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Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia
Journal of Cranio-Maxillo-Facial Surgery xxx (2017) 1e6
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Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia Xiaojun Chen 1, Aung M. Zin 1, Li Lin, Yu Xin, Wei Chen, Wenqing Han, Yan Zhang, Gang Chai**, Xianxian Yang* Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai JiaoTong University School of Medicine, People's Republic of China
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 27 July 2017 Accepted 8 December 2017 Available online xxx
Background: Many researchers have studied the relationship between facial asymmetry and cranial base morphology, but they have failed to reach a consensus. In this study, we aimed to verify whether the cranial base is involved in hemifacial microsomia (HFM). Methods: We included 66 patients with HFM who were treated at the Plastic and Reconstructive Surgery Department of Shanghai Ninth People's Hospital from January 2013 to October 2016. The patients were divided into three groups according to Pruzansky and OMENS classifications, separately. The controls were 20 patients diagnosed with mandibular angle hypertrophy but with no facial asymmetry. Angular and linear measurements of the cranial base were obtained for all patients. Results: The two classification methods yielded similar results. The intersection angle between two planes showed differences in the severe group. In the moderate and severe groups, the middle and posterior cranial angles were significantly different and the CIeP and SeP lengths were shorter in the affected side. Landmarks such as the carotid canal and internal acoustic canal could be considered as references. Conclusions: The cranial base is involved in hemifacial microsomia. This relationship supports the hypothesis of HFM pathogenesis and opens new avenues to classification methods. © 2017 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Hemifacial microsomia Cranial base Measurement
1. Introduction Hemifacial microsomia (HFM) is a disease characterized by facial asymmetry and a variety of other phenotypes, such as mandible anomalies and microtia (Cousley and Calvert, 1997). It is well known that the frontal and middle cranial base may affect facial morphology (Choi et al., 2010). Many researchers have studied the relationship between facial asymmetry and cranial base morphology, but they have failed to reach a consensus (Marsh et al.,
* Corresponding author. Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, 639 Zhi Zao Ju Road, 200011, Shanghai, People's Republic of China. ** Corresponding author. Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, 639 Zhi Zao Ju Road, 200011, Shanghai, People's Republic of China. E-mail addresses: [email protected] (G. Chai), [email protected] (X. Yang). 1 Xiaojun Chen and Aung Mar Zin are co-first authors and they contributed equally to the work.
1986; Figueroa et al., 1993; Kwon et al., 2006; Kapadia et al., 2013; Kim et al., 2013; Sepahdari and Mong, 2013; Marianetti et al., 2014). Only one study has explored cranial base deviation in HFM, but came to the conclusion that the cranial base was spared (Paliga et al., 2015). However, in clinical practice, we surmise that the cranial base is involved in HFM. This study aimed to verify this hypothesis.
2. Material and methods 2.1. Subjects We included 66 patients with HFM who were treated at the Plastic and Reconstructive Surgery Department of Shanghai Ninth People's Hospital between January 2013 and October 2016. Inclusion criteria were as follows: older than 2 years old; diagnosed with unilateral HFM; and no previous surgical treatment. Patients were divided into three groups according to Pruzansky's classification (Table 1) or the OMENS classification (Gougoutas et al., 2007)
https://doi.org/10.1016/j.jcms.2017.12.008 1010-5182/© 2017 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008
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X. Chen et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2017) 1e6
Table 1 Patients divided according to Pruzansky's classification. Group
Pruzansky classification
n
Age, years [range (mean)]
Lateral
Mild Moderate Severe
I IIa IIb, III
16 (12M 4F) 23 (21M 2F) 27 (13M 14F)
3e36 (10.38) 2e21 (6.48) 2e21 (5.37)
13L 3R 10L 13R 16L 11R
M: male; F: female; L: left; R: right.
(Table 2). Controls were 20 patients diagnosed with mandibular angle hypertrophy but with no facial asymmetry. Facial asymmetry was assessed using the menton deviation.
Table 3 Major landmarks. Cr (crista galli) CI (anterior clinoid process) P (petrous ridge)
2.2. Data collection All patients underwent full craniofacial computed tomography (CT) scans (including the cranium and facial skeleton) at the Frankfort horizontal plane (slice thickness, 1 mm). Threedimensional (3D) images were then constructed using Mimics 15.0: soft tissues were excluded by using the thresholding setting; the cranial base was selected by using the Edit Masks and Region Growing functions; 3D images were obtained by using Calculate 3D from the Masks menu; and finally measurements were obtained by using the Measure and Analyze functions. Several parameters were measured, including angles, lengths, and distances. Aside from the intersection angle between two planes (plane 1 defined by the crista galli, anterior clinoid process, and foramen cecum; plane 2 defined by the anterior clinoid process, opisthion, and occipital protuberance), the measurements were obtained as reported previously (Kwon et al., 2006; Paliga et al., 2015) (Table 3 and Figs. 1e3) by two well-trained, professional surgeons. Data were measured twice by each surgeon on different days, and then the mean values were calculated.
S (sphenoid) Op (opisthion)
Most superior edge of the crista galli Midpoint between the anterior clinoid processes Junction of the superior ridge of the petrous pyramid of the temporal bone and the inner surface of the parietal bone The most anterior point of the posterior edge of the lesser wing of the sphenoid Midpoint of the posterior arch of the foramen magnum
2.3. Data analysis Data were collected and analyzed using SAS V8. All the feature variables obeyed a normal distribution, so the intersection angles of patients were compared with those of the controls using a group ttest, whilst a paired t-test was used to compare the rest parameters between affected and unaffected sides. All the statistical analyses in this study set a ¼ 0.05, and regarded p < 0.05 as statistically significant. 3. Results 3.1. Patients divided according to Pruzansky's classification 3.1.1. Angles The mean intersection angles are shown in Table 4. There were significant differences between the severe group and the control (p ¼ 0.004). The mean intersection angle was 3.13 degrees in the severe group. In regard to the intersection angle, there were three abnormal values in the severe group (7.51, 7.69, and 10.66 degrees), which we
Fig. 1. Major landmarks: A (foramen cecum); Cr (crista galli); CI (anterior clinoid process); Op (opisthion); C (occipital protuberance); S (sphenoid); P (petrous ridge).
excluded from the analysis. These large angles were caused by oblique plane 1 because their foramen ceca were not in the middle. Since our sample size was relatively small, we could not identify whether the change was due to the presence of severe HFM.
