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Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419

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Journal of Cranio-Maxillo-Facial Surgery

journal homepage: www.jcmfs.com

Distraction osteogenesis as followed by CT scan in Pierre Robin sequenceq,qq

Ahmed Mahrous Mohamed a,*, Awad Al Bishri b,1, Ahmed Haroun Mohamed c,2

aMaxillofacial and Plastic surgery, Plastic Surgery Department, Faculty of medicine, El Minia University, EgyptbMaxillofacial Surgery Department, Al Noor Specialist Hospital, Makkah, Saudia ArabiacDiagnostic Radiology, Faculty of Medicine, Mansoura University, Al Noor Specialist Hospital, Makkah, Saudia Arabia

a r t i c l e i n f o

Article history:Paper received 3 April 2010Accepted 11 October 2010

Keywords:Distraction osteogenesisThree-dimensional CT scanPierre Robin sequence

q The department to which the work is attributed to:department of maxillofacial surgery, Al Noor SpecialArabia; Head of this institution and head of theDr Awad El Bishri who is one of the authors; the woethical committee of the hospital. Parents gave informqq Sources of support in the form of grants: There w

grants.* Corresponding author. Tel.: þ20 145051930; fax:

E-mail addresses: mahrous_ahmed2004@yahoo.calbishri@hotmail.com (A. Al Bishri), ahmharon@gmai

1 Tel.: þ966 50064067; fax: þ966 25664314.2 Tel.: þ966 0502561208; fax: þ966 25664314.

1010-5182/$ e see front matter � 2010 European Assdoi:10.1016/j.jcms.2010.10.016

a b s t r a c t

The aim: The aim of this work was to assess the multislice CT scan for analysis of the craniofacialanatomic changes in Pierre Robin sequence both predistraction and postdistraction, and to assess the useof unidirectional internal distractors in this patient group.Patients & methods: The study involved 11 patients. Their age at the time of distraction ranged from 2 to 7months. Six were females and 5 were males. All had retromicrognathia, glossoptosis and obstructivesleep apnoea. All were diagnosed clinically and by CT scan. All were managed by distraction osteogenesisand were followed postoperatively by multislice CT.Results: The distance between the base of the tongue and the posterior pharyngeal wall increased bya mean of 141%, and the total mandibular length increased by a mean of 26%. The increase in the distancebetween the hyoid bone and the posterior pharyngeal wall increased by a mean of 42% .The distancebetween the hyoid bone and the genoid process increased by a mean of 9%.Conclusion: Multislice CT scan was found to be a practical imaging technique to evaluate the morphologicchanges in the airway and the mandible after distraction osteogenesis. It rules out the need for othertraditionalmethods. Owing to the plasticity andmalleability of the infantmandible that allow for sufficientbone remodelling, unidirectional internal distractors achieved a satisfactory maxillomandibular relation-ship which was tolerated by the infants and accepted by the parents.

� 2010 European Association for Cranio-Maxillo-Facial Surgery.

1. Introduction

Pierre Robin (PR) is a sequence of events arising from the poordevelopment of the mandible. Micrognathia causes the tongue tobe displaced to the back of mouth (glossoptosis). Concomitantreduction of the oropharyngeal airway leads to upper airwayobstruction. The patients have symptoms of obstructive sleepapnoea (OSA) that in severe cases needs tracheostomy. The tonguemay interfere with the closure of the palate resulting in a horse

The work is attributed to theist Hospital, Makkah, Saudiamaxillofacial department isrk has been approved by theed consent to the work.

ere no sources in the form of

þ20 862342502/3.om (A. Mahrous Mohamed),l.com (A. Haroun Mohamed).

ociation for Cranio-Maxillo-Facial

shoe-shaped cleft palate (Cohen et al., 1998; Dauria and Marsh,2008; Marques et al., 1998).

