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Changes in bone blood ow in segmental LeFort I osteotomies

Winfried Bernhard Kretschmer, MD, DDS,a Grigore Baciut, MD, DDS, PhD,b Mihaela Baciut, MD, DDS, PhD,c Werner Zoder, MD, DDS,d and Konrad Wangerin, MD, DDS, PhD,e Stuttgart, Germany, and Cluj-Napoca, Romania
MARIENHOSPITAL AND UNIVERSITY OF MEDICINE AND PHARMACY IULIU HATIEGANU

Objective. The aim of the present study was to investigate the effect of segmentation and different movements of the segments in LeFort I osteotomies on the bone blood ow (BBF). Material and methods. The study sample of the prospective cohort study was composed of subjects scheduled to undergo 3-piece LeFort I osteotomies and simultaneous BSSO for correction of developmental skeletal deformities. The primary predictor variables were: time (T1, before LeFort I osteotomy; T2, after LeFort I osteotomy; T3, after segmentation and xation of the maxilla) and magnitude of maxillary movement in the sagittal, vertical, and transverse planes measured in millimeters (mm). The subjects were assigned to 2 risk groups (high/low) depending on the amount of the movement. The primary outcome variable was maxillary bone blood ow measured with a laser Doppler at 4 sites: premaxilla, right and left maxillary lateral segments, and the mandible. Results. No signicant difference was observed among the 3 maxillary regions. The mean decrease of the maxillary BBF between T1 and T2 as well as the reduction of BBF between T2 and T3 were statistically signicant for all regions (P .028 to P .005 for T1/T2; P .003 to P .028 for T2/T3). No signicant difference could be found between the 2 risk groups of maxillary movements. Conclusions. Multisegmental maxillary osteotomies lead to a signicant reduction of BBF. Moderate maxillary movements have no signicant inuence on the blood supply. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:178-183)

Multisegmental Le Fort I osteotomy is a standard procedure in orthognathic surgery. The reestablishment of a blood supply to the dento-osseous segments was shown by Bell et al.1,2 in animal studies on macaque monkeys. Yet, a signicant reduction in perfusion of the dento-osseous segments has been observed during the rst hours after surgery.1-7 Thus, adverse sequelae can occur, such as pulp changes, nonunion of the bone, and partial or complete loss of segments. Thirty-six cases of aseptic necroses were described by Lanigan and West.8 Expansion of the segmented maxilla and
a

Senior Registrar, Department of Oral and Maxillofacial Surgery, Marienhospital, Stuttgart, Germany; PhD Student, University of Medicine and Pharmacy Iuliu Hatieganu, Cluj-Napoca, Romania. b Professor and Chair, Clinic of Cranio-Maxillofacial Surgery, University of Medicine and Pharmacy Iuliu Hatieganu, Cluj-Napoca, Romania. c Associate Professor, Clinic of Cranio-Maxillofacial Surgery, University of Medicine and Pharmacy Iuliu Hatieganu, Cluj-Napoca, Romania. d Senior Registrar, Department of Oral and Maxillofacial Surgery, Marienhospital, Stuttgart, Germany. e Professor and Head of the Department, Department of Oral and Maxillofacial Surgery, Marienhospital, Stuttgart, Germany. Received for publication Feb 23, 2009; returned for revision Apr 4, 2009; accepted for publication Apr 16, 2009. 1079-2104/$ - see front matter 2009 Published by Mosby, Inc. doi:10.1016/j.tripleo.2009.04.029

superior repositioning seem to exhibit the highest risk for this kind of complication.8,9 Emshoff et al.10,11 have shown that segmentation leads to a reduction of pulpal blood ow (PBF) after LeFort I osteotomy. Expansion or specic movements of the maxilla were not quantied. So far, no study has been performed on the effect of expansion, advancement, or vertical repositioning on the bone blood ow in the dento-osseous segments. Laser Doppler owmetry has been described to be a reliable method for continuous measurement of pulpal or gingival blood ow in orthognathic surgery. Intraoperative recording of gingival blood ow (GBF) during Le Fort I osteotomies was done by Dodson et al.12-14 Studies on bone blood ow (BBF) with laser Doppler owmetry in orthognathic surgery are not known. The current study was designed to evaluate the effect of segmentation, intraoperative expansion, advancement, and vertical repositioning on BBF of premaxilla and lateral segments during multisegmental Le Fort I osteotomies. MATERIAL AND METHODS Study design and sample A prospective cohort study was designed to investigate the effect of segmentation and magnitude of maxillary movement in the sagittal, vertical and transverse planes on BBF of the maxilla. The study sample was composed of subjects scheduled to undergo 3-piece

