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Changes in the upper airway volume after orthognathic surgery: three-dimensional measurements in a supine body position

  • D. Pellby
    Affiliations
    Department of Imaging and Function, Skåne University Hospital, Lund, Sweden
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  • M. Bengtsson
    Correspondence
    Corresponding author at: Department of Oral & Maxillofacial Surgery, Skåne University hospital, Lund, Sweden.
    Affiliations
    Department of Oral & Maxillofacial Surgery, Skåne University hospital, Lund, Sweden

    Department of Clinical Sciences, Faculty of Medicine, Lund University, Lund, Sweden
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Open AccessPublished:December 06, 2022DOI:https://doi.org/10.1016/j.ijom.2022.11.012

      Abstract

      The objectives of this study were to analyse the changes in airway cross-sectional areas and volumes due to surgical movements of the jaws and to identify any possible correlation with the direction of the movements. Fifty-seven participants, aged 18–28 years (mean 20.8 years) at surgery, were followed up for 12 months postoperatively. Pre- and postoperative measurements of the facial region obtained from computed tomography in a supine position were analysed according to the surgical movements and changes in the upper airways. Intra-rater reliability was assessed. Comparisons and correlations of jaw movements, changes in airway volume, and body mass index (BMI) were made. The cohort showed a significant change between the pre- and postoperative measurements for areas associated with the anterior nasal spine (P = 0.013), posterior nasal spine (P = 0.049), uvula (P = 0.006), and epiglottis (P = 0.046). Additionally, a correlation was found between the airway volume change and the change in mandible position (correlation coefficient 0.324, P = 0.014). All participants were non-smokers, and no correlation was observed between BMI and the upper airway volume. Changes in the upper airway can be expected following surgical movements of the jaws. A correlation was shown between a sagittal direction of the movements and the changes in the airways. Patients with obstructive sleep apnoea who are indicated for surgical movements of the jaws are expected to benefit from orthognathic surgery.

      Keywords

      Breathing difficulties often lead to impaired sleep and consequently to a decrease in the individual’s overall capacity and performance.
      • Baldwin C.M.
      • Griffith K.A.
      • Nieto F.J.
      • O’Connor G.T.
      • Walsleben J.A.
      • Redline S.
      The association of sleep-disordered breathing and sleep symptoms with quality of life in the Sleep Heart Health Study.
      • Sacchetti L.M.
      • Mangiardi P.
      Obstructive sleep apnea causes, treatment and health implications.
      Obstructive sleep apnoea (OSA), which is estimated to occur in 5–10% of the population in Europe and the USA,
      • Bondemark L.
      • Lindman R.
      Craniomandibular status and function in patients with habitual snoring and obstructive sleep apnoea after nocturnal treatment with a mandibular advancement splint: a 2-year follow-up.
      • Young T.
      • Peppard P.E.
      • Gottlieb D.J.
      Epidemiology of obstructive sleep apnea: a population health perspective.
      • Walker-Engstrom M.L.
      • Wilhelmsson B.
      • Tegelberg A.
      • Dimenas E.
      • Ringqvist I.
      Quality of life assessment of treatment with dental appliance or UPPP in patients with mild to moderate obstructive sleep apnoea. A prospective randomized 1-year follow-up study.
      may have a great impact on health-related quality of life.
      • Baldwin C.M.
      • Griffith K.A.
      • Nieto F.J.
      • O’Connor G.T.
      • Walsleben J.A.
      • Redline S.
      The association of sleep-disordered breathing and sleep symptoms with quality of life in the Sleep Heart Health Study.
      Known predisposing factors are obesity, smoking, and older age.
      • Gami A.S.
      • Caples S.M.
      • Somers V.K.
      Obesity and obstructive sleep apnea.
      • Tishler P.V.
      • Larkin E.K.
      • Schluchter M.D.
      • Redline S.
      Incidence of sleep-disordered breathing in an urban adult population: the relative importance of risk factors in the development of sleep-disordered breathing.
      Medical, behavioural, and surgical treatment options are available, and the treatment is planned in detail on an individual basis. There is debate regarding the single method that gives the best normalization of function. Multidisciplinary assessment is proposed due to the complex aetiology of OSA.
      • Sacchetti L.M.
      • Mangiardi P.
      Obstructive sleep apnea causes, treatment and health implications.
      • Walker-Engstrom M.L.
      • Tegelberg A.
      • Wilhelmsson B.
      • Ringqvist I.
      4-year follow-up of treatment with dental appliance or uvulopalatopharyngoplasty in patients with obstructive sleep apnea: a randomized study.
      Methods aimed at providing permanent anatomical corrections may result in better treatment outcomes in OSA therapy. Such methods may also improve compliance with additional methods, e.g. positive airway pressure treatment.
      Alterations of the upper airway compartment will permanently alter the person’s breathing capability. Orthognathic surgery, primarily used to correct severe malocclusion and dentofacial deformities,
      • Angle E.H.
      Some studies in occlusion.
      • Hullihen S.P.
      Case of elongation of underjaw and distortion of face and neck, caused by burn, successfully treated.
      • Obwegeser H.
      The indications for surgical correction of mandibular deformity by the sagittal splitting technique.
      • Wassmund M.
      Frakturen und Luxationen des Gesichtsschädels.
      alters the anatomy of the hard tissue in the facial region, as well as the surrounding structures. The upper airway compartment is in close proximity to the teeth and jaws. Consequently, changes in the respiratory volume after orthognathic surgery are expected,
      • Kochel J.
      • Meyer-Marcotty P.
      • Sickel F.
      • Lindorf H.
      • Stellzig-Eisenhauer A.
      Short-term pharyngeal airway changes after mandibular advancement surgery in adult Class II patients—a three-dimensional retrospective study.
      • Magnusson A.
      • Bjerklin K.
      • Nilsson P.
      • Jonsson F.
      • Marcusson A.
      Nasal cavity size, airway resistance, and subjective sensation after surgically assisted rapid maxillary expansion: a prospective longitudinal study.
      and have been shown previously.
      • Moscarino S.
      • Kötter F.
      • Brandt M.
      • Modabber A.
      • Kniha K.
      • Hölzle F.
      • Wolf M.
      • Möhlhenrich S.C.
      Influence of different surgical concepts for moderate skeletal class II and III treatment on the nasopharyngeal airway space.
      • Kim J.S.
      • Kim J.K.
      • Hong S.C.
      • Cho J.H.
      Pharyngeal airway changes after sagittal split ramus osteotomy of the mandible: a comparison between genders.
      Changes in the upper airway volume after orthognathic surgery have previously been evaluated using measurements from three-dimensional images obtained by cone beam computed tomography (CBCT).
      • Kochel J.
      • Meyer-Marcotty P.
      • Sickel F.
      • Lindorf H.
      • Stellzig-Eisenhauer A.
      Short-term pharyngeal airway changes after mandibular advancement surgery in adult Class II patients—a three-dimensional retrospective study.
      This technique examines the patient in an upright position, while the position most associated with breathing problems is the resting supine position.
      • Joosten S.A.
      • O’Driscoll D.M.
      • Berger P.J.
      • Hamilton G.S.
      Supine position related obstructive sleep apnea in adults: pathogenesis and treatment.
      • Van Holsbeke C.S.
      • Verhulst S.L.
      • Vos W.G.
      • De Backer J.W.
      • Vinchurkar S.C.
      • Verdonck P.R.
      • van Doorn J.W.
      • Nadjmi N.
      • De Backer W.A.
      Change in upper airway geometry between upright and supine position during tidal nasal breathing.
      The hypothesis for the present study is that even small changes to the facial skeleton will have a measurable impact on the upper airway in a resting position. Hence, the aim of this study was to analyse the impact of orthognathic surgery on the upper airway respiratory volume in a supine position. The primary objective was to measure changes in the airway due to surgical movements of the teeth and jaws. The secondary objective was to determine any possible correlation between the direction of the movements and the changes in airway volume. Expected confounding factors including smoking habit and body mass index (BMI) were also analysed.