Table 2 Patients divided according to the OMENS classification (mainly by orbit and mandible). Group
OMENS classification
n
Age, years [range (mean)]
Lateral
Mild Moderate Severe
O0M1 O1M1, O0M2a, O1M2a O2M2a, O3M2a, O0M2b, O1M2b, O2M2b, O3M2b, O1M3, O3M3
15 (11M 4F) 16 (15M 1F) 35 (20M 15F)
2e36 (10.40) 2e18 (6.25) 2e21 (5.83)
12L 3R 7L 9R 20L 15R
M: male; F: female; L: left; R: right.
Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008
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Fig. 2. 3D-reconstruction of an 11-year-old boy in the moderate group (left to right: anterior view; left-anterior oblique view; left lateral view; upward view; cranial base).
Fig. 3. 3D-reconstruction of a 7-year-old boy in the severe group (left to right: anterior view; right-anterior oblique view; right lateral view; upward view; cranial base).
Table 4 Intersection angle between planes 1 and 2.
Table 6 Length measurements in mild groups.
Group
n
Mean ( )
SD ( )
p (a ¼ 0.05)
Mild Moderate Severe Control
16 23 24 20
2.03 2.17 3.13 2.05
1.05 1.26 1.47 0.64
0.943 0.705 0.004 e
A comparison of the cranial base angles between the affected and unaffected sides in different groups is provided in Table 5. The anterior cranial angle (:CreCIeS) showed no significant differences, whereas the middle angle (:SeCIeP) and posterior cranial angle (:PeCIeOp) were significantly different in the moderate and severe groups. 3.1.2. Lengths The mean lengths between two landmarks can be seen as a reflection of the size of the cranial base. There was no disparity in the mild group (Table 6), but there were significant differences in SeP in the moderate group (Table 7), and in CIeP and SeP in the
Table 5 A comparison of the cranial base angles between affected and unaffected sides in different groups. Cranial angle Mild Anterior Middle Posterior Moderate Anterior Middle Posterior Severe Anterior Middle Posterior
Affected ( )
Unaffected ( )
p (a ¼ 0.05)
61.99 ± 6.83 66.65 ± 3.51 53.41 ± 3.93
61.49 ± 4.35 68.55 ± 3.07 52.34 ± 3.15
0.696 0.099 0.101
61.19 ± 4.49 66.00 ± 4.55 54.68 ± 3.59
60.57 ± 4.92 68.91 ± 3.69 53.18 ± 3.22
0.375 0.001 0.008
60.80 ± 2.88 66.02 ± 3.26 55.60 ± 2.88
60.22 ± 3.04 67.91 ± 3.74 54.06 ± 2.37
0.393 0.032 0.021
Affected (mm) CreS CIeS CIeP SeP PeOp
45.70 46.00 68.72 65.87 62.20
± ± ± ± ±
7.37 7.23 9.69 7.73 4.27
Unaffected (mm) 44.67 45.00 70.50 68.45 61.64
± ± ± ± ±
5.47 5.97 7.05 6.04 4.38
p (a ¼ 0.05) 0.522 0.521 0.334 0.125 0.473
Table 7 Length measurements in moderate groups. Affected (mm) CreS CIeS CIeP SeP PeOp a
43.51 43.11 65.72 62.22 61.26
± ± ± ± ±
7.19 6.35 7.08 6.66 3.71
Unaffected (mm) 42.69 42.77 67.16 65.54 60.28
± ± ± ± ±
6.55 4.93 8.21 7.61 3.67
p (a ¼ 0.05) 0.238 0.673 0.156 0.001a 0.094
Significant difference.
severe group (Table 8). The length values on the affected side were shorter than those on the unaffected side, indicating a width gap in the posterior fossa of patients with HFM. 3.1.3. Distances Plane 2, defined by CI, Op, and occipital protuberance, can be considered as the midplane of the middle and posterior cranial fossa. The distances from certain landmarks to plane 2 may offer Table 8 Length measurements in severe groups. Affected (mm) CreS CIeS CIeP SeP PeOp a
40.87 41.64 63.15 59.96 60.18
± ± ± ± ±
4.65 4.87 6.36 5.95 3.98
Unaffected (mm) 40.47 41.59 65.13 62.82 59.74
± ± ± ± ±
4.09 4.57 5.27 5.80 3.09
p (a ¼ 0.05) 0.520 0.943 0.013a 0.001a 0.526
Significant difference.
Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008
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X. Chen et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2017) 1e6
some candidate measures to predict the asymmetry of the cranial base. In the mild group, there were significant differences in the carotid canal (p ¼ 0.027) and internal acoustic meatus (p ¼ 0.013). In the moderate group, there were significant differences in the carotid canal (p ¼ 0.008), foramen rotundum (p ¼ 0.012), foramen ovale (p ¼ 0.025), and internal acoustic meatus (p ¼ 0.006). In the severe group, there were significant differences in the optic canal (p ¼ 0.005), carotid canal (p ¼ 0.020), internal acoustic meatus (p < 0.001), and hypoglossal canal (p ¼ 0.008).
Table 12 Length measurements in moderate groups according to the OMENS classification.
