Accepted Manuscript Nasal function before and after rapid maxillary expansion in children: A randomized, prospective, controlled study G. Ottaviano, P. Maculan, G. Borghetto, V. Favero, B. Galletti, E. Savietto, B. Scarpa, A. Martini, E. Stellini, C. De Filippis, L. Favero PII:
S0165-5876(18)30495-6
DOI:
10.1016/j.ijporl.2018.09.029
Reference:
PEDOT 9196
To appear in:
International Journal of Pediatric Otorhinolaryngology
Received Date: 22 May 2018 Revised Date:
26 September 2018
Accepted Date: 26 September 2018
Please cite this article as: G Ottaviano, P Maculan, G Borghetto, V Favero, B Galletti, E Savietto, B Scarpa, A Martini, E Stellini, C De Filippis L Favero, Nasal function before and after rapid maxillary expansion in children: A randomized, prospective, controlled study, International Journal of Pediatric Otorhinolaryngology (2018), doi: https://doi.org/10.1016/j.ijporl.2018.09.029. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT NASAL FUNCTION BEFORE AND AFTER RAPID MAXILLARY EXPANSION IN CHILDREN: A RANDOMIZED, PROSPECTIVE, CONTROLLED STUDY.
Ottaviano G1, Maculan P1, Borghetto G2, Favero V3,
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Galletti B4, Savietto E1, Scarpa B5, Martini A1, Stellini E2, De Filippis C6, Favero L2
1Department
of Neurosciences DNS, Otolaryngology Section, University of Padova, Padova,
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Italy
Department of Neurosciences DNS, Odontostomatology Institute, University of Padova,
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Padova, Italy 3Department
of Surgery, Dentistry and Maxillofacial Unit, University of Verona, Verona, Italy
4Department
of Otorhinolaryngology, University of Messina, Messina, Italy.
5Department
of Statistical Sciences, University of Padova, Padova, Italy of Neuroscience, University of Padova, Audiology Unit at Treviso Hospital,
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6Department
Treviso, Italy. Correspondence to:
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Giancarlo Ottaviano, MD, PhD
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Department of Neurosciences DNS, Otolaryngology Section, University of Padova,
Via Giustiniani 2, 35128 Padova, Italy Tel. +39 (0)49 8212029; Fax: +39 (0)49 8213113 e-mail:
[email protected]
The authors declare no conflicts of interest
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NASAL FUNCTION BEFORE AND AFTER RAPID MAXILLARY EXPANSION IN
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CHILDREN: A RANDOMIZED, PROSPECTIVE, CONTROLLED STUDY.
4 Ottaviano G1, Maculan P1, Borghetto G2, Favero V3,
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Galletti B4, Savietto E1, Scarpa B5, Martini A1, Stellini E2, De Filippis C6, Favero L2
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Department of Neurosciences DNS, Otolaryngology Section, University of Padova, Padova, Italy
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Department of Neurosciences DNS, Odontostomatology Institute, University of Padova, Padova,
Italy
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Department of Surgery, Dentistry and Maxillofacial Unit, University of Verona, Verona, Italy
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Department of Otorhinolaryngology, University of Messina, Messina, Italy.
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Department of Statistical Sciences, University of Padova, Padova, Italy
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Department of Neuroscience, University of Padova, Audiology Unit at Treviso Hospital, Treviso,
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Italy.
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Correspondence to:
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Giancarlo Ottaviano, MD, PhD
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Department of Neurosciences DNS,
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Otolaryngology Section,
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University of Padova,
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Via Giustiniani 2, 35128 Padova, Italy
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Tel. +39 (0)49 8212029; Fax: +39 (0)49 8213113
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e-mail:
[email protected]
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The authors declare no conflicts of interest
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Abstract.