      Materials and methods

      Subjects

      Consecutive patients with a diagnosed dentofacial deformity, aged between 18 and 30 years, who were referred to the Department of Oral and Maxillofacial Surgery, University Hospital of Skåne in Lund, Sweden were invited to participate in the study. Regarding the malocclusion, there had to be a deviation of at least 5 mm in the sagittal and/or vertical aspect from the normal occlusion, as measured between the incisors of the upper and lower jaws. Patients with systemic diseases of the musculoskeletal system, drug abuse, mental health disorder, or disease of the temporomandibular joint were excluded from the study. The participants were consented for participation prior to the study onset, and the study was performed in accordance with the principles laid down in the Declaration of Helsinki 1964 and its later amendments. Due to the need for increased radiation exposure compared to routine X-ray examinations, the study protocol was evaluated by the local radiation protection committee in southern Sweden. Their opinion was attached to the application to the Ethics Committee. The project was approved by the Ethics Committee in Gothenburg 2011–04–09 (Dnr. 011–11). The study was registered prospectively at ClinicalTrials.gov (NCT05060133; https://clinicaltrials.gov/ct2/show/NCT05060133).
      The participants were included prior to surgery but after the completion of preoperative orthodontic treatment.

      Methods

      The study was performed as an observational cohort study based on data collected prospectively in a previously presented study.
      • Bengtsson M.
      • Wall G.
      • Greiff L.
      • Rasmusson L.
      Treatment outcome in orthognathic surgery—a prospective randomized blinded case-controlled comparison of planning accuracy in computer-assisted two- and three-dimensional planning techniques (part II).
      This cohort of patients also participated in a health-related quality of life study,
      • Bengtsson M.
      • Wall G.
      • Larsson P.
      • Becktor J.P.
      • Rasmusson L.
      Treatment outcomes and patient-reported quality of life after orthognathic surgery with computer-assisted 2- or 3-dimensional planning: a randomized double-blind active-controlled clinical trial.
      and underwent clinical examinations, dental casts, photography, a questionnaire, and two- and three-dimensional radiographs and cephalometric techniques. BMI and smoking habits were recorded. Computed tomography (CT) of the head and neck region was performed prior to and 12 months after surgery.
      The CT was performed with the following settings: 120 kV, matrix 512 × 512 pixels, slice thickness 0.800 mm, slice increment 0.399 mm, pixel size 0.352 mm. The field of view was set from the top of the forehead to the inferior part of the throat. The image recordings (radiographs and photographs) were imported into a computer software program (Simplant Pro 12.00 OMS; Materialise, Leuven, Belgium), which was used for the analysis of the orthodontic and surgical movements. Three-dimensional cephalometric measurements of distances and angles between standardized landmarks were performed in the pre- and postoperative CT images. Changes in landmark positions in the two examinations were recorded as a measure of the surgical movements. The cephalometric measurements used were the A-point, B-point, sella–nasion–A-point angle (SNA), and sella–nasion–B-point angle (SNB).
      Upper airway cross-sectional areas and volumes were compared between the pre- and postoperative CT images using Philips IntelliSpace Portal 11 software (Philips Healthcare, Best, the Netherlands) (Fig. 1). The upper airway was segmented and the measurements were performed according to the method described by Kim et al.
      • Kim Y.J.
      • Hong J.S.
      • Hwang Y.I.
      • Park Y.H.
      Three-dimensional analysis of pharyngeal airway in preadolescent children with different anteroposterior skeletal patterns.
      A pre-set threshold level for imaging air in the software (Hounsfield units) was used in all cases. It was thereby ensured that all images analysed were set up with the same threshold level. The areas investigated were those associated with the anterior nasal spine (ANS), the region vertical to the posterior nasal spine (PNS-vertical), the region horizontal to the posterior nasal spine (PNS-horizontal), uvula, and epiglottis. Hence, the upper airway was segmented into four compartments, which were used for the volume measurements. The cross-sectional areas of the airway between these segments, the individual segment volumes, and the total airway volume were measured (Fig. 1). The intra-rater reliability of the area, volume, and cephalometric landmark measurements was assessed by repeating the measurements on 10 subjects with an interval of at least 2 weeks.
      Fig. 1
      Fig. 1Airway volume measurement on CT. Segmented analysis of the upper airway according to the method described by Kim et al.
      • Kim Y.J.
      • Hong J.S.
      • Hwang Y.I.
      • Park Y.H.
      Three-dimensional analysis of pharyngeal airway in preadolescent children with different anteroposterior skeletal patterns.
      Measurements of volume segments and areas (at the intersection of segments) of the upper airway on preoperative CT, using Philips IntelliSpace Portal 11. Upper right: schematic cross-section in the midsagittal plane showing the segmentation of the upper airway into four volumes. The green lines represent the interfaces between the segments. The green marker points indicate A-point (A), B-point (B), sella turcica (S), nasion (N), anterior nasal spine (ANS), posterior nasal spine (PNS), uvula (Uv), and epiglottis (Epi). The laryngeal (yellow), pharyngeal (blue), epi-pharyngeal (green), and nasal (pink) spaces are visualized in 3D.
      In total, 616 cephalometric landmarks were placed, and 536 cephalometric measurements and 1742 volumetric measurements were performed. Comparisons and correlations of jaw movements, changes in airway areas and volumes, and BMI were made.

      Statistical methods

      The sample size was based on the numbers of patients included in previous similar studies performed in other centres.
      • Marchetti C.
      • Bianchi A.
      • Bassi M.
      • Gori R.
      • Lamberti C.
      • Sarti A.
      Mathematical modeling and numerical simulation in maxillo-facial virtual surgery (VISU).
      • Xia J.J.
      • Gateno J.
      • Teichgraeber J.F.
      • Christensen A.M.
      • Lasky R.E.
      • Lemoine J.J.
      • Liebschner M.A.
      Accuracy of the computer-aided surgical simulation (CASS) system in the treatment of patients with complex craniomaxillofacial deformity: a pilot study.
      • Mazzoni S.
      • Badiali G.
      • Lancellotti L.
      • Babbi L.
      • Bianchi A.
      • Marchetti C.
      Simulation-guided navigation: a new approach to improve intraoperative three-dimensional reproducibility during orthognathic surgery.
      • Tucker S.
      • Cevidanes L.H.
      • Styner M.
      • Kim H.
      • Reyes M.
      • Proffit W.
      • Turvey T.
      Comparison of actual surgical outcomes and 3-dimensional surgical simulations.
      • Hsu S.S.
      • Gateno J.
      • Bell R.B.
      • Hirsch D.L.
      • Markiewicz M.R.
      • Teichgraeber J.F.
      • Zhou X.
      • Xia J.J.
      Accuracy of a computer-aided surgical simulation protocol for orthognathic surgery: a prospective multicenter study.
      • Ohrbach R.
      • Larsson P.
      • List T.
      The jaw functional limitation scale: development, reliability, and validity of 8-item and 20-item versions.
      Simple statistics, the mean and standard deviation, and the 95% confidence interval (CI) were calculated. Differences in airway volume and movements from preoperative to postoperative were compared with the t-test. Spearman’s correlation analysis was used to test the correlation between the surgical movements and volume changes. Two-sided tests and an alpha level of 0.05 for acceptance/rejection of the null hypotheses were used. The reliability test (test–retest reliability) was performed with Fisher’s test for paired comparisons and Dahlberg’s formula. A Bland–Altman plot was used to determine any correlation between the level of mean airway volume and measurement error.
      • Bland J.M.
      • Altman D.G.
      Statistical methods for assessing agreement between two methods of clinical measurement.
      IBM SPSS Statistics for Windows version 26.0 (IBM Corp., Armonk, NY, USA) was used for all computations.