3.2. Patients divided according to the OMENS classification
Table 13 Length measurements in severe groups according to the OMENS classification.
Pruzansky's classification focuses on the mandible, which is only one of the affected features in HFM. The OMENS classification is more comprehensive. Pairwise correlation analysis showed significant correlations among the orbit (O), mandible (M), and soft tissue (S) (O and M: p ¼ 0.004; O and S: p ¼ 0.009; M and S: p ¼ 0.017), which is contrary to the results of the meta-analysis conducted by Tuin et al. (2015). Soft tissue grading is subjective and lacks a quantitative index. Here, we combined the orbit and mandible to perform a new grading system. We defined O0M1 as mild, O1M1, O0M2a, O1M2a as moderate, and O2e3 or M2be3 as severe. Then we repeated the procedures described above. The results were similar to those obtained using Pruzansky's classification (Tables 9e16). Positive findings were summarized in Table 17. 4. Discussion The inclusion criteria for HFM patients used to start from 1 year old (Paliga et al., 2015). In this study, we increased this inclusion criterion from 1 year old to 2 years old. According to pediatrics, the Table 9 Intersection angle between planes 1 and 2 according to the OMENS classification. Group
n
Mean ( )
SD ( )
p (a ¼ 0.05)
Mild Moderate Severe Controls
15 16 35 20
1.99 2.14 3.47 2.05
1.08 1.26 2.30 0.64
0.827 0.802 0.010 e
Table 10 A comparison of the cranial base angles between affected and unaffected sides in different groups divided according to the OMENS classification. Cranial angle Mild Anterior Middle Posterior Moderate Anterior Middle Posterior Severe Anterior Middle Posterior
Affected ( )
Unaffected ( )
p (a ¼ 0.05)
61.84 ± 7.04 66.58 ± 3.62 53.45 ± 4.07
61.24 ± 4.39 68.64 ± 3.16 52.39 ± 3.26
0.664 0.093 0.127
61.26 ± 4.59 65.96 ± 4.99 55.04 ± 3.39
59.14 ± 3.85 69.59 ± 3.91 53.24 ± 2.85
0.003 0.001 0.004
60.95 ± 3.23 66.08 ± 3.26 55.17 ± 3.17
61.09 ± 3.95 67.78 ± 3.49 53.78 ± 2.78
0.814 0.020 0.013
Table 11 Length measurements in mild groups according to the OMENS classification. Affected (mm) CreS CIeS CIeP SeP PeOp
45.64 46.16 68.67 65.82 62.08
± ± ± ± ±
7.62 7.46 10.03 8.00 4.40
Unaffected (mm) 44.56 45.20 70.32 68.43 61.47
± ± ± ± ±
5.65 6.12 7.26 6.25 4.48
p (a ¼ 0.05) 0.530 0.567 0.401 0.149 0.467
Affected (mm) CreS CIeS CIeP SeP PeOp
44.67 43.91 66.47 63.00 62.43
± ± ± ± ±
6.96 6.26 5.33 5.55 3.42
42.93 43.51 67.60 66.57 60.92
Affected (mm) CreS CIeS CIeP SeP PeOp
41.02 41.63 63.50 60.24 59.97
± ± ± ± ±
5.23 5.11 7.15 6.52 3.83
Unaffected (mm) ± ± ± ± ±
6.59 5.39 5.75 5.69 2.74
Unaffected (mm) 40.97 41.50 65.57 63.06 59.68
± ± ± ± ±
4.76 4.25 7.21 6.95 3.58
p (a ¼ 0.05) 0.023 0.652 0.351 0.002 0.030
p (a ¼ 0.05) 0.923 0.849 0.004 <0.001 0.610
Table 14 Distances from certain points to plane 2 in the mild group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
7.96 ± 1.29 9.37 ± 1.89 17.45 ± 2.89 24.22 ± 4.24 22.74 ± 2.49 14.83 ± 3.45
8.23 ± 1.68 10.55 ± 1.72 18.27 ± 2.54 24.16 ± 3.29 24.73 ± 3.40 14.49 ± 2.37
0.442 0.046 0.173 0.939 0.016 0.795
Table 15 Distances from certain points to plane 2 in the moderate group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
7.71 ± 1.36 9.70 ± 1.22 15.99 ± 1.66 20.95 ± 3.38 20.38 ± 2.28 13.00 ± 1.80
8.22 ± 1.23 11.26 ± 1.48 17.58 ± 1.77 23.23 ± 1.87 23.16 ± 2.57 14.23 ± 2.26
0.111 <0.001 0.008 0.011 <0.001 0.075
Table 16 Distances from certain points to plane 2 in the severe group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
8.09 ± 1.28 9.91 ± 1.59 16.65 ± 2.37 21.41 ± 4.56 21.09 ± 2.49 12.48 ± 1.39
7.51 ± 1.24 10.53 ± 1.57 16.84 ± 2.79 21.76 ± 2.62 22.37 ± 2.53 13.52 ± 1.92
0.002 0.036 0.632 0.590 0.002 0.020
average head circumference is 34 mm in newborns, 46 mm at 1 year, 48 mm at 2 years, and 49e50 mm at 6 years of age (Hu and Jiang, 2002; Kliegman and Nelson, 2011). So infants continue to grow quickly after 1 year old. In other words, there is a serious possibility that cranial base morphology changes as those 1-yearold patients get older. The ideal situation would be for all the patients have developed fully, resulting in relatively accurate measuring results. However, the skull may not reach its mature shape until 11e12 years old (Bastir et al., 2006). Most patients were treated at an early age to achieve the best outcome, so we failed to find enough cases in which the skull had fully developed. We therefore chose the period during which skull development is relatively slow e from the age of two years. In previous studies, deviation of the cranial base was often evaluated through the cranial base angle, which is articulated by
Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008
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Table 17 A summary of positive findings. Classification group
Mild Moderate Severe
Angles
Lengths
Distances
Pruzansky
OMENS
Pruzansky
OMENS
Pruzansky
OMENS
e MCA; PCA IA; MCA; PCA
e ACA; MCA; PCA IA; MCA; PCA
e SeP CIeP; SeP
e CreS; SeP; PeOp CIeP; SeP
CC; IAM CC; FR; FO; IAM OC; CC; IAM; HC
CC; IAM CC; FR; FO; IAM; HC OC; CC; IAM; HC
IA: intersection angle; ACA: anterior cranial angle; MCA: middle cranial angle; PCA: posterior cranial angle; CC: carotid canal; FR: foramen rotundum; FO: foramen ovale; IAM: internal acoustic meatus; HC: hypoglossal canal.