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Objectives: Children can well detect and respond to odours in order to have information about food
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and environment. Rapid Maxillary Expansion seems to improve dental and skeletal crossbite and increase
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nasal patency correcting oral respiration in children. A previous pilot study suggested that Rapid
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Maxillary Expansion may lead to improved N-Butanol olfactory thresholds, and peak nasal
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inspiratory flow values (PNIF). The aim of the present study was to prospectively evaluate olfactory
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threshold, nasal flows and nasal resistances in children aged from 6 to 11 years before and after
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Rapid Maxillary Expansion, comparing treated children with a control group of similar age, growth
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stage (prepubertal) and transversal skeletal deficiency.
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Methods: N-butanol olfactory thresholds, anterior active rhinomanometry (AAR) and PNIF were
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measured in 11 children (6-11 years) before (T0), immediately and 6 months after Rapid Maxillary
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Expansion application (T1 and T2 respectively), and in a control group of 11 children (6-11 years)
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whose members remained under observation for the period of the study.
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Results: Considering the study group, PNIF values improved at T1 respect to the T0 values
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(p=0.003), while T2 values were significantly higher than T0 ones (p=0.0002). N-Butanol Olfactory
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Threshold significantly improved at each control (p=0.01, p=0,01 and p=0.0003, for T1 vs T0, T2
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vs T1, T2 vs T0 respectively). No differences on AAR values were found during the six months
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follow-up in this group.
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Considering the control group, no significant differences were found for any of the considered variables during the time of the study.
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Comparing the two groups, there was a significant increase of PNIF values in the study
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group compared to the control group (p=0.003) at T1, which was even more evident six months
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after Rapid Maxillary Expansion (p=0.0005). This improvement was not shown by AAR values. N-
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Butanol Olfactory Threshold showed a significant improvement at T2 respect to T1 (p=0.002) and
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T0 (p=0.0005). 2
ACCEPTED MANUSCRIPT Conclusion: Rapid Maxillary Expansion seems to significantly improve the respiratory capacity of
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treated patients, at least in terms of PNIF, and their olfactory function, measured by N-Butanol
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Olfactory Threshold Test. Further studies should be performed to evaluate if also changes in nasal
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resistances, measured by AAR, could occur, maybe considering a larger group of subjects and
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possibly using 4-phase rhinomanometry in order to evaluate the effective resistances during the
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entire breath.
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Keywords: olfaction, Peak nasal inspiratory flow, Anterior active rhinomanometry, rapid maxillary
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expansion, crossbite, children
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1. Introduction
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Human infants react to odours from birth. [1] Olfactory discrimination is already present in the
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neonatal period and improves from years 3 to 12. [2] Children can detect, discriminate, and respond
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to odours in order to have information about food and the environment at large. [3] Peak nasal inspiratory flow (PNIF) has been shown to be reproducible in the evaluation of
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nasal airway obstruction and as good an indication of objective nasal patency as formal
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rhinomanometry. [4,5] Furthermore, PNIF is a cheap, simple and easily performed method to assess
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nasal flows also in children. [6] A recent pilot study of our group demonstrated that rapid Maxillary
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Expansion (RME) improves dentoskeletal malocclusion, increases nasal flows, reduces nasal
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resistances and also improves olfactory threshold. [7] Anyway, no case-control studies have been
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performed on both olfactory function and RME in this kind of population.
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The aim of the present study was to evaluate N-Butanol olfactory thresholds together with
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nasal flows and resistances, measured by means of PNIF and anterior active rhinomanometry
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(AAR), in a new group of children aged from 6 to 11 years before and after RME and in a control
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group.
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ACCEPTED MANUSCRIPT 2.Material and methods
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For the present study twenty-two consecutive patients (11 males and 11 females) aged 6 to 11 years
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(mean age 8,27 ± 1,41) with unilateral or bilateral posterior crossbite, transversal discrepancy of 4
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mm between upper jaw and mandible (grade 3c or 4c of IOTN, Index of Treatment Needs) [9] that
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needed RME as initial phase of interceptive treatment were enrolled from June 2015 to January
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2016. All these patients underwent a preliminary orthodontic evaluation including radiographic
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examination such as Orthopantomography and Teleradiography and for each patient intra- and
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extra-oral photographic documentation was collected (Fig. 1.a, 1.b).