      Results

      Sixty-two of 128 consecutive patients who were invited to participate were included in this study. The participants were treated for dentofacial deformities and severe malocclusion with orthognathic surgery in the Department of Oral and Maxillofacial Surgery in Lund between 2011 and 2016. All participants were non-smokers.
      Five patients were lost to follow-up before the 12-month review, hence 57 participants (27 female, 30 male), aged between 18 and 28 years at surgery (mean 20.8 years), were included in the analysis. Regarding the individual treatment plan, 12 participants (21.1%) were treated with a maxillary surgical movement, 16 (28.1%) with a mandibular surgical movement, and 29 (50.9%) with surgical movements of both jaws.
      Descriptive statistics for the whole study cohort are provided in Supplementary Material Table S1. For further analyses, the cohort was divided into the following four subgroups according to the directions of the movements resulting from the surgery: group 1: maxilla (A-point) and chin (B-point) moved forward (n = 18); group 2: maxilla (A-point) moved forward and chin (B-point) moved backward (n = 23); group 3: maxilla (A-point) did not move and chin (B-point) moved forward (n = 5); group 4: maxilla (A-point) did not move and chin (B-point) moved backward (n = 11). Descriptive statistics for each of these groups are also given in Supplementary Material Table S1.
      Due to mandibular autorotation, the chin moved without any mandibular surgery in the 12 patients treated with maxillary surgery only. Hence movements of both the maxilla and mandible were observed for 41 patients: 29 who underwent surgery to both jaws and 12 who underwent maxillary surgery.
      The results of the reliability tests for the placement of cephalometric landmarks and measurements of airway volume and areas are reported in Supplementary Material Table S2. The mean difference between the two measurements of the total airway volume was 1.66 cm3. The Bland–Altman analysis showed a variance of measurement difference of 0.25–3.65 and no indication of any linear correlation to the mean (Fig. 2).
      Fig. 2
      Fig. 2Scatterplot of measurement error. Bland–Altman scatterplot of the variation in measurement difference at the range of means of the repeated volume measurements.
      • Bland J.M.
      • Altman D.G.
      Statistical methods for assessing agreement between two methods of clinical measurement.
      Comparisons of the preoperative and 12-month postoperative measurements of cross-sectional areas and total airway volume for the whole cohort and for the four subgroups, performed with a paired t-test, are shown in Table 1. No significant difference in total airway volume between the pre- and postoperative measurements was observed for the whole cohort, or for any of the four subgroups. For the whole cohort, significant changes between the pre- and postoperative measurements were found for the airway cross-sectional areas associated with the ANS (increase, P = 0.013), PNS-vertical (decrease, P = 0.049), uvula (decrease, P = 0.006), and epiglottis (decrease, P = 0.046). Further analysis by subgroup showed statistically significant changes between the pre- and postoperative measurements for cross-sectional area at ANS in group 1 (increase, P = 0.034) and group 2 (increase, P = 0.008), PNS-horizontal in group 4 (decrease, P = 0.006), and uvula in group 2 (decrease, P = 0.009) and group 4 (decrease, P = 0.018).
      Table 1Comparisons of the mean differences in airway cross-sectional area (mm2) and total airway volume (cm3) of the upper airway between the preoperative and 12-month follow-up measurements—whole cohort and by group.
      Group 1: maxilla and chin moved forward; group 2: maxilla moved forward and chin moved backward; group 3: maxilla did not move and chin moved forward; group 4: maxilla did not move and chin moved backward.
      Whole cohort (N = 57)Group 1 (n = 18)Group 2 (n = 23)Group 3 (n = 5)Group 4 (n = 11)
      MD (95% CI) P-value
      Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      MD (95% CI) P-value
      Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      MD (95% CI) P-value
      Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      MD (95% CI) P-value
      Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      MD (95% CI) P-value
      Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      Volume total0.20

      (−2.22, 2.63)

      P = 0.867
      2.97

      (−1.67, 7.63)

      P = 0.197
      − 1.21

      (−5.27, 2.84)

      P = 0.541
      − 0.84

      (−6.30, 4.62)

      P = 0.691
      − 0.88

      (−7.53, 5.76)

      P = 0.773
      Area ANS17.74

      (3.86, 31.62)

      P = 0.013 *
      26.25

      (2.18, 50.32)

      P = 0.034 *
      31.91

      (9.26, 54.56)

      P = 0.008 *
      − 7.55

      (−59.14, 44.05)

      P = 0.705
      − 14.31

      (−48.43, 19.81)

      P = 0.372
      Area PNS-vertical− 27.51

      (−54.93, −0.08)

      P = 0.049 *
      − 42.15

      (−91.29, 6.98)

      P = 0.088
      − 49.45

      (−101.03, 2.13)

      P = 0.059
      41.55

      (−35.97, 119.07)

      P = 0.211
      10.95

      (−35.91, 57.81)

      P = 0.614
      Area PNS-horizontal− 1.64

      (−32.59, 28.65)

      P = 0.898
      − 0.40

      (−48.83, 48.03)

      P = 0.986
      23.29

      (−37.85, 84.43)

      P = 0.437
      21.68

      (−126.21, 169.57)

      P = 0.705
      − 65.80

      (−108.35, −23.26)

      P = 0.006 *
      Area uvula− 57.89

      (−93.57, −16.71)

      P = 0.006 *
      1.32

      (−63.44, 66.09)

      P = 0.966
      − 89.74

      (−154.83, −24.64)

      P = 0.009 *
      4.37

      (−199.98, 208.72)

      P = 0.956
      − 105.37

      (−188.74, −22.00)

      P = 0.018 *
      Area epiglottis− 35.30

      (−66.99, −0.56)

      P = 0.046 *
      − 0.68

      (−48.03, 46.67)

      P = 0.976
      − 53.35

      (−106.85, 0.16)

      P = 0.051
      24.60

      (−200.40, 249.60)

      P = 0.777
      − 75.32

      (−168.12, 17.48)