three points: 1. the foramen cecum or crista galli; 2. the tuberculum sella or anterior clinoid process; 3. the occipital protuberance (Marsh et al., 1986; Figueroa et al., 1993; Kwon et al., 2006; Kapadia et al., 2013; Kim et al., 2013; Marianetti et al., 2014; Paliga et al., 2015). However, just three points might not reflect the deviation so accurately. When researchers locate these points in the software, there will no doubt exist some degree of deviation. A small deviation may cause great bias in the angle, so we summarized the landmarks used before and defined two new planes: one (defined by the crista galli, anterior clinoid process, and foramen cecum) as the middle axle of the anterior cranial fossa; the another (articulated by the anterior clinoid process, occipital protuberance, and occipital protuberance) as the middle axle of the middle and posterior cranial fossa. The intersection angle is used to estimate the cranial base deviation, theoretically with fewer error values than those caused by human factors. Measurements were carried out on the basis of both the Pruzansky and OMENS classifications, which increased credibility. In the moderate and severe groups, the middle and posterior cranial angles were statistically significant, and the CIeP and SeP lengths were clearly shorter on the affected side, which implied growth restriction on the affected side, especially in the posterior fossa. Such landmarks as the carotid canal and internal acoustic canal can also be considered as reference points. Asymmetry in the morphology of the cranial base between affected and unaffected sides shows clearly that the cranial base is not spared in HFM. It seems that the more severe the HFM is, the more changes there are in cranial base morphology. This cranial base morphology change may be in direct proportion to HFM severity as judged by a Pruzansky/OMENS classification. Our study first revealed that the cranial base may be part of the hemifacial microsomia, and that it is derived from the first branchial arch (Sadler and Langman, 2000). Using a pairwise correlation method, we showed that the orbit, mandible, and soft tissues were associated in terms of degree of severity, which was consistent with a previous meta-analysis (Gougoutas et al., 2007), and they were also mainly developed from the first branchial arch (Poswillo, 1988). In other words, the cranial base, orbit, mandible, and soft tissues are of the same origin. The positive results for cranial base variation in HFM may help to verify the hypothesis that HFM is caused by an abnormity during the migration and development of the first branchial arch, especially by the expanding hematoma arising from the stapedial artery disruption (Mao and Nah, 2004). As reported by Murray et al. (1984), the spheno-occipital synchondrosis (SOS), which is located between the sphenoid and occipital bones, is primarily responsible for the growth of the cranial base and all facial skeletal structures, including the mandible. It seems to be the only growth plate that remains functional in the cranial base until adolescence in humans. The SOS may therefore be the origin of HFM. No existing classifications of HFM involve the cranial base. The Pruzansky classification only concentrates on mandibular deformities, while the OMENS classification also pays little attention to the cranial base. A new item e ‘cranial base’ e might as well be
added into the OMENS classification but, before that can happen, a lot of further research needs to be carried out to verify this. This study has some limitations. The number of inclusive patients was not big enough to eliminate sampling error. In an ideal situation, there should be more subjects, of a similar age, to reduce the influence of age and corresponding growth and development. In our study, compared with the reported gender ratio (male:female ¼ 3:2) (Murray et al., 1984), the boys far outnumbered the girls (male:female ¼ 46:20), which may be due to the small sample size or to a traditional preference for male heirs in some areas of China. Although no significant gender effects on differences in cranial base measurements have been uncovered, whether this sex inequality will influence the results remains unknown. 5. Conclusions The cranial base is involved in HFM. We found significant differences in the intersection angle, middle angle, and posterior cranial base angle, as well as the CIeP and SeP lengths, in moderate and severe HFM. Landmarks such as the carotid canal and internal acoustic canal could be considered as references. It may help to verify the hypothesis of pathogenesis, and offer a new classification option. Financial disclosure statement Financial support was provided by National Natural Science Foundation of China (No. 81372097), The Shanghai Committee of Science and Technology, China (No. 14441900800, No. 14441900802), Project of Shanghai Jiao Tong University Medical and Engineering Cross Fund (YG2014MS06). The three years' plan of promoting Municipal Hospital's Clinical Skill and Innovation (16CR2010A). The authors have no financial interest in any of the products or devices mentioned in this article. Authors' contributions Xiaojun Chen, M.D. Analysis and interpretation of the data, draft the article. Aung M. Zin, M.D. Acquisition of the data and measurements. Li Lin, M.D. Acquisition of the data. Yu Xin, M.D. Acquisition of the data. Wei Chen, M.D. Completion of the Measurement. Wenqing Han, M.D. Completion of the Measurement. Yan Zhang, M.D. The overall arrangements and revision of the article. Gang Chai, M.D. Design the implementation plane. Xianxian Yang, M.D. Guidance of the task and revision of the article. Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.jcms.2017.12.008.
