Available online at www.sciencedirect.com
British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349
Morphometric study of the scapular free flap and the free rib osteomyocutaneous flap Tolga Taha Sönmez a,b,∗ , Andreas Prescher b , Anastasios Kanatas c , Arash Zaker Shahrak a , Marcus Gerressen a,d , Matthias Knobe e , Selman Hakki Altuntas f , Ali Modabber a , Timm Walter Steiner a , Ralf Smeets g , Alireza Ghassemi a , Frank Hölzle a a
Department of Oral and Maxillofacial Surgery, Medical Faculty, RWTH Aachen University, Aachen, Germany Institute of Molecular and Cellular Anatomy, Prosection, Medical Faculty, RWTH Aachen University, Aachen, Germany c Department of Oral and Maxillofacial Surgery, Leeds Teaching Hospitals and St James Institute of Oncology, Leeds Dental Institute, Leeds, United Kingdom d Department of Oral and Maxillofacial Surgery, Heinrich-Braun-Hospital, Location Zwickau, Zwickau, Germany e Department of Orthopedic and Trauma Surgery, Medical Faculty, RWTH Aachen University, Aachen, Germany f Department of Plastic Reconstructive and Aesthetic Surgery, Medical Faculty, Süleyman Demirel University School of Medicine, Isparta, Turkey g Department of Oral and Maxillofacial Surgery, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany b
Accepted 6 January 2014 Available online 28 January 2014
Abstract The scapula free flap is often the first choice for reconstruction of bony defects of the facial skeleton. However, the vascularised rib as part of a free rib osteomyocutaneous flap may be a suitable second choice. We have investigated the morphology and clinical dimensions of the 7th rib and the scapula, and the ability of the available bone to carry dental implants. The age and sex of the cadaver, and the donor side, were also recorded. The dimensions of the scapulas and 7th ribs (n = 130 of each) from 65 cadavers were measured at 4 different points using osteometric methods. Examination showed that bone from the scapula and 7th rib were sufficient for placement of implants. The 7th rib gave reliable measurements for both height and width, and a consistent relation between compact and cancellous bone. Although the scapula provided adequate compact and cancellous bone, there were variations depending on the segment of bone chosen. Bones from male cadavers were more suitable for implantation. In both the scapula and the 7th rib ageing had a significant adverse effect in only one dimension. Most points of measurement have satisfactory bony dimensions for insertion of dental implants. © 2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Keywords: Scapula; Rib; Oral and maxillofacial implant-carrying bone reconstruction; Morphometric and morphological bone measurements
Introduction Defects in the bone of the facial skeleton can be reconstructed successfully using free vascularised autogenous bony flaps.1,2 Anatomical reconstruction with adequate bone
∗ Corresponding author at: Department of Oral and Maxillofacial Surgery, Medical Faculty, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany. Tel.: +49 241 8035966; fax: +49 241 8082430. E-mail addresses: [email protected], [email protected], [email protected] (T.T. Sönmez).
for the insertion of dental implants is essential for optimal functional and aesthetic outcomes, with restoration of speech and chewing.2,3 The free vascularised rib flap is rarely used in clinical practice. The free rib osteomyocutaneous flap was first used in the head and neck by Serafin et al.,4 and their results were later confirmed by other studies.5–7 The latissimus-serratus-rib free flap has also been used successfully as a second choice of free flap.8,9 Since the early 1980s the osteocutaneous scapular flap has been the free flap of choice for reconstructions of combined bone and soft-tissue defects because it can
0266-4356/$ – see front matter © 2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.bjoms.2014.01.005
T.T. Sönmez et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349
provide bone, muscle, and skin paddles in 3-dimensional configurations.10,11 An important objective of oral rehabilitation after bony reconstruction is a stable, implant-supported, prosthesis.12 Satisfactory osseointegration of an implant requires a width of bone sufficient to incorporate the length of the dental implant in the viable bony flap.12–14 However, there is no reported universally adopted guidance on the optimal anthropometric properties of the rib and the scapula.15,16 Methods for measuring implantable bone segments are also not adequately detailed in cadaveric studies for the microsurgical era.10,17,18 The clinical applicability of free vascularised rib flaps has been assessed in a few anatomical studies in which the authors have tried to work out the optimal characteristics of these bony flaps and their ability to provide a stable base for dental implants.19–23 However, we know of only one study that has compared the dimensions and biomechanical properties of the rib with those of other donor sites.22 Most other studies have been small, and the comparisons reported were not paired from the same cadavers, which is important for morphometric studies. In addition, the impacts of age, sex, and donor side were not adequately investigated. We aimed to study the bony morphology of scapular and free rib osteomyocutaneous flaps and their implantable bony dimensions to find out whether they fulfil the minimum requirements for osseointegration of dental implants. We also assessed the impact of age, sex, and donor side on these flaps.