      P = 0.101
      ANS, anterior nasal spine; CI, confidence interval; MD, mean difference; PNS, posterior nasal spine.
      a Group 1: maxilla and chin moved forward; group 2: maxilla moved forward and chin moved backward; group 3: maxilla did not move and chin moved forward; group 4: maxilla did not move and chin moved backward.
      b Paired t-test to determine whether the differences were statistically significant. * P < 0.05 (two-tailed).
      The mean BMI of the study participants was 23.56 kg/m2 (95% CI 22.42–24.71, range 17.24–43.34 kg/m2), indicating that most of the participants in the study had a normal weight. Only one participant, with a BMI of 43.34 kg/m2, was categorized as obese. The mean BMI was determined to be similar across the subgroups (range 20.36–25.26 kg/m2) (Supplementary Material Table S1). Spearman’s test for the correlation between BMI and upper airway volume did not show any significant correlation for preoperative volume (r = 0.056, P = 0.680) or for the change in volume between the pre- and postoperative measurements (r = 0.222, P = 0.097).
      The results of the correlation test between surgical movements and changes in the upper airway volume are shown in Table 2. A significant correlation was found between the airway volume change and the change in mandible position (correlation of the change in SNB with the volume change: correlation coefficient 0.324, P = 0.014).
      Table 2Correlations between the mean differences of the surgical movements and changes in the total upper airway volume between the pre- and postoperative measurements—whole cohort and by group.
      Cephalometric landmark/angleVolume change
      Whole cohort (N = 57)Group 1 (n = 18)Group 2 (n = 23)Group 3 (n = 5)Group 4 (n = 11)
      Corr. coeff. (95% CI) P-valueCorr. coeff. (95% CI) P-valueCorr. coeff. (95% CI) P-valueCorr. coeff. (95% CI) P-valueCorr. coeff. (95% CI) P-value
      A-point0.156

      (−0.11, 0.40)

      P = 0.247
      0.225

      (−0.28, 0.63)

      P = 0.369
      − 0.053

      (−0.46, 0.37)

      P = 0.809
      0.300

      (−0.80, 0.94)

      P = 0.624
      0.245

      (−0.42, 0.74)

      P = 0.467
      B-point0.241

      (−0.02, 0.40)

      P = 0.071
      0.458

      (−0.04, 0.77)

      P = 0.056
      − 0.030

      (−0.44, 0.39)

      P = 0.893
      0.300

      (−0.80, 0.94)

      P = 0.624
      0.282

      (−0.39, 0.76)

      P = 0.401
      Angle SNA0.252

      (−0.01, 0.48)

      P = 0.059
      0.445

      (−0.05, 0.77)

      P = 0.064
      − 0.021

      (−0.43, 0.39)

      P = 0.926
      0.051

      (−0.87, 0.89)

      P = 0.935
      0.236

      (−0.43, 0.74)

      P = 0.484
      Angle SNB0.324

      (0.06, 0.54)

      P = 0.014
      Correlation significant at the 0.05 level (two-tailed).
      0.640

      (0.20, 0.87)

      P = 0.004
      Correlation significant at the 0.01 level (two-tailed).
      − 0.051

      (−0.45, 0.37)

      P = 0.818
      0.900

      (−0.17, 1.00)

      P = 0.037
      Correlation significant at the 0.05 level (two-tailed).
      0.218

      (−0.45, 0.73)

      P = 0.519
      Corr. coeff., correlation coefficient; SNA, sella–nasion–A-point angle; SNB, sella–nasion–B-point angle.
      aGroup 1: maxilla and chin moved forward; group 2: maxilla moved forward and chin moved backward; group 3: maxilla did not move and chin moved forward; group 4: maxilla did not move and chin moved backward.
      * Correlation significant at the 0.05 level (two-tailed).
      ** Correlation significant at the 0.01 level (two-tailed).
      Scatterplots for the correlation of the airway volume change and movement at A-point and B-point are shown in Fig. 3, Fig. 4, respectively. These showed a tendency towards an increased airway volume for groups 1 and 2 that was dependent on the magnitude of surgical movement of the A-point. A similar tendency of correlation to the magnitude of movement of the B-point was not evident.
      Fig. 3
      Fig. 3Scatterplot of maxillary movement. Scatterplot for the correlation of airway volume change and movement of A-point for each subgroup of the study cohort.
      Fig. 4
      Fig. 4Scatterplot of mandibular movement. Scatterplot for the correlation of airway volume change and movement of B-point for each subgroup of the study cohort.