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Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia Xiaojun Chen 1, Aung M. Zin 1, Li Lin, Yu Xin, Wei Chen, Wenqing Han, Yan Zhang, Gang Chai**, Xianxian Yang* Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, Shanghai JiaoTong University School of Medicine, People's Republic of China
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 27 July 2017 Accepted 8 December 2017 Available online xxx
Background: Many researchers have studied the relationship between facial asymmetry and cranial base morphology, but they have failed to reach a consensus. In this study, we aimed to verify whether the cranial base is involved in hemifacial microsomia (HFM). Methods: We included 66 patients with HFM who were treated at the Plastic and Reconstructive Surgery Department of Shanghai Ninth People's Hospital from January 2013 to October 2016. The patients were divided into three groups according to Pruzansky and OMENS classifications, separately. The controls were 20 patients diagnosed with mandibular angle hypertrophy but with no facial asymmetry. Angular and linear measurements of the cranial base were obtained for all patients. Results: The two classification methods yielded similar results. The intersection angle between two planes showed differences in the severe group. In the moderate and severe groups, the middle and posterior cranial angles were significantly different and the CIeP and SeP lengths were shorter in the affected side. Landmarks such as the carotid canal and internal acoustic canal could be considered as references. Conclusions: The cranial base is involved in hemifacial microsomia. This relationship supports the hypothesis of HFM pathogenesis and opens new avenues to classification methods. © 2017 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Hemifacial microsomia Cranial base Measurement
1. Introduction Hemifacial microsomia (HFM) is a disease characterized by facial asymmetry and a variety of other phenotypes, such as mandible anomalies and microtia (Cousley and Calvert, 1997). It is well known that the frontal and middle cranial base may affect facial morphology (Choi et al., 2010). Many researchers have studied the relationship between facial asymmetry and cranial base morphology, but they have failed to reach a consensus (Marsh et al.,
* Corresponding author. Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, 639 Zhi Zao Ju Road, 200011, Shanghai, People's Republic of China. ** Corresponding author. Department of Plastic and Reconstructive Surgery, Shanghai Ninth People's Hospital, 639 Zhi Zao Ju Road, 200011, Shanghai, People's Republic of China. E-mail addresses: [email protected] (G. Chai), [email protected] (X. Yang). 1 Xiaojun Chen and Aung Mar Zin are co-first authors and they contributed equally to the work.
1986; Figueroa et al., 1993; Kwon et al., 2006; Kapadia et al., 2013; Kim et al., 2013; Sepahdari and Mong, 2013; Marianetti et al., 2014). Only one study has explored cranial base deviation in HFM, but came to the conclusion that the cranial base was spared (Paliga et al., 2015). However, in clinical practice, we surmise that the cranial base is involved in HFM. This study aimed to verify this hypothesis.
2. Material and methods 2.1. Subjects We included 66 patients with HFM who were treated at the Plastic and Reconstructive Surgery Department of Shanghai Ninth People's Hospital between January 2013 and October 2016. Inclusion criteria were as follows: older than 2 years old; diagnosed with unilateral HFM; and no previous surgical treatment. Patients were divided into three groups according to Pruzansky's classification (Table 1) or the OMENS classification (Gougoutas et al., 2007)
https://doi.org/10.1016/j.jcms.2017.12.008 1010-5182/© 2017 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008
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Table 1 Patients divided according to Pruzansky's classification. Group
Pruzansky classification
n
Age, years [range (mean)]
Lateral
Mild Moderate Severe
I IIa IIb, III
16 (12M 4F) 23 (21M 2F) 27 (13M 14F)
3e36 (10.38) 2e21 (6.48) 2e21 (5.37)
13L 3R 10L 13R 16L 11R
M: male; F: female; L: left; R: right.
(Table 2). Controls were 20 patients diagnosed with mandibular angle hypertrophy but with no facial asymmetry. Facial asymmetry was assessed using the menton deviation.
Table 3 Major landmarks. Cr (crista galli) CI (anterior clinoid process) P (petrous ridge)
2.2. Data collection All patients underwent full craniofacial computed tomography (CT) scans (including the cranium and facial skeleton) at the Frankfort horizontal plane (slice thickness, 1 mm). Threedimensional (3D) images were then constructed using Mimics 15.0: soft tissues were excluded by using the thresholding setting; the cranial base was selected by using the Edit Masks and Region Growing functions; 3D images were obtained by using Calculate 3D from the Masks menu; and finally measurements were obtained by using the Measure and Analyze functions. Several parameters were measured, including angles, lengths, and distances. Aside from the intersection angle between two planes (plane 1 defined by the crista galli, anterior clinoid process, and foramen cecum; plane 2 defined by the anterior clinoid process, opisthion, and occipital protuberance), the measurements were obtained as reported previously (Kwon et al., 2006; Paliga et al., 2015) (Table 3 and Figs. 1e3) by two well-trained, professional surgeons. Data were measured twice by each surgeon on different days, and then the mean values were calculated.
S (sphenoid) Op (opisthion)
Most superior edge of the crista galli Midpoint between the anterior clinoid processes Junction of the superior ridge of the petrous pyramid of the temporal bone and the inner surface of the parietal bone The most anterior point of the posterior edge of the lesser wing of the sphenoid Midpoint of the posterior arch of the foramen magnum
2.3. Data analysis Data were collected and analyzed using SAS V8. All the feature variables obeyed a normal distribution, so the intersection angles of patients were compared with those of the controls using a group ttest, whilst a paired t-test was used to compare the rest parameters between affected and unaffected sides. All the statistical analyses in this study set a ¼ 0.05, and regarded p < 0.05 as statistically significant. 3. Results 3.1. Patients divided according to Pruzansky's classification 3.1.1. Angles The mean intersection angles are shown in Table 4. There were significant differences between the severe group and the control (p ¼ 0.004). The mean intersection angle was 3.13 degrees in the severe group. In regard to the intersection angle, there were three abnormal values in the severe group (7.51, 7.69, and 10.66 degrees), which we
Fig. 1. Major landmarks: A (foramen cecum); Cr (crista galli); CI (anterior clinoid process); Op (opisthion); C (occipital protuberance); S (sphenoid); P (petrous ridge).
excluded from the analysis. These large angles were caused by oblique plane 1 because their foramen ceca were not in the middle. Since our sample size was relatively small, we could not identify whether the change was due to the presence of severe HFM.