The management of Pierre Robin sequence (PRS) variesaccording to the degree of severity of the individual case. Conser-vative management includes prone positioning and the placementof nasopharyngeal airway stents. Significant airway obstructionmandates more aggressive therapy, including tongueelip adhesionand hyomandibulopexy. Tracheostomy has been considered theconventional alternative for management of upper airwayobstruction in PRS; however, it is associated with a high cost interms of morbidity and mortality rates. The average age of dec-anulation for childrenwith PRS is 3.1 years (Denny and Kalantarian,2002; Mandell et al., 2004).

Distraction osteogenesis (DO) has become an accepted methodof treatment for patients with a hypoplastic mandible. It achievesmandibular lengthening without need for a bone graft. During therecent past, mandibular reconstruction by DO has been demon-strated to be effective in resolving upper airway obstruction and fortracheostomy decanulation. It has also been used in respiratorydistressed neonates and infants to avoid tracheostomy (Denny andKalantarian, 2002; Looby et al., 2009; Morovic and Monasterio,2000).

Surgery.

Fig. 1. Preoperative 3DCT showing the craniofacial skeleton of one patient withretromicrognathic mandible and maxillomandibular ridge disharmony.

Fig. 2. Preoperative sagittal CT showing glossoptosis and severe airway obliteration.

Fig. 3. Preoperative axial CT showing narrowing of the transverse and theanteroposterior dimensions of the airway.

Fig. 4. Preoperative 3DCT for the transverse dimensions of the airway. The arrowpoints to the site of narrowing.

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419 413

Traditional methods of mandibular distraction use multidirec-tional external distractors. These distractors allow multiplanarmanipulation of the mandibular segments and allow fine adjust-ment of the maxillomandibular relationship. New, unidirectionalinternal microdistractors allow placement of inconspicuousinternal devices with minimal morbidity. Infants tolerate theseinternal distractors more readily than the external distractors. Theinternal distractors also offer minimal risk of dislodgement andthey avoid the scars associated with the insertion of external dis-tractor pins through soft tissues. They do not allow fine adjustmentof mandibular segments to correct any occlusal disharmony thatoccurs during the distraction process which is a reported drawback(Roy et al., 2009).

Computed tomography (CT) and its 3-dimensional (3D) recon-structive imaging technique have been widely used in the diag-nosis, treatment planning, surgical guidance, evaluation of results,and follow-up studies of maxillofacial deformities. Helical CTscanning technique in combination with 3D rendering techniquesenables the use of high-quality 3DCT images. The helical CT scannerprovides adequate image data to create 3D images with reducedscanning time and radiation dose compared with the conventionalCT scans because of the continuous scanner rotation and Tabletopmovement (Cademartiri et al., 2004; Girod et al., 1995; Hoponiket al., 1983; Metes et al., 1993; Ono et al., 1992). The scan timehas been reduced significantly and the smallest details can bescanned within a predictable scan time (Springer and Heidelberg,2007).

Fig. 5. Preoperative 3DCT for the anteroposterior dimensions of the airway. The arrowpoints to the site of narrowing.

Fig. 6. Intraoperative view showing distractor application.

Fig. 7. Postoperative 3DCT showing the craniofacial skeleton of the same patient inFig. 1 with increase in the total mandibular length and normal maxillomandibularridge relationship.

Fig. 8. Postoperative sagittal CT showing improvement in the anteroposterior airwaydimensions and forward displacement of the hyoid bone.

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Because the informationwithin the CT image data involves bothhard and soft tissue structures, it is possible to design a three-dimensional computerized imaging technique to allow three-dimensional visualization of the pharyngeal airway and themandible (Calhoun et al., 1999; Kawamata et al., 2000).

A new innovative 3D cephalometric analysis has been recom-mended for making a precise diagnosis. It uses the set-up andvalidation of a voxel-based semi-automatic 3D cephalometricreference system. The 3DCT method is widely used and acceptablefor many reasons. Actual measurement can be obtained, and the 3D

image can be rotated easily by changing the rotational axis. Inaddition, 3DCT image can also show asymmetry of the midface andthe cranial base that is difficult to be detected in ordinary 2D X-rayfilm (Maeda et al., 2006; Netherway et al., 2006; Swennen et al.,2006). Olszewski et al. (2010), proposed a classification schemeand exclusion criteria for reference landmarks used in 3D cepha-lometrics, based on inter-observer reproducibility and anatomicalreality.