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LeFort I osteotomies and simultaneous bilateral sagittal split osteotomy (BSSO) for correction of developmental skeletal deformities. Inclusion criteria were the following: xed orthodontic appliances, availability of a sterilized probe (the laser probes had to be sent outside the hospital for gamma sterilization), a sufcient bone thickness of the measurement areas, and a clinical postoperative follow-up of at least 6 weeks. Patients with previous surgery in the maxilla (e.g., cleft palate, rapid maxillary expansion) or general diseases (non class I according to the American Society of Anesthesiology) were excluded. The protocol was reviewed and approved by the institutional review board. Each subject has given a written informed consent. Study variables The predictor variables were time, direction, and magnitude of maxillary movement and location of blood ow measurement. BBF (outcome variable) was measured after incision of the upper and lower vestibule and soft tissue dissection (T1), after Le Fort I osteotomy and mobilization of the maxilla (T2) and after segmentation and xation of the maxilla (T3). Direction and magnitude of maxillary movement were planned with the Onyxceph software 2.7.15 (Image Instruments GmbH, Jena, Germany). The following landmarks were used for the study: upper incision (horizontal movement) and mesial cusp of the rst molar (vertical movement). The movements are given in relation to the Frankfurt horizontal plane. Widening of the maxillary dental arch was measured for the rst molar on the dental casts before and after model surgery. The subjects were assigned to 2 risk groups. Advancement, superior repositioning, and widening of 2 mm and more were considered a risk. The high-risk group included subjects with 2 or 3 movements at risk, whereas the low-risk group included subjects with only 1 or no movement at risk. The locations of BBF measurement were premaxilla, right and left lateral segment of the maxilla, and mandible (control measurement). Other collected variables included age and gender. Anesthesia and surgical technique All patients received hypotensive anesthesia. Standardized Le Fort I and sagittal split osteotomies with rigid xation were performed according to Bell and Proft15 and Hunsuck.16 Tissue perfusion was optimized by administration of 500 mL of hydroxyethyl starch 6%/200/0.5 before segmentation of the maxilla; this bolus infusion was repeated after 8 and 20 hours. Segmentation of the maxilla was done between the lateral incisor and the canine on both sides with appropriate burrs. The maxilla was operated on rst in all

Fig. 1. Probe holder xed into the maxillary bone (premaxilla and lateral segments) intraoperatively.

cases. The maxillary segments were stabilized with 2.0-mm miniplates and an interocclusal splint. Blood ow measurement A laser Doppler owmeter (Periux PF 5001, Perimed, Jrflla, Sweden) was used to assess the BBF in the maxilla and the mandible. Light with a wavelength of 632.8 nm is produced by a 1-mW He-Ne laser. Custom-made probe holders (Perimed) were xed in the premaxilla, both canine regions and the mandible (anterior to the planned sagittal split) through 1.9-mm burr holes in the cortical bone (Fig. 1). The measurement in the mandible served as a control. A custommade probe (PF 415-310, Perimed) (Fig. 2) was used to conduct the light to the measurement site in the cancellous bone and to return the backscattered light to the owmeter. The probe had a diameter of 1 mm. The optical ber had a diameter of 125 m; the ber-tober distance was 500 m. According to the Doppler effect, the amount of backscattered light is recorded by the owmeter. The voltage of the produced output signal has a linear relation to the ow of the red blood cells (number of cells average velocity). The perfusion units (PU) shown by the laser Doppler are a relative measurement of the blood ow in the respective tissue. The data were collected on a wide band setting. A computer was connected to the RS-232 port of the laser Doppler for storage of the date and later analysis with the specic software (PeriSoft for Windows, Perimed). Reproducibility of the measurements was ensured with the xed probeholder. Calibration of the probes was done before each sterilization process with a plastic block for zero voltage and a motility standard for 250 PU (Perimed). For each site the data were registered continuously until at least 2 minutes of stable values were seen on the screen.

