopharyngeal
view provided by this assessment, which makes it possible to analyze not only the
pharyngeal tonsil size, but also its relation with other structures in the region.
This may explain the reason why, in the comparison between nasopharyngoscopy and cephalometry,
the latter tended to underestimate the size and position of the pharyngeal tonsils
in relation to the nasopharynx.
Frequently in clinical practice, it is possible to verify that patients with mouth
breathing symptoms who show normal or next to normal pharyngeal tonsil size with radiological
exams, may present hyperplasia of the pharyngeal tonsils and other alterations, such
as hypertrophy of the lower turbinate and posterior nasal septal deviation, when assessed
by nasopharyngoscopy.
This statement is reinforced by another study[11 ] in which 45 children between 4 and 12 years of age were assessed with nasopharyngoscopy;
all of them presented chronic nasal obstruction due to hyperplasia of the pharyngeal
tonsils, and cavum radiography revealed no alterations. The results demonstrated that
27% (17 cases) of the pharyngeal tonsils were estimated to be large, 42% (24 cases)
of the pharyngeal tonsils were of moderate size, and 31% (19 cases) of the pharyngeal
tonsils were small. Furthermore, the exams detected 8 cases of hypertrophy of the
lower turbinate (13.3%) and 4 cases of posterior nasal septal deviation (6.6%). These
findings reinforced the importance of the indication of nasopharyngoscopy for children
with nasal obstruction and normal radiological exams, as this exam allows direct,
tridimensional, and dynamic assessment of the cavum area.
On the other hand, another study[23 ] that verified the efficacy of lateral cephalometric radiography in the diagnosis
of hyperplasia of the pharyngeal tonsils compared with nasal endoscopy, differs from
the results of the present study, as the authors substantiated that lateral cephalometric
radiography proved to be an effective exam because of its sensitivity, specificity,
and high positive and negative predictive values for diagnosis. They concluded that
in spite of the superiority of nasopharyngoscopy in assessing the nasopharynx, a cephalometric
exam that was negative for hypertrophy of the pharyngeal tonsils would be sufficient
to exclude this pathology.
Based on information that was derived from 3 units that comprise the SUS (Sistema
Único de Saúde), another study reported that mouth breathing is the most frequently
cited complaint and that cavum radiography was the most commonly requested exam by
otorhinolaryngologists[19 ]. From the results of the present study, it can be inferred that if only the radiographic
exam is used for the detection of hyperplasia of the pharyngeal tonsils, a proper
mouth-breather diagnosis and treatment might be compromised, as in some cases the
grade of pharyngeal tonsil obstruction was underestimated relative to the nasopharyngoscopic
exam.
When not treated in childhood, mouth breathing causes many alterations, including
craniofacial, dental, and phonoarticulatory changes, as well as alterations in body
posture, oral functions, sleep, nutrition, behavior, and others[24 ]. All of these alterations that are presented by mouth breathers require multidisciplinary
intervention, including physicians, phonoaudiologists, odontologists, physiotherapists,
among others[1 ].
Although cephalometry was only regularly correlated with nasopharyngoscopy in diagnosing
mouth breathing, that exam was able to complement the endoscopic exam, thus providing
information regarding facial growth that could be documented and monitored. This information
will be useful for other professionals involved in the care of mouth-breathing patients.
Cephalometry provides early identification of many alterations that are present in
mouth-breathing patients and provides the otorhinolaryngologist with information about
the nasopharynx, informs the phonoaudiologist about morphological alterations of the
stomatognathic system, and informs the odontologists about facial growth and dental
occlusion[3 ]
[14 ]
[23 ]. Therefore, cephalometry is useful not only for the initial diagnosis, but also
in cost reduction and promoting collaboration between the multidisciplinary staff
members that are involved in the care of mouth-breathing patients.
A research study comparing cavum radiography with cephalometry found that in the first
exam 61% of the patients were incorrectly positioned[25 ]. Importantly, the cephalostat is used in cephalometry to control the positioning
of the patient, which explains the superiority of this exam compared to cavum radiography.
Although nasopharyngoscopy is the gold standard exam for nasopharyngeal assessments,
cephalometry is a complementary exam that provides information about craniofacial
growth, thus making it possible to document and monitor the complex morphofunctional
modifications related to mouth breathing.
In this study, cephalometry showed a tendency to underestimate the size of pharyngeal
tonsil compared with nasopharyngoscopy; therefore, we suggest that patients presenting
with mouth-breathing symptoms and normal radiography be referred for a complementary
assessment with nasopharyngoscopy, which is associated with greater diagnostic accuracy
due to its tridimensional and dynamic nature.
Conclusions
Nasopharyngeal assessment of children can be performed with nasopharyngoscopy and
cephalometry, as these exams are associated with a regular and positive correlation.
However, we found that cephalometry tends to underestimate the size of the pharyngeal
tonsil compared with nasopharyngoscopy. Therefore, nasopharyngoscopy is suggested
when the cephalometry results for nasopharyngeal obstruction are negative in patients
with mouth-breathing symptoms.