Table 2 Patients divided according to the OMENS classification (mainly by orbit and mandible). Group
OMENS classification
n
Age, years [range (mean)]
Lateral
Mild Moderate Severe
O0M1 O1M1, O0M2a, O1M2a O2M2a, O3M2a, O0M2b, O1M2b, O2M2b, O3M2b, O1M3, O3M3
15 (11M 4F) 16 (15M 1F) 35 (20M 15F)
2e36 (10.40) 2e18 (6.25) 2e21 (5.83)
12L 3R 7L 9R 20L 15R
M: male; F: female; L: left; R: right.
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Fig. 2. 3D-reconstruction of an 11-year-old boy in the moderate group (left to right: anterior view; left-anterior oblique view; left lateral view; upward view; cranial base).
Fig. 3. 3D-reconstruction of a 7-year-old boy in the severe group (left to right: anterior view; right-anterior oblique view; right lateral view; upward view; cranial base).
Table 4 Intersection angle between planes 1 and 2.
Table 6 Length measurements in mild groups.
Group
n
Mean ( )
SD ( )
p (a ¼ 0.05)
Mild Moderate Severe Control
16 23 24 20
2.03 2.17 3.13 2.05
1.05 1.26 1.47 0.64
0.943 0.705 0.004 e
A comparison of the cranial base angles between the affected and unaffected sides in different groups is provided in Table 5. The anterior cranial angle (:CreCIeS) showed no significant differences, whereas the middle angle (:SeCIeP) and posterior cranial angle (:PeCIeOp) were significantly different in the moderate and severe groups. 3.1.2. Lengths The mean lengths between two landmarks can be seen as a reflection of the size of the cranial base. There was no disparity in the mild group (Table 6), but there were significant differences in SeP in the moderate group (Table 7), and in CIeP and SeP in the
Table 5 A comparison of the cranial base angles between affected and unaffected sides in different groups. Cranial angle Mild Anterior Middle Posterior Moderate Anterior Middle Posterior Severe Anterior Middle Posterior
Affected ( )
Unaffected ( )
p (a ¼ 0.05)
61.99 ± 6.83 66.65 ± 3.51 53.41 ± 3.93
61.49 ± 4.35 68.55 ± 3.07 52.34 ± 3.15
0.696 0.099 0.101
61.19 ± 4.49 66.00 ± 4.55 54.68 ± 3.59
60.57 ± 4.92 68.91 ± 3.69 53.18 ± 3.22
0.375 0.001 0.008
60.80 ± 2.88 66.02 ± 3.26 55.60 ± 2.88
60.22 ± 3.04 67.91 ± 3.74 54.06 ± 2.37
0.393 0.032 0.021
Affected (mm) CreS CIeS CIeP SeP PeOp
45.70 46.00 68.72 65.87 62.20
± ± ± ± ±
7.37 7.23 9.69 7.73 4.27
Unaffected (mm) 44.67 45.00 70.50 68.45 61.64
± ± ± ± ±
5.47 5.97 7.05 6.04 4.38
p (a ¼ 0.05) 0.522 0.521 0.334 0.125 0.473
Table 7 Length measurements in moderate groups. Affected (mm) CreS CIeS CIeP SeP PeOp a
43.51 43.11 65.72 62.22 61.26
± ± ± ± ±
7.19 6.35 7.08 6.66 3.71
Unaffected (mm) 42.69 42.77 67.16 65.54 60.28
± ± ± ± ±
6.55 4.93 8.21 7.61 3.67
p (a ¼ 0.05) 0.238 0.673 0.156 0.001a 0.094
Significant difference.
severe group (Table 8). The length values on the affected side were shorter than those on the unaffected side, indicating a width gap in the posterior fossa of patients with HFM. 3.1.3. Distances Plane 2, defined by CI, Op, and occipital protuberance, can be considered as the midplane of the middle and posterior cranial fossa. The distances from certain landmarks to plane 2 may offer Table 8 Length measurements in severe groups. Affected (mm) CreS CIeS CIeP SeP PeOp a
40.87 41.64 63.15 59.96 60.18
± ± ± ± ±
4.65 4.87 6.36 5.95 3.98
Unaffected (mm) 40.47 41.59 65.13 62.82 59.74
± ± ± ± ±
4.09 4.57 5.27 5.80 3.09
p (a ¼ 0.05) 0.520 0.943 0.013a 0.001a 0.526
Significant difference.
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X. Chen et al. / Journal of Cranio-Maxillo-Facial Surgery xxx (2017) 1e6
some candidate measures to predict the asymmetry of the cranial base. In the mild group, there were significant differences in the carotid canal (p ¼ 0.027) and internal acoustic meatus (p ¼ 0.013). In the moderate group, there were significant differences in the carotid canal (p ¼ 0.008), foramen rotundum (p ¼ 0.012), foramen ovale (p ¼ 0.025), and internal acoustic meatus (p ¼ 0.006). In the severe group, there were significant differences in the optic canal (p ¼ 0.005), carotid canal (p ¼ 0.020), internal acoustic meatus (p < 0.001), and hypoglossal canal (p ¼ 0.008).
Table 12 Length measurements in moderate groups according to the OMENS classification.
3.2. Patients divided according to the OMENS classification
Table 13 Length measurements in severe groups according to the OMENS classification.