      Discussion

      The measurements of the areas and volumes in the whole cohort showed statistically significant changes between the pre- and postoperative values. Significant changes in the cross-sectional area at ANS, PNS-vertical, uvula, and epiglottis were found (Table 1), with an increased area at ANS and a decreased area for the others. This indicates that additional surgical factors may have affected the change. The direction of the movement was expected to have an impact, which is why the cohort was divided into four subgroups according to the direction of the surgical movement. As a mandibular movement was also expected in patients undergoing maxilla-only surgery, the participants were grouped based on the directions of the measured sagittal movements of the cephalometric landmarks, instead of on the surgical technique. The subgroup analysis showed statistically significant changes between the pre- and postoperative measurements for the cross-sectional area at ANS in groups 1 and 2 (increased area), PNS-horizontal in group 4 (decreased area), and uvula in groups 2 and 4 (decreased area) (Table 1). Thus, as was expected, the group with only posterior movements – group 4 – showed a decreased area in the superior pharyngeal airway. Further, the group with only anterior movements – group 1 – showed an increased area of the anterior nasal airway, which also was expected. In group 2, with both anterior and posterior movements, an increased area of the anterior nasal airway and a decreased area of the pharyngeal airway was shown. This group was treated with anterior movements of the maxilla and posterior movements of the mandible, which indicate the same pattern of airway reaction as was detected in groups 1 and 4; i.e. maxillary anterior movements resulted in an increased nasal airway area, while mandibular movements affected the pharyngeal airway in both anterior and posterior movements (Table 1).
      No correlation between BMI and the upper airway volume was seen, which might be due to the overall normal BMI of the patients in the study cohort and previous knowledge that tongue fat is strongly related to OSA.
      The results of the reliability tests on airway measurements showed measurement errors comparable to those reported in other studies.
      • Kochel J.
      • Meyer-Marcotty P.
      • Sickel F.
      • Lindorf H.
      • Stellzig-Eisenhauer A.
      Short-term pharyngeal airway changes after mandibular advancement surgery in adult Class II patients—a three-dimensional retrospective study.
      • Liu Y.T.
      • Gravely J.F.
      The reliability of the ‘Ortho Grid’ in cephalometric assessment.
      • Stabrun A.E.
      • Danielsen K.
      Precision in cephalometric landmark identification.
      Statistically significant differences were observed for all measurements except for SNA (Supplementary Material Table S2). The Bland–Altman plot shows the variation in difference as a function of the mean airway volume (Fig. 2). It shows deviations from the mean difference (1.66 cm3) for all levels of mean airway volume, but without a correlation to the change in the level of the mean.
      Regarding the measurement error for cephalometric landmarks in the three dimensions (Supplementary Material Table S2), an effect of this was observed in the results of measurements of A-point in groups 3 and 4 (Fig. 3). These groups included 16 patients whose treatment did not involve any surgical movement of the maxilla, but who showed movements of A-point. Fourteen of the measured A-points were within the expected range of systematic error. However, the measurements exceeded the expected range in two patients (1.8 mm and 2.5 mm). The reason for this is not clear, but possible factors explaining this might include the postoperative orthodontic movement, which may have affected the bone morphology, or an effect of a late maxillary growth pattern.
      Compared to the observed statistically significant differences between the pre- and postoperative measurements (Table 1), the measured systematic and casual errors of the method were well below these findings.
      A statistically significant correlation was found between the airway change and changes in the SNB angle (Table 2). This was true for the whole cohort, and for groups 1 and 3. These two groups included all patients with mandibular advancement. From this correlation and the findings of a significant change in the airway upon sagittal movements (Table 2), the results of this study support the hypothesis that jaw movements affect the upper airways in a predictable manner.
      However, the patients included in the present study are not representative of an OSA cohort. The study was performed on patients treated because of dentofacial deformities and severe malocclusion. Thus, the studied surgical movements were aimed at treating a condition different from OSA. From the authors’ experience, movements used for the treatment of OSA are designed without a limitation depending on the dental occlusion. Instead, the advancements performed are as large as is allowed by facial aesthetics.
      Despite this, the present study, even with the limited number of participants and a cohort treated with minor surgical movements, showed that changes to the upper airway can be expected following surgical movements of the jaws.