345
Fig. 1. Reference marks for measurements. Sites of chosen measurement points in the scapula (left, dorsal view) and rib (right, inferior view). X = the costal tubercle.
of the rib was marked as measurement point 1. The distance from the upper margin to the lower margin in a straight line was defined as the height, and the distance from the outer to the inner surface in a straight line was defined as the width, as described by Martin and Saller (Figs. 1 and 2).16 The morphology of the bone was macroscopically assessed and documented at both donor sites (Fig. 2). Then, to evaluate the overall ability of the scapula and rib to withstand placement of dental implants, all measurements above our cut-off values that were 5.5 mm or wider and 10 mm or
Materials and methods We obtained samples of bone from central European adult cadavers (n = 65) at the Institute of Anatomy, RWTH (Rheinisch-Westfälische Technische Hochschule) University, Aachen. A total of 130 samples of 7th rib and 130 samples of scapula were taken bilaterally from 37 (57%) female and 28 (43%) male cadavers. Specimens ranged in age from 50 to 95 (mean 78) years. We used 4 measurement points on each bone sample to make 520 measurements of the width and height of the scapula and 520 of the width and height of the rib (Fig. 1). On the lateral border of the scapula, measurement point 4 was marked 2 cm inferior to the infraglenoid tuberculum and measurement point 1 was marked 2 cm superior to the inferior angle (Fig. 1). We defined height as the distance in a straight line from the lateral margin of the lateral border to the transitional zone of a thin, transparent, bony lamella of the infraspinal fossa (transverse diameter). The transitional zone was defined for each measurement point on each scapula. The width at each point was defined as the distance in a straight line, perpendicular to the height (Fig. 2). We used the pair of 7th ribs for our measurements. On each rib we marked the costal tubercle (X on Fig. 1), and at a point 8 cm lateral to the costal tubercle we then marked measurement point 4. A point 8 cm ventral to this point on the body
Fig. 2. The lateral border of the scapula (left) and the rib (right) from both sites of the same cadaver. Bones are shown in cross-sections with the side of origin. The figure integrates measurement points, sides, and surfaces. Morphology of the bone and the relation between compact and cancellous bone is seen in cross-sections of measurement points (MPs) 1–4/bony segment.
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Table 1 Mean (SD) and range of height and width (mm) of scapulas (n = 65) and ribs (n = 65). Two scapulas and 2 ribs were harvested from each cadaver. Each bone had 4 measuring points (n = 520). Measurement Scapula Width Height Rib Width Height
Mean (SD)
Range
10.9 (3.8) 12.3 (4.9)
4.4–22.4 4.6–28.7
6.7 (1.3) 13.2 (1.7)
4.3–12.1 8.5–18.8
Table 2 Overall ability by sex to withstand placement of a dental implant at each measurement point on the lateral borders of scapulas and 7th ribs, which had to be 5.5 mm or more wide and 10 mm or more high. Data are expressed as percentages. Measurement point
Point 1 Male Female Point 2 Male Female Point 3 Male Female Point 4 Male Female
Scapula 5.5 mm or more wide and 10 mm or more high
Rib 5.5 mm or more wide and 10 mm or more high
100 95.9
99.2 91.9
99.6 93.9
98.7 90.8
84.4 77.1
92.9 84.1
84.4 76.4
91.6 84.8
higher were taken for each measurement point and compared for both sexes (Tables 1 and 2, Fig. 4), as considered to be acceptable for successful osseointegration of an implant.12–14 Any measurement point with both height and width above the cut-off values was implantable (Table 2). Our statistical analyses were made with the help of SPSS for Windows (Version 15.0, SPSS Inc, Chicago, IL). We used the one-sample Kolmogorov Smirnov test for normality. Parametric or non-parametric tests were selected according to the distribution of variables. Student’s t test or the Mann–Whitney U test were used to compare variables between 2 groups. Descriptive statistics for continuous variables were reported as mean (SD) or median (range), and frequency and percentages were reported for categorical variables. Pearson’s correlation coefficient was calculated to assess the relations between variables. Probabilities of less than 0.05 were accepted as significant.