2. Patients & methods

Over the past 3 years, 27 patients having retromicrognathia,glossoptosis, obstructive sleep apnoea and cleft palate were

Fig. 9. Postoperative axial CT of the same patient in Fig. 3 showing improvement in thetransverse and the anteroposterior dimensions of the airway.

Fig. 10. Postoperative 3DCT showing widening of the transverse dimensions of theairway.

Fig. 12. 3DCT of the distracted mandible with the distractors in place at the end of theconsolidation period showing a good quality of deposited bone as shown by smoothintact regular cortices.

Fig. 11. Postoperative 3DCT showing widening of the anteroposterior dimensions ofthe airway.

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419 415

diagnosed as Pierre Robin sequence. These infants were managedby conservative measures including prone positioning, applicationof nasopharyngeal airway or tongue stitch. Most of these patients(16 patients) responded to these conservative measures, but 11patients did not respond well. They were subjected to DO. Six ofthem were females and 5 were males. Their age at initial presen-tation ranged from 3 days to 7 months age. All had retro-micrognathia, glossoptosis, cleft palate and symptoms of OSAS asnoisy breathing during sleep, fragmented sleep, pauses in respira-tion and daytime somnolence. All patients were unable to controltheir airway during feeding, as evidenced by repeated episodes ofchoking and obstruction. Birth weights ranged from 2.9 to 3.3 kg.Their age at the time of DO ranged from 2 to 7 months. Poly-somnographic sleep studies revealed that the respiratory distur-bance index ranged between 9 and 20 apnoeas per hour (mean 14),and oxygen saturation ranged between 75 and 85% (mean was81%).

Patients were assessed by multidetector CT scan in a low dosetechnique with the eye closed using a sedating dose of midazolam(0.01e0.1 mgm/kgm) under care of an anaesthiologist. The deviceused was 64 multidetector CT, GE(¼General Electric), CTV(¼CTvolume), ADW (¼Advantage workstation) 4.3 (Figs. 1e5).

The surgical procedure was performed under GA withnasotracheal intubation in 7 patients and by tracheostomy in the

remaining 4 patients because of severe upper airway obstruction.A submandibular incisionwas done bilaterally and the flap elevatedto the lower border of the mandible. Buccal and lingual corticoto-mies were done in the distal part of the mandibular body. Unidi-rectional internal microdistractors were used bilaterally (modifiedtrack plus alveolar distractor e KLS Martin, L.P., modified byremoving its distractor arms on one side). The distractor was fixedby screws anterior and posterior to the corticotomy. Completion ofthe corticotomy into osteotomy was then done. Activation of thedistractor in place was tried to assess the completeness of theosteotomy. The tissues were closed over the distractor. The dis-tractor arm was placed subcutaneously and its free end was leftuncovered to facilitate the distraction process (Fig. 6).

Distraction started 24 h after application of the distractor andactivated 1 mm daily (0.5 mm morning and 0.5 mm evening).Patients with severe OSAS were kept in the intensive care unit forseveral days for monitoring the postoperative airway and oxygen

Fig. 13. Intraoperative view at the time of distractor removal showing good quality ofbone as appears between the distractor arms.

Fig. 14. One year postdistraction 3DCT of the head and neck shows normal growth ofthe mandible with normal alveolar ridge relationship.

Fig. 15. Preoperative profile view of one of the patients with retromicrognathia andtracheostomy tube in place.

Fig. 16. Profile view of the same previous patient after distractor removal withimprovement of the micrognathia and inconspicuous scar.

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419416

saturation until the swelling reduced and the distractionwas nearlycompleted. After 10 weeks of consolidation period, the distractorswere removed under GA.

With respect to the airway, either uneventful decanulation ofthe tracheostomy, uneventful removal of the tongue stitch,uneventful removal of the nasopharyngeal airway or oxygen satu-ration above 95% was considered as success.