Pruzansky's classification focuses on the mandible, which is only one of the affected features in HFM. The OMENS classification is more comprehensive. Pairwise correlation analysis showed significant correlations among the orbit (O), mandible (M), and soft tissue (S) (O and M: p ¼ 0.004; O and S: p ¼ 0.009; M and S: p ¼ 0.017), which is contrary to the results of the meta-analysis conducted by Tuin et al. (2015). Soft tissue grading is subjective and lacks a quantitative index. Here, we combined the orbit and mandible to perform a new grading system. We defined O0M1 as mild, O1M1, O0M2a, O1M2a as moderate, and O2e3 or M2be3 as severe. Then we repeated the procedures described above. The results were similar to those obtained using Pruzansky's classification (Tables 9e16). Positive findings were summarized in Table 17. 4. Discussion The inclusion criteria for HFM patients used to start from 1 year old (Paliga et al., 2015). In this study, we increased this inclusion criterion from 1 year old to 2 years old. According to pediatrics, the Table 9 Intersection angle between planes 1 and 2 according to the OMENS classification. Group
n
Mean ( )
SD ( )
p (a ¼ 0.05)
Mild Moderate Severe Controls
15 16 35 20
1.99 2.14 3.47 2.05
1.08 1.26 2.30 0.64
0.827 0.802 0.010 e
Table 10 A comparison of the cranial base angles between affected and unaffected sides in different groups divided according to the OMENS classification. Cranial angle Mild Anterior Middle Posterior Moderate Anterior Middle Posterior Severe Anterior Middle Posterior
Affected ( )
Unaffected ( )
p (a ¼ 0.05)
61.84 ± 7.04 66.58 ± 3.62 53.45 ± 4.07
61.24 ± 4.39 68.64 ± 3.16 52.39 ± 3.26
0.664 0.093 0.127
61.26 ± 4.59 65.96 ± 4.99 55.04 ± 3.39
59.14 ± 3.85 69.59 ± 3.91 53.24 ± 2.85
0.003 0.001 0.004
60.95 ± 3.23 66.08 ± 3.26 55.17 ± 3.17
61.09 ± 3.95 67.78 ± 3.49 53.78 ± 2.78
0.814 0.020 0.013
Table 11 Length measurements in mild groups according to the OMENS classification. Affected (mm) CreS CIeS CIeP SeP PeOp
45.64 46.16 68.67 65.82 62.08
± ± ± ± ±
7.62 7.46 10.03 8.00 4.40
Unaffected (mm) 44.56 45.20 70.32 68.43 61.47
± ± ± ± ±
5.65 6.12 7.26 6.25 4.48
p (a ¼ 0.05) 0.530 0.567 0.401 0.149 0.467
Affected (mm) CreS CIeS CIeP SeP PeOp
44.67 43.91 66.47 63.00 62.43
± ± ± ± ±
6.96 6.26 5.33 5.55 3.42
42.93 43.51 67.60 66.57 60.92
Affected (mm) CreS CIeS CIeP SeP PeOp
41.02 41.63 63.50 60.24 59.97
± ± ± ± ±
5.23 5.11 7.15 6.52 3.83
Unaffected (mm) ± ± ± ± ±
6.59 5.39 5.75 5.69 2.74
Unaffected (mm) 40.97 41.50 65.57 63.06 59.68
± ± ± ± ±
4.76 4.25 7.21 6.95 3.58
p (a ¼ 0.05) 0.023 0.652 0.351 0.002 0.030
p (a ¼ 0.05) 0.923 0.849 0.004 <0.001 0.610
Table 14 Distances from certain points to plane 2 in the mild group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
7.96 ± 1.29 9.37 ± 1.89 17.45 ± 2.89 24.22 ± 4.24 22.74 ± 2.49 14.83 ± 3.45
8.23 ± 1.68 10.55 ± 1.72 18.27 ± 2.54 24.16 ± 3.29 24.73 ± 3.40 14.49 ± 2.37
0.442 0.046 0.173 0.939 0.016 0.795
Table 15 Distances from certain points to plane 2 in the moderate group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
7.71 ± 1.36 9.70 ± 1.22 15.99 ± 1.66 20.95 ± 3.38 20.38 ± 2.28 13.00 ± 1.80
8.22 ± 1.23 11.26 ± 1.48 17.58 ± 1.77 23.23 ± 1.87 23.16 ± 2.57 14.23 ± 2.26
0.111 <0.001 0.008 0.011 <0.001 0.075
Table 16 Distances from certain points to plane 2 in the severe group. Points to plane 2
Affected (mm)
Unaffected (mm)
p (a ¼ 0.05)
Optic canal Carotid canal Foramen rotundum Foramen ovale Internal acoustic meatus Hypoglossal canal
8.09 ± 1.28 9.91 ± 1.59 16.65 ± 2.37 21.41 ± 4.56 21.09 ± 2.49 12.48 ± 1.39
7.51 ± 1.24 10.53 ± 1.57 16.84 ± 2.79 21.76 ± 2.62 22.37 ± 2.53 13.52 ± 1.92
0.002 0.036 0.632 0.590 0.002 0.020
average head circumference is 34 mm in newborns, 46 mm at 1 year, 48 mm at 2 years, and 49e50 mm at 6 years of age (Hu and Jiang, 2002; Kliegman and Nelson, 2011). So infants continue to grow quickly after 1 year old. In other words, there is a serious possibility that cranial base morphology changes as those 1-yearold patients get older. The ideal situation would be for all the patients have developed fully, resulting in relatively accurate measuring results. However, the skull may not reach its mature shape until 11e12 years old (Bastir et al., 2006). Most patients were treated at an early age to achieve the best outcome, so we failed to find enough cases in which the skull had fully developed. We therefore chose the period during which skull development is relatively slow e from the age of two years. In previous studies, deviation of the cranial base was often evaluated through the cranial base angle, which is articulated by
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Table 17 A summary of positive findings. Classification group
Mild Moderate Severe
Angles
Lengths
Distances
Pruzansky
OMENS
Pruzansky
OMENS
Pruzansky
OMENS
e MCA; PCA IA; MCA; PCA
e ACA; MCA; PCA IA; MCA; PCA
e SeP CIeP; SeP
e CreS; SeP; PeOp CIeP; SeP
CC; IAM CC; FR; FO; IAM OC; CC; IAM; HC
CC; IAM CC; FR; FO; IAM; HC OC; CC; IAM; HC
IA: intersection angle; ACA: anterior cranial angle; MCA: middle cranial angle; PCA: posterior cranial angle; CC: carotid canal; FR: foramen rotundum; FO: foramen ovale; IAM: internal acoustic meatus; HC: hypoglossal canal.