Results The mean (SD) height and width of both the scapula and the rib satisfied the dimensional requirements for successful osseointegration of implants (5.5 mm or more wide and 10 mm or more high) (Fig. 3, Tables 1 and 2).12–14 The mean values for height at both donor sites were clearly above the
Fig. 3. Diagram showing the mean width and height (mm) at 4 measurement points on the scapula and rib in men and women.
necessary value for length, with the mean height of the rib being slightly greater. The mean values for the width of the scapula were greater than those for the rib and were above the necessary value for width for both donor sites (Fig. 3). These bony dimensions and the relation of compact to cancellous bone are apparent in cross-section (Fig. 2). The morphology of ribs tended to be more consistent across bony segments from measuring points 1–4 (Fig. 2). The height:width proportion of each bony segment changed minimally from ventral to dorsal, with a relative increase in width. However, the morphology of the lateral border of the scapula showed characteristic propagation towards the infraglenoid tubercle with a decrease in height (Fig. 2). At the dorsal end, an inverse morphological structure emerged so that this bone became both narrower and taller. The difference between the range of values of both dimensions is therefore greater in the scapula than in the rib (Table 1). The minimum values of both dimensions of the rib were slightly lower than the acceptable values for placement of an implant. Measuring points 1 and 2 in male scapulas gave adequate bone for implants in all cases (Table 2), whereas at points 3 and 4 the dimensions of the scapula were not implantable in just 84.4% of male scapulas. In male ribs, implants could have been placed in between 91.6% and 99.2%. The bony morphology of the rib was relatively constant over the entire length from measuring points 1–4. There were significant sex differences in the width of ribs (female ribs 88.99, p < 0.0001), height of ribs (female ribs 14.94, p = 0.0002), width of scapula (female scapula 85.92, p < 0.0001) and height of scapula (female scapula 48.25, p < 0.0001), with male bones being larger. The relations between sex and the measured dimensions of scapulas and ribs are shown in Fig. 3.
T.T. Sönmez et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349
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Fig. 4. Diagrams showing the relations between age (years) and height of the scapula (r = −0.26) (left) and age (years) and width of the rib (r = −0.32) (right).
Our results also showed that age negatively correlated both with width of rib (r = −0.32, 95% CI −0.527 to −0.088) and height of scapula (r = −0.26, 95% CI −0.474 to −0.018) (Fig. 4). We found no significant differences between the donor sides.
Discussion This study is to our knowledge one of the largest cadaver series ever conducted.18–23 The scapula, the iliac crest, and the fibula have each been rated highly for use in mandibular reconstruction.19 In other osteometric studies, the scapula has been considered equivalent to the iliac crest as a donor site, and in some aspects it may even be superior for placement of implants.21 In the present study we explored the dimensions of implantable bone of the 7th rib and the lateral border of the scapula for suitability during dental implantation (Table 2). We also considered the paired harvesting of bones from the same cadaver, which allowed statistical comparison of differences in the side from which the bone was taken. We found that the morphology of the lateral border of the scapula was such that it rotated around its own axis in a half spiral. Consequently, as one moved towards the infraglenoid portion of the lateral border, the height of harvestable bone decreased while the width increased (Figs. 1 and 2, Table 1). For this reason the anthropometric measurements do not reflect the clinically relevant bony dimensions of the lateral border, and a specific measuring technique is required.15,16 The anthropometric measurements for measuring the height and width of the rib have previously been reported to be clinically acceptable.16 A minimal vertical height of 10 mm with 1 mm of transversal bone around the implant is typically considered acceptable for successful osseointegration of implants.12–14 According to previous publications, an implant 3.5 mm in diameter requires a segment of bone with an overall minimum width
of 5.5 mm.19–23 The rib was not as wide as the scapula, but the mean values remained above 5.5 mm (Fig. 2 and Table 1), suggesting that it was nevertheless suitable. The rib offers advantages beyond consideration of width as it is higher, it has a constant ratio of compact:cancellous bone, and bony morphology is relatively constant (Figs. 1 and 2). The thick, compact bony structure improves the primary stability of an implant while the cancellous part facilitates better osseointegration.13,14 The scapula contains rich cancellous bone towards the inferior angle, while the compact bone widens in the lateral part as the cancellous area narrows (Fig. 2). In comparison, the harvestable region of bone in the 7th rib has an almost constant compact:cancellous bony relation across segments. The descriptive statistics of both donor sites showed that the mean height and width of bone was adequate (Table 1). However, some bony segments of the scapula fell below the required width and height that are acceptable for safe placement of implants. This is an important consideration for anyone contemplating the use of scapula as an implantcarrying bone flap. On the one hand the high maximum values alone would justify this use, but on the other, not all measured bony areas were adequate. In male bones the overall suitability for placement of implants was 84.4% at measuring points 3 and 4, and almost complete at points 1 and 2 (Table 2), so shorter and wider implants can be inserted in the lateral half of the harvested bone. The dorsal part (including the inferior angle to the harvested bone) better satisfies the requirements for safe placement of dental implants (Fig. 2). Alternatively, as one clinical study suggested, greater bony dimensions could be achieved by integrating the medial and the lateral border of the same microvascular flap.11 This may be an alternative to double-barrelled fibular flaps. To our knowledge this is the first study to show clearly such contrasting morphometric information about these 2 dimensions over several measurement points. Such information is likely to have been missed because in previous research fewer measurement points were used, and the