Follow up of the distraction process was done by CT scan in axial,sagittal planes and three-dimensional CT of the facial bones andupper airway (Figs. 7e12). The measurements were made on 2Dimages (of 3D models) and were cephalometrically calibrated. TheCT data from the in vivo scan were extracted and analysed for thefollowing:

1. Distance from the posterior pharyngeal wall to the tongue baseat the level of the C1 archmeasured in the axial andmidsagittalplanes. This represented the anteroposterior dimensions of theairway (Figs. 8 and 9).

2. Distance from the lateral pharyngeal wall on one side to that onthe other side at the level of the C1 arch measured in the axialplane. This represented the transverse dimensions of theairway (Figs. 3 and 9).

3. Mandibular ramus length as measured from a point on theposterior condyle (articulare: Ar) to the midpoint of themandibular angle (gonion: G) (Figs. 17 and 18).

4. Mandibular body length as measured from the gonion to themost protrusive point of the symphysis (pogonion: Pg) (Figs. 17and 18).

5. Total mandibular length which is the sum of both the length ofthe ramus and the body (Figs. 17 and 18).

6. The distance from the posterior pharyngeal wall to the hyoidbone and the distance from the hyoid to the genoid process.This represented the degree of forward displacement of thehyoid bone with distraction (Fig. 8).

7. The maxillomandibular alveolar ridge distances weremeasured by extending their long axis up and down. Thedistance between the maxillary and the mandibular axis wasmeasured at the occlusal plane. It ranged from 14 to 18 mm(mean 15 mm).

Fig. 17. Extracted 3DCT of the mandible showing its predistraction dimensions. Arpoints to the point articulare, G points to the gonion point and Pg points to thepogonion point.

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419 417

The follow-up period was from 12 to 24months after removal ofthe distractor.

Fig. 18. Extracted 3DCT of the mandible showing its postdistraction dimensions.

3. Results

Mandibular distraction was successful in all patients (Figs.15e18). The deposited bone was of good quality (Figs. 12 and 13).Bone quality was defined subjectively at the time of distractorremoval (intact smooth regular cortices), from the 2D CT and fromthe 3D CT. From 2D CT the bone density of the newly formed bonewas the same density of the adjacent bone. From 3D CT, the newlyformed bonewas homogenous with the adjacent bone. The averagelinear mandibular lengthening was 18 mm (range 15e23 mm). Onepatient had an incomplete osteotomy on one side. The distractionstopped on this side. He was diagnosed both clinically and radio-logically. The osteotomy was completed again and the distractioncontinued. One patient developed unilateral mild weakness of themarginal branch of the facial nerve which improved spontaneouslybefore removal of the distractor. The surgical scar was hidden in thesubmandibular region.

Polysomnographic sleep studies revealed that the respiratorydisturbance index ranged between 0 and 2 apnoeas per hour (mean1), and oxygen saturation ranged between 95 and 99% (mean 97%).

All patients with a tracheostomy were decanulated, patientswith tongue stitches had them removed and patients with naso-pharyngeal airways had them removed, all uneventfully. Symptomsof OSAS improved and weight gain was excellent. Clinical exami-nation showed good arch harmony without open bite or cross bitedeformity (Fig. 7).

There were signs of mild infection in 3 patients at the distractorsite. These were successfully managed with systemic antibioticsand dressings.

Analysis of the CT demonstrated the followings (Table 1):

1. The increase in the anteroposterior dimensions of the airwayranged from 81 to 248% with a mean of 141% (Figs. 8, 9, 11).

2. The increase in the transverse dimensions of the airway rangedfrom 1 to 8% with a mean of 4% (Figs. 9 and 10).

3. The ramus height increased between 15 and 20% with a meanof 18% (Figs. 7, 17 and 18).

4. The body length increased between 5 and 30% with a mean of22% (Figs. 7, 17 and 18).

5. The total mandibular length increased between 16 and 33%with a mean of 26%. The forward lengthening of the mandibleresulted in forward traction of the tongue and increasedhypopharyngeal airway space. A reciprocal relationship wasfound between the % of increase in the total mandibular lengthand the % of increase in the anteroposterior dimensions of theairway (Figs. 7, 17 and 18).