three points: 1. the foramen cecum or crista galli; 2. the tuberculum sella or anterior clinoid process; 3. the occipital protuberance (Marsh et al., 1986; Figueroa et al., 1993; Kwon et al., 2006; Kapadia et al., 2013; Kim et al., 2013; Marianetti et al., 2014; Paliga et al., 2015). However, just three points might not reflect the deviation so accurately. When researchers locate these points in the software, there will no doubt exist some degree of deviation. A small deviation may cause great bias in the angle, so we summarized the landmarks used before and defined two new planes: one (defined by the crista galli, anterior clinoid process, and foramen cecum) as the middle axle of the anterior cranial fossa; the another (articulated by the anterior clinoid process, occipital protuberance, and occipital protuberance) as the middle axle of the middle and posterior cranial fossa. The intersection angle is used to estimate the cranial base deviation, theoretically with fewer error values than those caused by human factors. Measurements were carried out on the basis of both the Pruzansky and OMENS classifications, which increased credibility. In the moderate and severe groups, the middle and posterior cranial angles were statistically significant, and the CIeP and SeP lengths were clearly shorter on the affected side, which implied growth restriction on the affected side, especially in the posterior fossa. Such landmarks as the carotid canal and internal acoustic canal can also be considered as reference points. Asymmetry in the morphology of the cranial base between affected and unaffected sides shows clearly that the cranial base is not spared in HFM. It seems that the more severe the HFM is, the more changes there are in cranial base morphology. This cranial base morphology change may be in direct proportion to HFM severity as judged by a Pruzansky/OMENS classification. Our study first revealed that the cranial base may be part of the hemifacial microsomia, and that it is derived from the first branchial arch (Sadler and Langman, 2000). Using a pairwise correlation method, we showed that the orbit, mandible, and soft tissues were associated in terms of degree of severity, which was consistent with a previous meta-analysis (Gougoutas et al., 2007), and they were also mainly developed from the first branchial arch (Poswillo, 1988). In other words, the cranial base, orbit, mandible, and soft tissues are of the same origin. The positive results for cranial base variation in HFM may help to verify the hypothesis that HFM is caused by an abnormity during the migration and development of the first branchial arch, especially by the expanding hematoma arising from the stapedial artery disruption (Mao and Nah, 2004). As reported by Murray et al. (1984), the spheno-occipital synchondrosis (SOS), which is located between the sphenoid and occipital bones, is primarily responsible for the growth of the cranial base and all facial skeletal structures, including the mandible. It seems to be the only growth plate that remains functional in the cranial base until adolescence in humans. The SOS may therefore be the origin of HFM. No existing classifications of HFM involve the cranial base. The Pruzansky classification only concentrates on mandibular deformities, while the OMENS classification also pays little attention to the cranial base. A new item e ‘cranial base’ e might as well be
added into the OMENS classification but, before that can happen, a lot of further research needs to be carried out to verify this. This study has some limitations. The number of inclusive patients was not big enough to eliminate sampling error. In an ideal situation, there should be more subjects, of a similar age, to reduce the influence of age and corresponding growth and development. In our study, compared with the reported gender ratio (male:female ¼ 3:2) (Murray et al., 1984), the boys far outnumbered the girls (male:female ¼ 46:20), which may be due to the small sample size or to a traditional preference for male heirs in some areas of China. Although no significant gender effects on differences in cranial base measurements have been uncovered, whether this sex inequality will influence the results remains unknown. 5. Conclusions The cranial base is involved in HFM. We found significant differences in the intersection angle, middle angle, and posterior cranial base angle, as well as the CIeP and SeP lengths, in moderate and severe HFM. Landmarks such as the carotid canal and internal acoustic canal could be considered as references. It may help to verify the hypothesis of pathogenesis, and offer a new classification option. Financial disclosure statement Financial support was provided by National Natural Science Foundation of China (No. 81372097), The Shanghai Committee of Science and Technology, China (No. 14441900800, No. 14441900802), Project of Shanghai Jiao Tong University Medical and Engineering Cross Fund (YG2014MS06). The three years' plan of promoting Municipal Hospital's Clinical Skill and Innovation (16CR2010A). The authors have no financial interest in any of the products or devices mentioned in this article. Authors' contributions Xiaojun Chen, M.D. Analysis and interpretation of the data, draft the article. Aung M. Zin, M.D. Acquisition of the data and measurements. Li Lin, M.D. Acquisition of the data. Yu Xin, M.D. Acquisition of the data. Wei Chen, M.D. Completion of the Measurement. Wenqing Han, M.D. Completion of the Measurement. Yan Zhang, M.D. The overall arrangements and revision of the article. Gang Chai, M.D. Design the implementation plane. Xianxian Yang, M.D. Guidance of the task and revision of the article. Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.jcms.2017.12.008.
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Please cite this article in press as: Chen X, et al., Three-dimensional analysis of cranial base morphology in patients with hemifacial microsomia, Journal of Cranio-Maxillo-Facial Surgery (2017), https://doi.org/10.1016/j.jcms.2017.12.008