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predefined margins of the height of scapular bone were set to a predefined width.18–23 In comparison we individually measured the height of each scapula. For example Shimizu et al.23 calculated heights of 19–28 mm for the lateral border of the scapula and widths of 9–12 mm, using 3 measurement points. Another pilot study24 used a different measuring guide, and reported heights in the range of 13.2–19.5 mm and widths of 7.5–9 mm. Beckers et al.19 found the mean width to be 9.7 mm, which allowed an effective height for insertion of an implant of 13.2 mm. Unlike the scapula, the rib has a minimum height of 8.5 mm (with sufficient width), which is perfectly acceptable for implantation using currently available implant systems (Tables 1 and 2). Seikaly et al.22 reported that 89% (n = 22) of ribs satisfied the requirements (10 mm × 5.75 mm in this study) for safe placement of implants. As our study assessed the overall ability to withstand placement of a dental implant separately at each measuring point, we have been able to make precise statements for each bony region (Table 2). We therefore found, in contrast to their results, that the overall ability of the 7th rib to withstand placement of an implant ranged from 91.6% to 99.2% in male subjects. The bony morphology of the 7th rib can therefore be characterised as relatively constant for the placement of implants across all 4 measuring points (Fig. 2). This is the major advantage of using the 7th rib. It has consistent morphological dimensions along the whole length of the available bone with no need to compromise any osteotomies to rotate each bony segment. The impacts of age, sex, and side are extremely important in clinical practice. Despite their importance, these factors have rarely been investigated in previous morphometric studies.18–21 As expected, our statistical evaluation showed that there were significant differences between the sexes across all dimensions of both scapula and rib, with men’s bones being larger (Fig. 3, Tables 1 and 2). It is interesting that the adverse impact of ageing on the values measured at both donor sites was statistically confirmed in only one dimension for each bone, with the width of the rib and the height of the scapula diminishing with increasing age (Fig. 4). This finding may allow the placement of suitable dental implants in these bones, even though the patients are old.
Conflict of interest The authors have no financial interest to declare in relation to the content of this article.
Ethics statement The use of human cadavers is not considered to be human subject research as human subjects must be by definition “living individuals”. No additional ethical approval is needed to
use of cadavers for purposes of “science and research” in Germany.
Acknowledgments We thank Wolfgang Graulich, Andre Döring and Sarah Nüsser, Prof. Cengizhan Acikel and Prof. Fatih Zor from FAVOR Laboratories of GATA for statistical support, Prof. Saman Warnakulasuriya, Dr. Robert Sykes and Dr. David Mitchell for their grateful editorial supports.
References 1. Urken ML, Buchbinder D, Costantino PD, et al. Oromandibular reconstruction using microvascular composite flaps: report of 210 cases. Arch Otolaryngol Head Neck Surg 1998;124:46–55. 2. Holzle F, Wolff KD, Mohr C. Reconstructive oral and maxillofacial surgery. Dtsch Arztebl Int 2008;105:815–22. 3. Gurlek A, Miller MJ, Jacob RF, Lively JA, Schusterman MA. Functional results of dental restoration with osseointegrated implants after mandible reconstruction. Plast Reconstr Surg 1998;101:650–9. 4. Serafin D, Villarreal-Rios A, Georgiade NG. A rib-containing free flap to reconstruct mandibular defects. Br J Plast Surg 1977;30:263–6. 5. Bhathena HM, Kavarana NM. Primary reconstruction of head and neck cancer with anterior rib, osteomyocutaneous composite flap. Head Neck 1992;14:183–7. 6. Penfold CN, Davies HT, Cole RP, Evans BT, Hobby JA. Combined latissimus dorsi-serratus anterior/rib composite free flap in mandibular reconstruction. Int J Oral Maxillofac Surg 1992;21:92–6. 7. Song R, Lu C, Song Y, Liu J. Repair of large mandibular defects with vascularized rib grafts. Clin Plast Surg 1982;9:73–8. 8. Trignano E, Fallico N, Nitto A, Chen HC. The treatment of composite defect of bone and soft tissues with a combined latissimus dorsi and serratus anterior and rib free flap. Microsurgery 2013;33:173–83. 9. Kim PD, Blackwell KE. Latissimus-serratus-rib free flap for oromandibular and maxillary reconstruction. Arch Otolaryngol Head Neck Surg 2007;133:791–5. 10. Swartz WM, Banis JC, Newton ED, Ramasastry SS, Jones NF, Acland R. The osteocutaneous scapular flap for mandibular and maxillary reconstruction. Plast Reconstr Surg 1986;77:530–45. 11. Nkenke E, Vairaktaris E, Stelzle F, Neukam FW, Stockmann P, Linke R. Osteocutaneous free flap including medial and lateral scapular crests: technical aspects, viability, and donor site morbidity. J Reconstr Microsurg 2009;25:545–53. 12. Adell R, Lekholm U, Rockler B, Branemark PA. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387–416. 13. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983;50:399–410. 14. Breine U, Branemark PI. Reconstruction of alveolar jaw bone. An experimental and clinical study of immediate and preformed autologous bone grafts in combination with osseointegrated implants. Scand J Plast Reconstr Surg 1980;14:23–48. 15. Gallino M, Santamaria E, Doro T. Anthropometry of the scapula: clinical and surgical considerations. J Shoulder Elbow Surg 1998;7:284–91. 16. Martin R, Saller K. Textbook of anthropology. Stuttgart: Fischer; 1957 [in German]. 17. Hui KC, Zhang F, Lineaweaver WC, Moon W, Buncke GM, Buncke HJ. Serratus anterior-rib composite flap: anatomic studies and clinical application to hand reconstruction. Ann Plast Surg 1999;42:132–6. 18. Van Thienen CE, Deraemaecker R. The serratus anterior scapular flap—a new osteomuscular unit. Eur J Plast Surg 1988;11:156–61.