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Table I. Study variables (n 12; 7 male, 5 female)


Variable Age Maxillary advancement, mm Vertical movement rst molar, mm Expansion rst molars, mm Mean 22.5 1.6 2.4 1.5 SD 4.25 1.16 3.02 1.90 Range 16 to 31 0 to 3 7 to 2 1 to 4.5

Table II. Risk groups for decrease of bone blood ow in segmental LeFort I osteotomies: high (n 7) and low (n 5)
Patient Advancement Vertical movement Expansion Risk group 1 2 3 4 5 6 7 8 9 10 11 12 2 3 1 1 1 3 0 1 3 0 3 1 2.5 7 1 2 1 4 4 6 1 2 3 5 4 0 3 1 0 3 2 0 3 0 0 4.5 High High Low Low Low High High Low High Low High High

Fig. 2. Laser Doppler probe (PF 415-310, Perimed, Jrflla, Sweden) for measurement of bone blood ow (BBF).

Advancement, superior repositioning, and expansion of 2 mm or more were considered a risk. Subjects with 2 or 3 movements at risk were assigned to the high-risk group.

Data analysis For the analysis of the recordings, the PeriSoft for Windows software was used. The mean perfusion was calculated for each session during the phase of stable values. Peaks attributable to movement artefacts were excluded. Further data analysis was done with the Statistica 8.0 software (StatSoft Inc., Tulsa, OK). Perfusion changes of the mandible, the premaxilla, and the lateral segments between the respective sessions were investigated with the Wilcoxon matched pairs test. The Friedman analysis of variance (ANOVA) was used to detect differences among the 3 maxillary regions within every session. To compare the results with those of other studies, the percentage of BBF reduction was calculated for the 3 maxillary regions. Differences between the 2 risk groups at T2 and T3 were analyzed with the KruskalWallis ANOVA by ranks. A probability of P less than .05 was considered signicant. RESULTS Twelve patients undergoing bimaxillary osteotomies with 3-piece maxilla from April 2008 to February 2009 were included in the study. Two patients were excluded from the study, because maxillary blood ow measurement was not possible in the lateral segments because of extremely thin bone. Mean, standard deviation, and range of the study variables are given in Table I. Seven

patients were included in the high-risk group, whereas 5 patients were assigned to the low-risk group (Table II). No anesthetic or surgical complications were observed during surgery. The descending palatine artery was preserved in all cases. Means, standard deviations, and ranges of all measurement sites and time points are shown in Table III. The mandibular perfusion showed no signicant differences between the recording sessions T1/T2 (P .071) and T2/T3 (P .875). No signicant differences could be found between premaxilla, right and left lateral segment at T1 (P .338), T2 (P .920), and T3 (P .368). A signicant reduction of BBF was observed between T1 to T2 in the right lateral segment (P .028), the premaxilla (P .028), and the left lateral segment (P .005). Between T2 and T3 a further signicant decrease of perfusion was seen in the right lateral segment (P .028), the premaxilla (P .003), and the left lateral segment (P .008) (Table III). The mean percentage of BBF reduction at the end of the maxillary procedure (T1/T3) was 63.3% (SD 18.54) in the premaxilla, 45.5% (SD 44.27) in the right lateral segment, and 60.7% (SD 18.63) in the left lateral segment. No signicant differences could be

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Table III. Regional bone blood ow measurements (n 12) in perfusion units (PU)
T1 Region Mandible Maxilla: Right lateral segment Left lateral segment Premaxilla Mean (SD) 59.7 (44.8) 77.5 (63.4) 79.6 (30.6) 70.6 (31.9) Range 12.9-151.6 12.7-210.3 19.5-112.3 24.8-121.8 Mean (SD) 40.5 (30.2) 46.8 (40.0) 41.1 (20.5) 47.5 (35.1) T2 Range 9.1-99.6 5.1-139.2* 13.8-75.5* 13.0-105.1* Mean (SD) 44.4 (34.6) 34.7 (41.8) 30.5 (19.4) 22.8 (15.4) T3 Range 7.9-115.6 1.4-145.9* 4.1-67.0* 3.5-52.8*

T1, before LeFort I osteotomy; T2, after LeFort I osteotomy; T3, after segmentation and xation of the maxilla. *Signicant difference to the previous session (P .05) in the Wilcoxon matched pairs test.