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The subjects were selected regardless of sex, social class or race, with the following
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exclusion criteria: genetic disease or congenital syndromes, systemic diseases, periodontal disease,
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ENT diseases, bad habits and mouth breathing; previous orthodontic treatment. Furthermore, all
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subjects included had not undergone any previous ENT surgery.
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All patients were in mixed or early permanent dentition phase, with the first upper molars fully
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erupted and in prepubertal phase (stage CS1-CS2) according to Cervical Vertebral Maturation
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method [10].
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At the enrolment into the study, parents together with the children were administered a
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SNOT 22 questionnaire as already done. [7] All the children enrolled scored < 1 on the SNOT 22
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and were considered to have “healthy noses”. [7,8]
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The subjects were then randomized into two groups: the study group (11 subjects, mean age
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8,27 ± 1,62 years) underwent RME treatment; the control group (11 subjects; mean age
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8,27 ± 1,25 years) remained under observation for the period of the study, and was subsequently
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treated.
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Both groups underwent all nasal procedures (PNIF, AAR, and olfactory measurements) and
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the evaluation of nasal symptoms by means of SNOT 22. In particular, at the enrolment into the
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study before RME application (T0), at the end of the active phase of the expansion (T1, 25-40 days
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ACCEPTED MANUSCRIPT after RME application; mean 30,18 ± 5,33) and 6 months after the second examination (T2) for the
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study group and at the enrolment into the study (T0), after 1 month (T1) and 6 month after the
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second examination (T2) for the control group. All nasal procedures were performed at ENT Clinic,
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Department of Neurosciences DNS of Padua University. All tests were performed by the same
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operator.
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The present investigation was conducted in accordance with the 1996 Helsinki Declaration
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and was approved by the internal committee of the Sections involved. Written informed consent
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was obtained from all children’ parents before undertaking any study-related procedures.
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111 2.1 Olfactory test
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All children underwent a quick olfactory screening test with the Nez du Vin, which involves
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identifying six aromas (lemon, mint, strawberry, pine, vanilla, smoke) by giving multiple-choice
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answers, as reported elsewhere. [7,11] The test was further simplified with cards showing pictures-
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related odours [7]. As they all revealed a normal sense of smell (scores of 5 or 6), they were then
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studied to ascertain their odour threshold for N-Butanol (Burghart Medical Technology, Wedel,
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Germany), using the Sniffin’ Sticks® test as already described. [11,12]
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2.2 Nasal respiratory evaluation
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A portable Youlten peak flow meter (Clement Clark International) was used for the measurement of
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PNIF. PNIF measurements were conducted as previously reported. [6, 13, 14] Nasal respiratory
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evaluation was also conducted using AAR (Rhinolab, Rendsburg, Germany) as previously
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described [7,16]. AAR values were expressed in Pascal (Pa).
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2.3 Rapid Maxillary Expansion
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After maxillary impression, for each child of the study group was installed an Hyrax-type Rapid
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Maxillary Expander, designed with bands on permanent molars, an 8-mm expansion screw (Leone
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S.p.A., Sesto Fiorentino, Firenze) and palatal arms resting on deciduous canines. [17,18,19] (Fig. 2)
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The expanders were cemented with light-curing cement Transbond Plus for bands and parents 6
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ACCEPTED MANUSCRIPT were instructed to activate the screw, with a quarter turn each day. Each quarter turn corresponded
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to 0,2 mm. The average expansion was of 6,04 ± 1,07 mm (range 5-8 mm) with an average of
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30,18 ± 5,33 total activations of the screw (range 25-40).
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2.4 Statistical analysis
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The Wilcoxon test was used to compare PNIF, AAR, N-Butanol Olfactory Threshold, SNOT 22 for
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nasal obstruction (22nd question) and for smell (21st question) obtained at the different time
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intervals (T0, T1 and T2) for each group and between the two groups. A p-value <0.05 was
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considered statistically significant. The R: a language and environment for statistical computing (R
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Foundation for Statistical Computing, Vienna, Austria) was used for all analyses.