T.T. Sönmez et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349 19. Beckers A, Schenck C, Klesper B, Koebke J. Comparative densitometric study of iliac crest and scapula bone in relation to osseous integrated dental implants in microvascular mandibular reconstruction. J Craniomaxillofac Surg 1998;26:75–83. 20. Frodel Jr JL, Funk GF, Capper DT, et al. Osseointegrated implants: a comparative study of bone thickness in four vascularized bone flaps. Plast Reconstr Surg 1993;92:449–58. 21. Moscoso JF, Keller J, Genden E, et al. Vascularized bone flaps in oromandibular reconstruction. A comparative anatomic study of bone
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stock from various donor sites to assess suitability for enosseous dental implants. Arch Otolaryngol Head Neck Surg 1994;120:36–43. 22. Seikaly H, Chau J, Li F, et al. Bone that best matches the properties of the mandible. J Otolaryngol 2003;32:262–5. 23. Shimizu T, Ohno K, Michi K, Segawa K, Takiguchi R. Morphometric examination of the free scapular flap. Plast Reconstr Surg 1997;99:1947–53. 24. Ariyan S, Finseth FJ. The anterior chest approach for obtaining free osteocutaneous rib grafts. Plast Reconstr Surg 1978;62:676–85.
British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349
Morphometric study of the scapular free flap and the free rib osteomyocutaneous flap Tolga Taha Sönmez a,b,∗ , Andreas Prescher b , Anastasios Kanatas c , Arash Zaker Shahrak a , Marcus Gerressen a,d , Matthias Knobe e , Selman Hakki Altuntas f , Ali Modabber a , Timm Walter Steiner a , Ralf Smeets g , Alireza Ghassemi a , Frank Hölzle a a
Department of Oral and Maxillofacial Surgery, Medical Faculty, RWTH Aachen University, Aachen, Germany Institute of Molecular and Cellular Anatomy, Prosection, Medical Faculty, RWTH Aachen University, Aachen, Germany c Department of Oral and Maxillofacial Surgery, Leeds Teaching Hospitals and St James Institute of Oncology, Leeds Dental Institute, Leeds, United Kingdom d Department of Oral and Maxillofacial Surgery, Heinrich-Braun-Hospital, Location Zwickau, Zwickau, Germany e Department of Orthopedic and Trauma Surgery, Medical Faculty, RWTH Aachen University, Aachen, Germany f Department of Plastic Reconstructive and Aesthetic Surgery, Medical Faculty, Süleyman Demirel University School of Medicine, Isparta, Turkey g Department of Oral and Maxillofacial Surgery, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany b
Accepted 6 January 2014 Available online 28 January 2014
Abstract The scapula free flap is often the first choice for reconstruction of bony defects of the facial skeleton. However, the vascularised rib as part of a free rib osteomyocutaneous flap may be a suitable second choice. We have investigated the morphology and clinical dimensions of the 7th rib and the scapula, and the ability of the available bone to carry dental implants. The age and sex of the cadaver, and the donor side, were also recorded. The dimensions of the scapulas and 7th ribs (n = 130 of each) from 65 cadavers were measured at 4 different points using osteometric methods. Examination showed that bone from the scapula and 7th rib were sufficient for placement of implants. The 7th rib gave reliable measurements for both height and width, and a consistent relation between compact and cancellous bone. Although the scapula provided adequate compact and cancellous bone, there were variations depending on the segment of bone chosen. Bones from male cadavers were more suitable for implantation. In both the scapula and the 7th rib ageing had a significant adverse effect in only one dimension. Most points of measurement have satisfactory bony dimensions for insertion of dental implants. © 2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Keywords: Scapula; Rib; Oral and maxillofacial implant-carrying bone reconstruction; Morphometric and morphological bone measurements
Introduction Defects in the bone of the facial skeleton can be reconstructed successfully using free vascularised autogenous bony flaps.1,2 Anatomical reconstruction with adequate bone
∗ Corresponding author at: Department of Oral and Maxillofacial Surgery, Medical Faculty, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany. Tel.: +49 241 8035966; fax: +49 241 8082430. E-mail addresses: [email protected], [email protected], [email protected] (T.T. Sönmez).