Table IV. Comparison of the maxillary bone blood ow between the high-risk group (n 7) and the low-risk group (n 5) at T2 and T3 (P values)
Region Right lateral segment Left lateral segment Premaxilla T2 0.685 0.570 0.223 T3 0.935 0.935 0.168

Kruskal-Wallis analysis of variance by ranks. T2, after LeFort I osteotomy; T3, after segmentation and xation of the maxilla.

found between the 2 risk groups at T2 and T3 (Table IV). Postoperatively, no avascular sequelae were seen. DISCUSSION Avascular necrosis is a possible sequelae of a compromised blood supply to the dento-osseous segments in multisegmental Le Fort I osteotomies.8,9 Lanigan and West8 reported 36 cases with aseptic necrosis following maxillary osteotomies. Of these 36 cases, 34 were multisegmental osteotomies. Basic research on the BBF after different osteotomies of the maxilla was done by Bell et al.,1,2 Nelson et al.,3 and Meyer and Cavanaugh4 on macaque monkeys. As it is not possible to use radioactive microspheres for clinical research in humans, laser Doppler owmetry has shown to be the method of choice for blood ow measurements in orthognathic surgery.5,10-14,17-24 The work of Firestone et al.,17 Buckley et al.,18 and Hellem et al.25 conrmed its reproducibility. Emshoff et al.10,11 have shown the decrease of pulpal blood ow 3 to 5 days after segmental maxillary osteotomies. Although it is known that the highest reduction of maxillary perfusion can be found during the rst hours after Le Fort I osteotomy,1-7 few data have been published about the intraoperative dynamics of maxillary blood ow.12-14 Superior repositioning and transverse expansion seem to be a potential risk for vascular impairment.8,9 So far, no research has been reported on the correlation between different max-

illary movements and the drop of maxillary blood supply in multisegmental osteotomies. To investigate the effects of orthognathic surgery on maxillary blood supply, research has mainly been done with laser Doppler assessment of pulpal (PBF) and gingival blood ow (GBF).5,10-14,17,18,22-24 This has some disadvantages: orthodontic treatment has shown to have an effect on PBF5,17 as well as the distance of the subapical osteotomy to the apex.24,26 Injuries of the teeth during surgery will certainly have an inuence on PBF. Furthermore, positioning of the probes with custom-made wafers, as done by most authors,10,11,19-23 is difcult intraoperatively, especially in cases with segmentation of the maxilla. Measurement of BBF with laser Doppler owmetry has been developed for the control of free aps.27-29 Animal studies have shown the reliability of this method.25,27,30-32 The intraoperative decrease of maxillary perfusion found in the present study was up to 95% in certain areas of the maxilla. This is comparable to the animal study of Nelson et al.3 with radioactive microspheres. They found a decrease of BBF up to 89% when the descending palatine artery (DPA) was cut. The DPA was not, however, severed in any case of the present study. The role of the DPA is not clear. Dodson and Bays12 did not nd a signicant difference between 2 groups with and without ligation of the DPA when measuring gingival blood ow intraoperatively. In contrast to this, Ramsay et al.23 reported 2 mild avascular complications in a sample of 14 patients. Both underwent a 2-piece Le Fort I osteotomy with expansion and had 1 descending palatine artery transected. They have not found signicantly lower perfusion values in these cases measuring 1 to 6 days after surgery. This conrms the importance of intraoperative assessment as proclaimed by Dodson et al.12-14 It is not clear when to classify a decrease of perfusion as adverse outcome. In a recent study, Emshoff et al.10 dened a reduction of PBF of more than 40% as adverse; 64% of their subjects with multisegmental maxillary osteotomy and 32% of those with single-piece Le Fort I osteotomy showed an adverse outcome 3 to 5 days after surgery.