6. The increase in the distance between the hyoid bone and theposterior pharyngeal wall ranged from 33 to 56% with a meanof 42%. The distance between the hyoid bone and the genoidprocess increased between 8% and 12% with a mean of 9%(Fig. 8).

7. Maxillomandibular alveolar ridge distances were corrected toa mean of 2 mm after distraction.

After 6e12 months (Fig. 14), all patients had grown normally asevidenced clinically, were able to feed themselves and had nobreathing problems.

4. Discussion

The use of mandibular DO in alleviating upper airway obstruc-tion in infants with micrognathia is rapidly expanding. Series pre-sented by Denny et al. (2001); Denny and Kalantarian (2002);Sidman et al. (2001); Wittenborn et al. (2004), and Mandell et al.(2004), confirm the utility of this option. New internal deviceshave been shown to have significant advantages over the bulkyexternal devices. This was also shown by Lin et al. (2007), and byRoy et al. (2009). One purpose of this study was to determine ifunidirectional vector forces are sufficient to achieve a goodmaxillomandibular relationship. The study has shown that thishave been achieved clinically with no open bite or cross bitedeformities. Functional loading and bony remodelling in this youngage group are important in achieving this relationship.

Imaging evaluation of the morphological airway changes hasbeen performed in patients with OSAS. Imaging techniques includecephalometric radiography (Pépin et al., 1999), CT (Hoponik et al.,

Table 1Patient’s demographic data, average increase in airway dimensions, distance of the hyoid bone from the posterior pharyngeal wall and total mandibular length.

No Age at the time ofdistraction in months

Sex The % of increase in theanteroposterior dimensionsof the airway

The % of increase in thetransverse dimensionsof the airway

The % of increase in theanterior displacementof the hyoid

The % of increase in thetotal mandibular length

1 2 Male 81 1 33 162 5 Female 248 8 56 333 2 Male 128 5 42 264 2 Female 116 3 41 205 5.5 Male 138 4 41 306 5.5 Female 140 6 44 317 3 Female 135 4 38 288 7 Female 122 4 36 229 2 Male 126 2 43 2510 6 Female 124 1 43 2411 5 Male 198 6 45 32

Mean 4.5 141 4 42 26

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419418

1983; Pépin et al., 1999), and magnetic resonance imaging (Ryanet al., 1991). With conventional cephalometric radiography, it isdifficult to observe the pharyngeal airway 3-dimensionally. Infrontal cephalometric radiography, hard tissue structures such asthe anterior teeth and the pharyngeal airway overlap. With 3DCTimaging it is possible to visualize the pharyngeal airway3-dimensionally without obstruction by hard tissue structures(Iatrou et al., 2009).

CT scans create 3D images using ionizing radiation. According tothe alliance for radiation safety in paediatric imaging, a CT scan ofthe head exposes a child to the amount of radiation he shouldnaturally experience during approximately 8 months. Apart fromscientific reasons, it is better to avoid duplicating diagnostic CT. It ismandatory to discuss the benefits and risks with the parents(Zoetelief and Geleijns, 1998).

A study performed by Williams et al. (1999), demonstratedexpansion of the mandibular framework with advancement of thebase of the tongue, leading to increased pharyngeal airway for earlydecanulation of tracheostomy dependent patients. This is deter-mined on the basis of cephalometric study measuring theadvancement of hyoid bone along the axis of the mandibular bodyafter distraction.

Despite the great increase in the distance between the poste-rior pharyngeal wall and the hyoid bone (42%), the genioehyoidrelationship remained relatively constant after mandibulardistraction, with only a 9% increase. This relationship supports thenotion that the hyoid moves forward as the distal mandibularsegment is anteriorly distracted. This is in accordance with thatreported by Roy et al. (2009), who reported only a 14% increase inthe genioehyoid distance.