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Of the 22 children enrolled none was lost during the 6-months follow-up and they all met
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scrupulously the three appointments. In the study group, PNIF values significantly increased at T1
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and T2 compared to T0, (p = 0.003 and p = 0.0002, respectively) (Fig. 3a). It was also possible to
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appreciate a significant improvement of the N-Butanol olfactory threshold values between T0-T1 (p
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= 0.011), T1-T2 (p = 0.012) and T0-T2 (p = 0.0003) (Fig. 3b). Regarding AAR values, no
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significant changes were found between the three-time intervals (Fig. 3c). Analysing the values in
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the control group, no significant differences were found for any of the variables considered between
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the three different evaluations (Fig. 4a, 4b, 4c).
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Comparing the T0-T2 mean values variations between the two groups, we could not find
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any change in nasal resistances for AAR, (Fig. 5a). On the other hand, PNIF and N-Butanol
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olfactory threshold values showed an improvement in the study group compared to the control
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group (p=0.0005 for both) (Fig. 5b, 5c).
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Neither nasal obstruction, assessed using the 22nd question of the SNOT22, nor olfactory
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perception, assessed with the 21st SNOT22 question (the possible answers were: 0 no problem, 1
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very mild problem, 2 mild problem, 3 moderate problem, 4 severe problem, 5 the worst possible
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problem) changed significantly during the follow-up in both groups.
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ACCEPTED MANUSCRIPT 4.Discussion
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Rapid maxillary expansion (RME) is an effective orthopaedic procedure that has been routinely
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used in growing patients in orthodontics since the second half of last century [19,20]. The goal of
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RME is to open the midpalatal suture, providing correct and stable maxillary width [21]. Corrected
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dental and skeletal maxillary transverse discrepancies have been proposed to increase
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nasopharyngeal airway dimensions and improve patients’ nasal breathing [20, 21].
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There is a growing interest in literature in studying the effects of RME on nasal structures.
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Some static-volumetric studies have shown that the rapid expansion of the palate causes an increase
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in the width of the nasal cavities and their volumes [22, 23]. This goes for a larger area available for
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inspirational exchanges, thus reducing air passage resistance. Respiratory studies, thanks to AAR
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and Acoustic Rhinometry (AR), showed a reduction in nasal obstruction and an increase in the
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minimal cross-section areas of the nasal cavities [7, 22, 24].
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Recent studies [7, 24] recommended the use of PNIF, an easy, cost-effective, fast, well-
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reproducible method comparable to AAR, for studying nasal flows. PNIF, in fact, has proved to be
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a valid tool for diagnosing nasal obstruction [15] also in the paediatric population [13].
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The present paper follows another one conducted in 2014. [7] In the previous study PNIF,
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AAR and N-Butanol threshold values were compared before and after RME in a paediatric
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population, with significant improvements in PNIF values and olfactory threshold after the
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treatment [7]. A limitation of that study was the absence of a control group, so it was not possible
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to definitely exclude that such improvements could be secondary to a "learning" effect.
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In this study, a control group was also considered, matched by age, stage of growth and
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dentoskeletal characteristics. It is interesting to note that the results in the study group are pretty
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much overlapping with those obtained in the previous study.