      Regarding multiple testing, the use of too extensive a statistical analysis on a small cohort might risk the detection of findings that support the hypothesis but have weak, or even absent, support in the studied population. Consequently, no further analyses beyond the correlation test were performed in this study.
      Van Holsbeke et al.
      • Van Holsbeke C.S.
      • Verhulst S.L.
      • Vos W.G.
      • De Backer J.W.
      • Vinchurkar S.C.
      • Verdonck P.R.
      • van Doorn J.W.
      • Nadjmi N.
      • De Backer W.A.
      Change in upper airway geometry between upright and supine position during tidal nasal breathing.
      studied changes in the upper airway geometry between the upright and supine body positions and reported that the average and minimum cross-sectional area were 9.76% and 26.90% larger, respectively, in the CBCT scan than in the CT scan. This indicates the need for measurements of the airway in a resting position when evaluating the effect of orthognathic surgery on the respiratory geometry. Thus, in comparison to previous studies,
      • Kochel J.
      • Meyer-Marcotty P.
      • Sickel F.
      • Lindorf H.
      • Stellzig-Eisenhauer A.
      Short-term pharyngeal airway changes after mandibular advancement surgery in adult Class II patients—a three-dimensional retrospective study.
      an advantage of the present study is the recording of the upper airway in a resting supine position, which is the position that most often triggers the symptoms of OSA. A systematic review by Joosten et al.
      • Joosten S.A.
      • O’Driscoll D.M.
      • Berger P.J.
      • Hamilton G.S.
      Supine position related obstructive sleep apnea in adults: pathogenesis and treatment.
      concluded that supine OSA is the dominant phenotype of the OSA syndrome and explained why the supine position so favours upper airway collapse. This also supports the recording of measurements in a supine body position, as was performed in the present study. Through this conformity with the reality of OSA, the results of this study might add important knowledge and insight into the treatment options.
      A systematic review by Chen et al.,
      • Chen H.
      • Aarab G.
      • de Ruiter M.H.
      • de Lange J.
      • Lobbezoo F.
      • van der Stelt P.F.
      Three-dimensional imaging of the upper airway anatomy in obstructive sleep apnea: a systematic review.
      using the PICO format (population, intervention, comparison, outcome), suggested that a small minimum cross-sectional area is the most relevant anatomical characteristic of the upper airway related to the pathogenesis of OSA. This supports the use of airway area measurements in CT scans to evaluate the airway capacity, as was performed in the present study.
      Nevertheless, certain factors that may have affected the airways should be noted; for example, the variation in the neutral head posture in the recording position, variation of landmark positions before and after surgery, and changes in the upper airway due to nasal cycling. To decrease the impact of some of these confounding factors, the participants were instructed to rest their head in a similar position for both the preoperative and follow-up radiography recordings. Further, although segmented measurements of the airway volume were performed, as described by Kim et al.,
      • Kim Y.J.
      • Hong J.S.
      • Hwang Y.I.
      • Park Y.H.
      Three-dimensional analysis of pharyngeal airway in preadolescent children with different anteroposterior skeletal patterns.
      only the total airway volume was used in the analysis because of the changed jaw positions after surgery. Measurements of nasal cycling have shown a 14% larger volume on one side.
      • Zhao K.
      • Scherer P.W.
      • Hajiloo S.A.
      • Dalton P.
      Effect of anatomy on human nasal air flow and odorant transport patterns: implications for olfaction.
      However, because measurements in the present study were performed on both nasal cavities simultaneously, it is likely that the effect of nasal cycling was compensated.
      Due to the limited number of patients included in this study, caution should be applied when drawing any conclusions from the results. The authors suggest that any conclusions should be limited to the variables presenting a statistically significant difference. Any tendencies in the results beyond this limit might be clarified in future studies based on a larger cohort and including patients with OSA. Further, additional knowledge on treatment outcomes would be gained by adding patient-reported outcome measures in future studies. Thus, the volume measurement results could be tested for any correlation with patient perceived improvements.
      In conclusion, the results of this study showed that changes in the upper airway can be expected even with limited surgical movements of the jaws. It was also revealed that a sagittal direction of the movements was correlated with the changes in the airways. Based on these results, patients with OSA who are indicated for surgical movements of the jaws are expected to benefit from orthognathic surgery, with or without additional therapy.