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4. Meyer MW, Cavanaugh GD. Blood ow changes after orthognathic surgery: maxillary and mandibular subapical osteotomy. J Oral Surg 1976;34:495-501. 5. Geylikman YB, Artun J, Leroux BG, Bloomquist D, Baab D, Ramsay DS. Effects of Le Fort I osteotomy on human gingival and pulpal circulation. Int J Oral Maxillofac Surg 1995;24: 255-60. 6. Qeujada JG, Kawamura H, Finn RA, Bell WH. Wound healing associated with segmental total maxillary osteotomy. J Oral Maxillofac Surg 1986;44:366-77. 7. Sugg GR, Fonseca RJ, Leeb IJ, Howell RM. Early pulp changes after anterior maxillary osteotomy. J Oral Surg 1981;39:14-20. 8. Lanigan DT, West RA. Aseptic necrosis following maxillary osteotomies: report of 36 cases. J Oral Maxillofac Surg 1990;48:296-300. 9. Epker BN. Vascular considerations in orthognathic surgery: 2. Maxillary osteotomies. Oral Surg Oral Med Oral Pathol 1984; 57:467-72. 10. Emshoff R, Kranewitter R, Brunold S, Laimer K, Norer B. Characteristics of pulpal blood ow levels associated with nonsegmented and segmented Le Fort I osteotomy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:379-84. 11. Emshoff R, Kranewitter R, Gerhard S, Norer B, Hell B. Effect of segmental Le Fort I osteotomy on maxillary tooth-type related pulpal blood ow characteristics. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:749-52. 12. Dodson TB, Bays RA. Maxillary perfusion during Le Fort I osteotomy afterligation of the descending palatine artery. J Oral Maxillofac Surg 1997;55:51-5. 13. Dodson TB, Bays RA, Paul RE, Neuenschwander MC. The effect of local anesthesia with vasoconstrictor on gingival blood ow during Le Fort I osteotomy. J Oral Maxillofac Surg 1996;54:810-4. 14. Dodson TB, Neuenschwander MC, Bays RA. Intraoperative assessment of maxillary perfusion during Le Fort I osteotomy. J Oral Maxillofac Surg 1994;52:827-31. 15. Bell WH, Proft WB. Maxillary excess. In: Bell WH, Proft WR, White RP, editors. Surgical correction of dentofacial deformities. Philadelphia: Saunders; 1980. p. 234-442. 16. Hunsuck EE. A modied intraoral sagittal splitting technique for correction of mandibular prognathism. J Oral Surg 1968;26: 250-3. 17. Firestone AR, Wheatley AM, Ther UW. Measurement of blood perfusion in the dental pulp with laser Doppler owmetry. Int J Microcirc 1997;17:298-304. 18. Buckley JG, Jones ML, Hill M, Sugar AW. An evaluation of the changes in maxillary blood ow associated with orthognathic surgery. Br J Orthod 1991;26:39-45. 19. Harada K, Sato M, Omura K. Blood-ow and neurosensory changes in the maxillary dental pulp after differing Le Fort I osteotomies. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;97:12-7. 20. Harada K, Sato M, Omura K. Blood-ow change and recovery of sensibility in the maxillary dental pulp during and after maxillary distraction: a pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;98:528-32. 21. Sato M, Harada K, Okada Y, Omura K. Blood-ow change and recovery of sensibility in the maxillary dental pulp after a singlesegment LeFort I osteotomy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;95:660-4. 22. Justus T, Chang BL, Bloomquist D, Ramsey DS. Human gingival and pulpal blood ow during healing after Le Fort I osteotomy. J Oral Maxillofac Surg 2001;59:2-7.