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significant increase immediately after the end of the active phase of expansion, with a further
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marginally significant (p=0.12) improvement at T2 control. Similarly to the previous work, AAR
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did not show significant variations after RME, although in the previous one a trend towards a
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In particular, PNIF showed a
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ACCEPTED MANUSCRIPT significant decrease in nasal resistances was observed. N-Butanol olfactory threshold improved
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significantly after the active phase of expansion, continuing to improve even after six months (T2),
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accordingly to the previous results [7]. Interestingly, such PNIF and olfactory threshold changes
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were not observed in the control group, possibly demonstrating that RME treatment determines
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changes in nasal flows, measurable by PNIF, and olfactory threshold, and that such variation is not
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related either to a "learning" effect or to the growth of the small patients (at the end of the study all
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subjects enrolled, compared to T0, were 6-7 months older). Regarding AAR results, contrary to
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what could have been expected, but in a way comparable to other works [7, 20, 27], AAR did not
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show any significant variation in both groups. In several studies, AAR and PNIF correlated, anyway
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their correlation is usually acceptable, but not strong. [24]. A possible explanation may be that these
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instruments measure two different physical entities, namely AAR the nasal resistances, indirectly
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calculated from the values of nasal flows and pressures under resting breathing conditions, while
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PNIF the maximal inspiratory flows. Once more, the measurement of forced inspiratory flows by
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means of PNIF appears more sensitive to assess the respiratory changes that are obtained after RME
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than the measurement of nasal resistance measured by means of AAR. This result, already observed
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[7], is also comparable with Compadretti and collaborators’ work results, which showed that, in 27
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paediatric subjects, basal AAR, unlike AR, did not significantly change after RME [22]. It is also
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possible to suppose that the time needed to achieve significant changes in nasal resistances is
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greater than that required to appreciate an increase in forced nasal flows [29]. Another possible
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explanation of this result might dwell in the difficulty of the protocol needed to perform a
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rhinomanometry. Such a complex method requires considerable experience from the operator and
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collaboration from the tested subjects. It is therefore possible to assume that, given the age of the
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study population, this method is not the best tool for evaluating changes in respiratory function after
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RME. Finally, N-Butanol olfactory threshold improved only in the study group, confirming the
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hypothesis that RME provides an increase in nasal flows (evidenced by PNIF), and then an increase
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olfactory sensitivity in terms of threshold.
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The present study suggests that rapid maxillary expansion, besides of being a valid method to solve
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dental and skeletal crossbite in growing children, may lead to an improvement of olfactory function,
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in terms of N-butanol olfactory threshold. This could be the direct consequence of an increase of
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nasal flows, well demonstrated by the significantly higher PNIF values in the study group at the end
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of the treatment (T1), and even more after 6 months (T2). These results are in line with those found
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in the pilot study [7]. Similarly to the previous results, [7] the present study did not show a
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significant improvement in nasal resistances, measured by AAR.
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Further studies, based on larger series and possibly using a 4-phase rhinomanometer should be
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performed in order to see if studying the effective resistances during the entire breath could allow to
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demonstrate any nasal resistance variation after RME. [30]
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Acknowledgments: none;
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Conflict of Interest: none;
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Sponsor's Role: This research did not receive any specific grant from funding agencies in the
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public, commercial, or not-for-profit sectors.
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Fig. 1: Intra-oral frontal view of a child before (1a) and after (1b) the enrolment into the study
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showing a bilateral cross-bite with mandibular deviation
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Fig. 2: Rapid Maxillary Expander (Hyrax) once in place.
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Fig. 3: Boxplots showing value changes for the three variables before RME treatment (T0), at the
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end of the active phase of the expansion (T1) and after 6 months from RME treatment (T2) in the
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study group.
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RME: rapid maxillary expansion.
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PNIF: peak nasal inspiratory flow
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AAR: anterior active rhinomanometry
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Butanol: N-Butanol olfactory threshold
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Fig. 4: Boxplots showing value changes for the three variables at the enrolment (T0), 30 days after
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the enrolment (T1) and 6 months after the enrolment (T2) in the control group.
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RME: rapid maxillary expansion.
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PNIF: peak nasal inspiratory flow
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AAR: anterior active rhinomanometry
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Butanol: N-Butanol olfactory threshold
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Fig 5: boxplots showing the mean values differences for the three variables between the study and
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the control groups in time interval T0-T2.
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RME: rapid maxillary expansion.
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PNIF: peak nasal inspiratory flow
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AAR: : anterior active rhinomanometry
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Butanol: N-Butanol olfactory threshold
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