Roth et al. (1997) measured the advancement of the hyoid bonealong the axis of the mandibular body after distraction. An averageadvancement of 14.5 mmwas found. Any displacement of the hyoidbone away from the posterior pharyngeal wall was believed to aidin decreasing airway obstruction.

In their CT analysis after distraction osteogenesis in Pierre Robinsequence, Roy et al. (2009), showed that the total mandibularlength had been increased by 26%, and the posterior distance fromthe pharyngeal wall had been increased by 198.9%.

Three recent studies have examined both mandibular volumeand upper airway volume after DO of the mandible on the basis of3DCT calculations. The first study was done by Perlyn et al. (2002),who examined four patients (two with Nager syndrome and twowith Treacher Collins syndrome) who underwent mandibulardistraction. The mandibular volume and upper airway volumeincreased on postdistraction CT scan by an average of 27% and 37%,respectively. The second study was by Rachmiel et al. (2005), whostudied 12 patients who similarly underwent mandibular

distraction to correct airway obstruction. The mandibular volumeand upper airway volume increased on postdistraction CT scan byan average of 28% and 72%. Neither study, however, was performedon neonates (the youngest child in these studies was 12 monthsold). The third study was by Roy et al. (2009), who studied threeinfants with PRS and severe upper airway obstruction whounderwent DO. A 32.0% increase in mandibular bone volume waspresent after distraction osteogenesis compared with theremainder of the craniofacial skeleton. When mandibular bonevolume was compared with maxillary growth, they found a 39.1%increase in bone growth of the mandible after distraction osteo-genesis. The midsagittal airway area improved by 150.0%, and the3D airway volume increased by 192.0%.

Expansion of the width of the airway over part or the entireairway will be reflected in an increase of the internal volume of theairway, as this volume is the longitudinal integral of the cross-sectional area and consequently reflects a decrease in the flowresistance over the length of the airway (Perlyn et al., 2002).

We reviewed papers to relevant DO in themandible published inthe last 3 years. Kruse et al. (2008) utilized micro-CT to define bonequality and density. Wolvius et al. (2008) described a new custommade distractor fixed by wires for distraction of four PR patients.Schendel et al. (2008) described the use of an internal curvilineardistractor andevaluated theirwork clinically andbyCTscan afterDOof 16micrognathic infants. Rohit et al. (2008) stated thatmandibularDO is aviable option in the paediatric age groupwith intervention asearly as 8months of age. They utilized an intraoral ramus distractor.Iatrou et al. (2009) reported one case of severe PRS that wasdistracted extraorally bilaterally by an internal distractor due to lackof intraoral space. They followed the patient by anteroposteriorcephalogram and by 3DCT. Sadaka et al. (2009), utilized intraoraldistractors to relieve airway obstruction in seven patients. Their ageranged from 7 months to 8 years. They followed their patients byconventional radiography. Olszewski et al. (2010) measured thereproducibility of osseous landmarks identified from two recentlydescribed cephalometric analysis: 3D-ACRO and 3D-Swennenanalysis. Rania et al. (2010) showed that there is a wide variety intreatment approaches for craniofacial anomalies in Europe. There isdisagreement on the essential steps in the distraction process.

5. Conclusions

Multislice CT scanwas found to be a practical imaging techniqueto evaluate the morphologic changes in the airway and themandible after distraction osteogenesis. It rules out the need forother traditionalmethods.Owing totheplasticityandmalleabilityofthe infant mandible, that allow good bone remodelling, unidirec-tional internal distractors achieved satisfactory maxillomandibular

A. Mahrous Mohamed et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 412e419 419

relationship which was tolerated by the infants and accepted by theparents.

Conflict of interestThere was no conflict of interest.

Acknowledgments

The authors express their great appreciation to the staffmembers of the anaesthesia department, ENT department andPaediatric ICU in Al-Noor specialist hospital, Makkah who providedpure technical help and general support.

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