for the insertion of dental implants is essential for optimal functional and aesthetic outcomes, with restoration of speech and chewing.2,3 The free vascularised rib flap is rarely used in clinical practice. The free rib osteomyocutaneous flap was first used in the head and neck by Serafin et al.,4 and their results were later confirmed by other studies.5–7 The latissimus-serratus-rib free flap has also been used successfully as a second choice of free flap.8,9 Since the early 1980s the osteocutaneous scapular flap has been the free flap of choice for reconstructions of combined bone and soft-tissue defects because it can
0266-4356/$ – see front matter © 2014 The British Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.bjoms.2014.01.005
T.T. Sönmez et al. / British Journal of Oral and Maxillofacial Surgery 52 (2014) 344–349
provide bone, muscle, and skin paddles in 3-dimensional configurations.10,11 An important objective of oral rehabilitation after bony reconstruction is a stable, implant-supported, prosthesis.12 Satisfactory osseointegration of an implant requires a width of bone sufficient to incorporate the length of the dental implant in the viable bony flap.12–14 However, there is no reported universally adopted guidance on the optimal anthropometric properties of the rib and the scapula.15,16 Methods for measuring implantable bone segments are also not adequately detailed in cadaveric studies for the microsurgical era.10,17,18 The clinical applicability of free vascularised rib flaps has been assessed in a few anatomical studies in which the authors have tried to work out the optimal characteristics of these bony flaps and their ability to provide a stable base for dental implants.19–23 However, we know of only one study that has compared the dimensions and biomechanical properties of the rib with those of other donor sites.22 Most other studies have been small, and the comparisons reported were not paired from the same cadavers, which is important for morphometric studies. In addition, the impacts of age, sex, and donor side were not adequately investigated. We aimed to study the bony morphology of scapular and free rib osteomyocutaneous flaps and their implantable bony dimensions to find out whether they fulfil the minimum requirements for osseointegration of dental implants. We also assessed the impact of age, sex, and donor side on these flaps.
345
Fig. 1. Reference marks for measurements. Sites of chosen measurement points in the scapula (left, dorsal view) and rib (right, inferior view). X = the costal tubercle.
of the rib was marked as measurement point 1. The distance from the upper margin to the lower margin in a straight line was defined as the height, and the distance from the outer to the inner surface in a straight line was defined as the width, as described by Martin and Saller (Figs. 1 and 2).16 The morphology of the bone was macroscopically assessed and documented at both donor sites (Fig. 2). Then, to evaluate the overall ability of the scapula and rib to withstand placement of dental implants, all measurements above our cut-off values that were 5.5 mm or wider and 10 mm or
Materials and methods We obtained samples of bone from central European adult cadavers (n = 65) at the Institute of Anatomy, RWTH (Rheinisch-Westfälische Technische Hochschule) University, Aachen. A total of 130 samples of 7th rib and 130 samples of scapula were taken bilaterally from 37 (57%) female and 28 (43%) male cadavers. Specimens ranged in age from 50 to 95 (mean 78) years. We used 4 measurement points on each bone sample to make 520 measurements of the width and height of the scapula and 520 of the width and height of the rib (Fig. 1). On the lateral border of the scapula, measurement point 4 was marked 2 cm inferior to the infraglenoid tuberculum and measurement point 1 was marked 2 cm superior to the inferior angle (Fig. 1). We defined height as the distance in a straight line from the lateral margin of the lateral border to the transitional zone of a thin, transparent, bony lamella of the infraspinal fossa (transverse diameter). The transitional zone was defined for each measurement point on each scapula. The width at each point was defined as the distance in a straight line, perpendicular to the height (Fig. 2). We used the pair of 7th ribs for our measurements. On each rib we marked the costal tubercle (X on Fig. 1), and at a point 8 cm lateral to the costal tubercle we then marked measurement point 4. A point 8 cm ventral to this point on the body
Fig. 2. The lateral border of the scapula (left) and the rib (right) from both sites of the same cadaver. Bones are shown in cross-sections with the side of origin. The figure integrates measurement points, sides, and surfaces. Morphology of the bone and the relation between compact and cancellous bone is seen in cross-sections of measurement points (MPs) 1–4/bony segment.