      Ethics approval and consent to participate

      Approval was obtained from the Ethics Committee in Gothenburg 2011–04–09 (Dnr. 011–11).

      Funding

      This work was supported by research funds for oral health-related research from Region Skåne. The sponsor had no influence on the study.

      Acknowledgements

      The authors would like to thank Dr Mikael Korduner, Head of the Oral and Maxillofacial Department, Biostatistician Susann Ullén, PhD, Head of the Department of Epidemiology and Statistical Methodology, Oskar Ibohm, Radiographer, Department of Radiology, Skåne Univeristy hospital, Lund, Sweden for contributing to this study.

      Competing interests

      None.

      Patient consent

      The participants were consented for participation prior to onset and the study was performed in accordance with the principles laid down in the Declaration of Helsinki 1964 and its later amendments.

      Trial registration

      The study is registered at ClinicalTrials.gov (NCT05060133; https://clinicaltrials.gov/ct2/show/NCT05060133).

      Appendix A. Supplementary material

      References

        • Baldwin C.M.
        • Griffith K.A.
        • Nieto F.J.
        • O’Connor G.T.
        • Walsleben J.A.
        • Redline S.
        The association of sleep-disordered breathing and sleep symptoms with quality of life in the Sleep Heart Health Study.
        Sleep. 2001; 24: 96-105
        • Sacchetti L.M.
        • Mangiardi P.
        Obstructive sleep apnea causes, treatment and health implications.
        Otolaryngology Research Advances. Nova Science Publishers, New York2012
        • Bondemark L.
        • Lindman R.
        Craniomandibular status and function in patients with habitual snoring and obstructive sleep apnoea after nocturnal treatment with a mandibular advancement splint: a 2-year follow-up.
        Eur J Orthod. 2000; 22: 53-60
        • Young T.
        • Peppard P.E.
        • Gottlieb D.J.
        Epidemiology of obstructive sleep apnea: a population health perspective.
        Am J Respir Crit Care Med. 2002; 165: 1217-1239
        • Walker-Engstrom M.L.
        • Wilhelmsson B.
        • Tegelberg A.
        • Dimenas E.
        • Ringqvist I.
        Quality of life assessment of treatment with dental appliance or UPPP in patients with mild to moderate obstructive sleep apnoea. A prospective randomized 1-year follow-up study.
        J Sleep Res. 2000; 9: 303-308
        • Gami A.S.
        • Caples S.M.
        • Somers V.K.
        Obesity and obstructive sleep apnea.
        Endocrinol Metab Clin N Am. 2003; 32: 869-894
        • Tishler P.V.
        • Larkin E.K.
        • Schluchter M.D.
        • Redline S.
        Incidence of sleep-disordered breathing in an urban adult population: the relative importance of risk factors in the development of sleep-disordered breathing.
        JAMA. 2003; 289: 2230-2237
        • Walker-Engstrom M.L.
        • Tegelberg A.
        • Wilhelmsson B.
        • Ringqvist I.
        4-year follow-up of treatment with dental appliance or uvulopalatopharyngoplasty in patients with obstructive sleep apnea: a randomized study.
        Chest. 2002; 121: 739-746
        • Angle E.H.
        Some studies in occlusion.
        Angle Orthod. 1968; 38: 79-81
        • Hullihen S.P.
        Case of elongation of underjaw and distortion of face and neck, caused by burn, successfully treated.
        Am J Dent Surg. 1849; 9157
        • Obwegeser H.
        The indications for surgical correction of mandibular deformity by the sagittal splitting technique.
        Br J Oral Surg. 1964; 1: 157-171
        • Wassmund M.
        Frakturen und Luxationen des Gesichtsschädels.
        Herrmann Meuser, 1927
        • Kochel J.
        • Meyer-Marcotty P.
        • Sickel F.
        • Lindorf H.
        • Stellzig-Eisenhauer A.
        Short-term pharyngeal airway changes after mandibular advancement surgery in adult Class II patients—a three-dimensional retrospective study.
        J Orofac Orthop. 2013; 74: 137-152
        • Magnusson A.
        • Bjerklin K.
        • Nilsson P.
        • Jonsson F.
        • Marcusson A.
        Nasal cavity size, airway resistance, and subjective sensation after surgically assisted rapid maxillary expansion: a prospective longitudinal study.
        Am J Orthod Dentofacial Orthop. 2011; 140: 641-651
        • Moscarino S.
        • Kötter F.
        • Brandt M.
        • Modabber A.
        • Kniha K.
        • Hölzle F.
        • Wolf M.
        • Möhlhenrich S.C.
        Influence of different surgical concepts for moderate skeletal class II and III treatment on the nasopharyngeal airway space.