Information about clinically observed avascular sequelae was not given. We observed a mean intraoperative BBF reduction in the maxillary regions between 45.5% and 63.3% after segmentation and xation. Avascular complications were not seen. Dodson and Bays,12 Harada et al.,19,20 and Sato et al.21 reported similar results. The drop of GBF after downfracture was greater than 70% in both study groups (with and without DPA ligation) of Dodson and Bays.12 For both groups, a reduction of over 60% was found at the end of the procedure. PBF decreased by more than 80% 1 day after surgery in the studies of Harada et al.19,20 and Sato et al.21 None of these authors reported avascular sequelae. Segmentation of the maxilla with superior repositioning and expansion is reported to be one of the main factors for avasular necrosis.8,9 Epker9 mentioned a risk of avulsing portions of the palatal pedicle, when expanding the maxilla more than 3 to 5 mm. Lanigan and West8 reported maxillary widening up to 15 mm in one study about 36 cases exhibiting aseptic necrosis. In a study of Poswillo33 on Old World monkeys with open bite, 10-mm advancement of the premaxilla led to irreversible pulp changes. Animal studies with not more than 2 mm repositioning of the segments have not shown permanent effects.1,2,6,24,25,34 No data can be found concerning the correlation between vertical maxillary movement and decrease of blood supply. Advancement, vertical repositioning, and expansion of the maxilla did not have a signicant inuence on BBF in the present study. The moderate maxillary movements and the relatively small sample might be reasons for these ndings. As the supposed limit of expansion should not be exceeded in humans for ethical reasons, further animal studies are needed. Intraoperative measurement of BBF should be continued to investigate the effect of vertical repositioning, widening, and advancement with larger samples. Thus, regression analysis for single factors will be possible. Monitoring of critical dento-osseous segments, e.g., in patients with cleft palate and previous surgery, is a possible indication for routine clinical application of the technique.
We thank Dr. Sorana-Daniela Bolboaca, M.S., M.D., Ph.D., Department of Biometry, University of Cluj-Napoca, for help with the statistical analysis. REFERENCES
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23. Ramsay DS, Artun J, Bloomquist D. Orthognathic surgery and pulpal blood ow: a pilot study using Laser Doppler owmetry. J Oral Maxillofac Surg 1991;49:564-70. 24. Yoshida S, Kazuhiko O, Kazuo T. Biological responses of the pulp to single-tooth dento-osseous osteotomy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:152-60. 25. Hellem S, Jacobsson LS, Nilsson GE, Lewis DH. Measurement of microvascular blood ow in cancellous bone using laser Doppler owmetry and 133Xe-clearance. Int J Oral Surg 1983;12:165-77. 26. Zisser G, Gattinger B. Histological investigations of pulpal changes following maxillary and mandibular alveolar osteotomies in the dog. J Oral Maxillofac Surg 1982;40:332-9. 27. Schuurman AH, Bos KE. Laser Doppler bone probe: an experimental study in dogs. Microsurgery 1991;12:246-51. 28. Schuurman AH, Bos KE, Van Nus YH. Laser Doppler bone probe in vascularized bula transfers: a preliminary report. Microsurgery 1987;8:186-9. 29. Yuen JC, Feng Z. Monitoring free aps using the laser Doppler owmeter: ve-year experience. Plast Reconstr Surg 2000;105: 55-61. 30. Swiontkowski MF, Schlehr F, Collins JC, Sanders R, Pou A. Comparison of two laser Doppler owmetry systems for bone blood ow analysis. Calcif Tissue Int 1988;43:103-7.

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31. Swiontkowski MF, Collins JC, Schlehr A, Pou A, Sanders R. Correlation of Laser Doppler owmetry with microsphere estimates for bone blood ow. Microcirculation-an update 1987;1: 341-3. 32. Swiontkowski MF, Tepic S, Perren SM, Moor R, Ganz R, Rahn BA. Laser Doppler ow measurement: correlation with microsphere estimates and evaluation of the effect of intracapsular pressure on femoral head blood ow. J Orthop Res 1986;4: 362-71. 33. Poswillo DE. Early pulp changes following reduction of open bite by segmental surgery. Int J Oral Surg 1972;1:87-97. 34. Ware WH, Ashamalla M. Pulpal response following anterior maxillary osteotomies. Am J Orthod 1971;60:156-64.

Reprint requests: Winfried Bernhard Kretschmer, MD, DDS Department of Oral and Maxillofacial Surgery Marienhospital Stuttgart Boeheimstr. 37 70199 Stuttgart, Germany winfriedkretschmer@vinzenz.de

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