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Table 1 Mean (SD) and range of height and width (mm) of scapulas (n = 65) and ribs (n = 65). Two scapulas and 2 ribs were harvested from each cadaver. Each bone had 4 measuring points (n = 520). Measurement Scapula Width Height Rib Width Height
Mean (SD)
Range
10.9 (3.8) 12.3 (4.9)
4.4–22.4 4.6–28.7
6.7 (1.3) 13.2 (1.7)
4.3–12.1 8.5–18.8
Table 2 Overall ability by sex to withstand placement of a dental implant at each measurement point on the lateral borders of scapulas and 7th ribs, which had to be 5.5 mm or more wide and 10 mm or more high. Data are expressed as percentages. Measurement point
Point 1 Male Female Point 2 Male Female Point 3 Male Female Point 4 Male Female
Scapula 5.5 mm or more wide and 10 mm or more high
Rib 5.5 mm or more wide and 10 mm or more high
100 95.9
99.2 91.9
99.6 93.9
98.7 90.8
84.4 77.1
92.9 84.1
84.4 76.4
91.6 84.8
higher were taken for each measurement point and compared for both sexes (Tables 1 and 2, Fig. 4), as considered to be acceptable for successful osseointegration of an implant.12–14 Any measurement point with both height and width above the cut-off values was implantable (Table 2). Our statistical analyses were made with the help of SPSS for Windows (Version 15.0, SPSS Inc, Chicago, IL). We used the one-sample Kolmogorov Smirnov test for normality. Parametric or non-parametric tests were selected according to the distribution of variables. Student’s t test or the Mann–Whitney U test were used to compare variables between 2 groups. Descriptive statistics for continuous variables were reported as mean (SD) or median (range), and frequency and percentages were reported for categorical variables. Pearson’s correlation coefficient was calculated to assess the relations between variables. Probabilities of less than 0.05 were accepted as significant.
Results The mean (SD) height and width of both the scapula and the rib satisfied the dimensional requirements for successful osseointegration of implants (5.5 mm or more wide and 10 mm or more high) (Fig. 3, Tables 1 and 2).12–14 The mean values for height at both donor sites were clearly above the
Fig. 3. Diagram showing the mean width and height (mm) at 4 measurement points on the scapula and rib in men and women.
necessary value for length, with the mean height of the rib being slightly greater. The mean values for the width of the scapula were greater than those for the rib and were above the necessary value for width for both donor sites (Fig. 3). These bony dimensions and the relation of compact to cancellous bone are apparent in cross-section (Fig. 2). The morphology of ribs tended to be more consistent across bony segments from measuring points 1–4 (Fig. 2). The height:width proportion of each bony segment changed minimally from ventral to dorsal, with a relative increase in width. However, the morphology of the lateral border of the scapula showed characteristic propagation towards the infraglenoid tubercle with a decrease in height (Fig. 2). At the dorsal end, an inverse morphological structure emerged so that this bone became both narrower and taller. The difference between the range of values of both dimensions is therefore greater in the scapula than in the rib (Table 1). The minimum values of both dimensions of the rib were slightly lower than the acceptable values for placement of an implant. Measuring points 1 and 2 in male scapulas gave adequate bone for implants in all cases (Table 2), whereas at points 3 and 4 the dimensions of the scapula were not implantable in just 84.4% of male scapulas. In male ribs, implants could have been placed in between 91.6% and 99.2%. The bony morphology of the rib was relatively constant over the entire length from measuring points 1–4. There were significant sex differences in the width of ribs (female ribs 88.99, p < 0.0001), height of ribs (female ribs 14.94, p = 0.0002), width of scapula (female scapula 85.92, p < 0.0001) and height of scapula (female scapula 48.25, p < 0.0001), with male bones being larger. The relations between sex and the measured dimensions of scapulas and ribs are shown in Fig. 3.
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Fig. 4. Diagrams showing the relations between age (years) and height of the scapula (r = −0.26) (left) and age (years) and width of the rib (r = −0.32) (right).
Our results also showed that age negatively correlated both with width of rib (r = −0.32, 95% CI −0.527 to −0.088) and height of scapula (r = −0.26, 95% CI −0.474 to −0.018) (Fig. 4). We found no significant differences between the donor sides.