        J Craniomaxillofac Surg. 2019; 47: 1489-1497
        • Kim J.S.
        • Kim J.K.
        • Hong S.C.
        • Cho J.H.
        Pharyngeal airway changes after sagittal split ramus osteotomy of the mandible: a comparison between genders.
        J Oral Maxillofac Surg. 2010; 68: 1802-1806
        • Joosten S.A.
        • O’Driscoll D.M.
        • Berger P.J.
        • Hamilton G.S.
        Supine position related obstructive sleep apnea in adults: pathogenesis and treatment.
        Sleep Med Rev. 2014; 18: 7-17
        • Van Holsbeke C.S.
        • Verhulst S.L.
        • Vos W.G.
        • De Backer J.W.
        • Vinchurkar S.C.
        • Verdonck P.R.
        • van Doorn J.W.
        • Nadjmi N.
        • De Backer W.A.
        Change in upper airway geometry between upright and supine position during tidal nasal breathing.
        J Aerosol Med Pulm Drug Deliv. 2014; 27: 51-57
        • Bengtsson M.
        • Wall G.
        • Greiff L.
        • Rasmusson L.
        Treatment outcome in orthognathic surgery—a prospective randomized blinded case-controlled comparison of planning accuracy in computer-assisted two- and three-dimensional planning techniques (part II).
        J Craniomaxillofac Surg. 2017; 45: 1419-1424
        • Bengtsson M.
        • Wall G.
        • Larsson P.
        • Becktor J.P.
        • Rasmusson L.
        Treatment outcomes and patient-reported quality of life after orthognathic surgery with computer-assisted 2- or 3-dimensional planning: a randomized double-blind active-controlled clinical trial.
        Am J Orthod Dentofacial Orthop. 2018; 153: 786-796
        • Kim Y.J.
        • Hong J.S.
        • Hwang Y.I.
        • Park Y.H.
        Three-dimensional analysis of pharyngeal airway in preadolescent children with different anteroposterior skeletal patterns.
        Am J Orthod Dentofacial Orthop. 2010; 137306.e1–11
        • Marchetti C.
        • Bianchi A.
        • Bassi M.
        • Gori R.
        • Lamberti C.
        • Sarti A.
        Mathematical modeling and numerical simulation in maxillo-facial virtual surgery (VISU).
        J Craniofac Surg. 2006; 17: 661-667
        • Xia J.J.
        • Gateno J.
        • Teichgraeber J.F.
        • Christensen A.M.
        • Lasky R.E.
        • Lemoine J.J.
        • Liebschner M.A.
        Accuracy of the computer-aided surgical simulation (CASS) system in the treatment of patients with complex craniomaxillofacial deformity: a pilot study.
        J Oral Maxillofac Surg. 65. 2007: 248-254
        • Mazzoni S.
        • Badiali G.
        • Lancellotti L.
        • Babbi L.
        • Bianchi A.
        • Marchetti C.
        Simulation-guided navigation: a new approach to improve intraoperative three-dimensional reproducibility during orthognathic surgery.
        J Craniofac Surg. 2010; 21: 1698-1705
        • Tucker S.
        • Cevidanes L.H.
        • Styner M.
        • Kim H.
        • Reyes M.
        • Proffit W.
        • Turvey T.
        Comparison of actual surgical outcomes and 3-dimensional surgical simulations.
        J Oral Maxillofac Surg. 2010; 68: 2412-2421
        • Hsu S.S.
        • Gateno J.
        • Bell R.B.
        • Hirsch D.L.
        • Markiewicz M.R.
        • Teichgraeber J.F.
        • Zhou X.
        • Xia J.J.
        Accuracy of a computer-aided surgical simulation protocol for orthognathic surgery: a prospective multicenter study.
        J Oral Maxillofac Surg. 2013; 71: 128-142
        • Ohrbach R.
        • Larsson P.
        • List T.
        The jaw functional limitation scale: development, reliability, and validity of 8-item and 20-item versions.
        J Orofac Pain. 2008; 22: 219-230
        • Bland J.M.
        • Altman D.G.
        Statistical methods for assessing agreement between two methods of clinical measurement.
        Lancet. 1986; 1: 307-310
        • Liu Y.T.
        • Gravely J.F.
        The reliability of the ‘Ortho Grid’ in cephalometric assessment.
        Br J Orthod. 1991; 18: 21-27
        • Stabrun A.E.
        • Danielsen K.
        Precision in cephalometric landmark identification.
        Eur J Orthod. 1982; 4: 185-196
        • Chen H.
        • Aarab G.
        • de Ruiter M.H.
        • de Lange J.
        • Lobbezoo F.
        • van der Stelt P.F.
        Three-dimensional imaging of the upper airway anatomy in obstructive sleep apnea: a systematic review.
        Sleep Med. 2016; 21: 19-27
        • Zhao K.
        • Scherer P.W.
        • Hajiloo S.A.
        • Dalton P.
        Effect of anatomy on human nasal air flow and odorant transport patterns: implications for olfaction.
        Chem Senses. 2004; 29: 365-379