Discussion This study is to our knowledge one of the largest cadaver series ever conducted.18–23 The scapula, the iliac crest, and the fibula have each been rated highly for use in mandibular reconstruction.19 In other osteometric studies, the scapula has been considered equivalent to the iliac crest as a donor site, and in some aspects it may even be superior for placement of implants.21 In the present study we explored the dimensions of implantable bone of the 7th rib and the lateral border of the scapula for suitability during dental implantation (Table 2). We also considered the paired harvesting of bones from the same cadaver, which allowed statistical comparison of differences in the side from which the bone was taken. We found that the morphology of the lateral border of the scapula was such that it rotated around its own axis in a half spiral. Consequently, as one moved towards the infraglenoid portion of the lateral border, the height of harvestable bone decreased while the width increased (Figs. 1 and 2, Table 1). For this reason the anthropometric measurements do not reflect the clinically relevant bony dimensions of the lateral border, and a specific measuring technique is required.15,16 The anthropometric measurements for measuring the height and width of the rib have previously been reported to be clinically acceptable.16 A minimal vertical height of 10 mm with 1 mm of transversal bone around the implant is typically considered acceptable for successful osseointegration of implants.12–14 According to previous publications, an implant 3.5 mm in diameter requires a segment of bone with an overall minimum width
of 5.5 mm.19–23 The rib was not as wide as the scapula, but the mean values remained above 5.5 mm (Fig. 2 and Table 1), suggesting that it was nevertheless suitable. The rib offers advantages beyond consideration of width as it is higher, it has a constant ratio of compact:cancellous bone, and bony morphology is relatively constant (Figs. 1 and 2). The thick, compact bony structure improves the primary stability of an implant while the cancellous part facilitates better osseointegration.13,14 The scapula contains rich cancellous bone towards the inferior angle, while the compact bone widens in the lateral part as the cancellous area narrows (Fig. 2). In comparison, the harvestable region of bone in the 7th rib has an almost constant compact:cancellous bony relation across segments. The descriptive statistics of both donor sites showed that the mean height and width of bone was adequate (Table 1). However, some bony segments of the scapula fell below the required width and height that are acceptable for safe placement of implants. This is an important consideration for anyone contemplating the use of scapula as an implantcarrying bone flap. On the one hand the high maximum values alone would justify this use, but on the other, not all measured bony areas were adequate. In male bones the overall suitability for placement of implants was 84.4% at measuring points 3 and 4, and almost complete at points 1 and 2 (Table 2), so shorter and wider implants can be inserted in the lateral half of the harvested bone. The dorsal part (including the inferior angle to the harvested bone) better satisfies the requirements for safe placement of dental implants (Fig. 2). Alternatively, as one clinical study suggested, greater bony dimensions could be achieved by integrating the medial and the lateral border of the same microvascular flap.11 This may be an alternative to double-barrelled fibular flaps. To our knowledge this is the first study to show clearly such contrasting morphometric information about these 2 dimensions over several measurement points. Such information is likely to have been missed because in previous research fewer measurement points were used, and the
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predefined margins of the height of scapular bone were set to a predefined width.18–23 In comparison we individually measured the height of each scapula. For example Shimizu et al.23 calculated heights of 19–28 mm for the lateral border of the scapula and widths of 9–12 mm, using 3 measurement points. Another pilot study24 used a different measuring guide, and reported heights in the range of 13.2–19.5 mm and widths of 7.5–9 mm. Beckers et al.19 found the mean width to be 9.7 mm, which allowed an effective height for insertion of an implant of 13.2 mm. Unlike the scapula, the rib has a minimum height of 8.5 mm (with sufficient width), which is perfectly acceptable for implantation using currently available implant systems (Tables 1 and 2). Seikaly et al.22 reported that 89% (n = 22) of ribs satisfied the requirements (10 mm × 5.75 mm in this study) for safe placement of implants. As our study assessed the overall ability to withstand placement of a dental implant separately at each measuring point, we have been able to make precise statements for each bony region (Table 2). We therefore found, in contrast to their results, that the overall ability of the 7th rib to withstand placement of an implant ranged from 91.6% to 99.2% in male subjects. The bony morphology of the 7th rib can therefore be characterised as relatively constant for the placement of implants across all 4 measuring points (Fig. 2). This is the major advantage of using the 7th rib. It has consistent morphological dimensions along the whole length of the available bone with no need to compromise any osteotomies to rotate each bony segment. The impacts of age, sex, and side are extremely important in clinical practice. Despite their importance, these factors have rarely been investigated in previous morphometric studies.18–21 As expected, our statistical evaluation showed that there were significant differences between the sexes across all dimensions of both scapula and rib, with men’s bones being larger (Fig. 3, Tables 1 and 2). It is interesting that the adverse impact of ageing on the values measured at both donor sites was statistically confirmed in only one dimension for each bone, with the width of the rib and the height of the scapula diminishing with increasing age (Fig. 4). This finding may allow the placement of suitable dental implants in these bones, even though the patients are old.
Conflict of interest The authors have no financial interest to declare in relation to the content of this article.
Ethics statement The use of human cadavers is not considered to be human subject research as human subjects must be by definition “living individuals”. No additional ethical approval is needed to
use of cadavers for purposes of “science and research” in Germany.
Acknowledgments We thank Wolfgang Graulich, Andre Döring and Sarah Nüsser, Prof. Cengizhan Acikel and Prof. Fatih Zor from FAVOR Laboratories of GATA for statistical support, Prof. Saman Warnakulasuriya, Dr. Robert Sykes and Dr. David Mitchell for their grateful editorial supports.
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