Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 43e47
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Influence of different palate repair protocols on facial growth in unilateral complete cleft lip and palate Xue Xu a, Hyuk-Jae Kwon b, Bing Shi a, Qian Zheng a, Heng Yin a, Chenghao Li a, * a b
Department of Oral and Maxillofacial Surgery, West China College of Stomatology, Sichuan University, Chengdu, People's Republic of China Division of Anatomy and Developmental Biology, Department of Oral Biology, Yonsei University College of Dentistry, Seoul, 120-752, Republic of Korea
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 29 May 2014 Accepted 13 October 2014 Available online 25 October 2014
Objective: To address the question of whether one- or two-stage palatal treatment protocol has fewer detrimental effects on craniofacial growth in patients aged 5 years with unilateral complete cleft lip and palate. Materials and methods: Forty patients with non-syndromic unilateral complete cleft lip and palate (UCCLPs) who had received primary cleft lip repair at age 6e12 months and cleft palate repair at age 18e30 months were selected in this study. Eighteen UCCLP patients who received two-stage palate repair were selected as group 1, and 22 UCCLP patients who received one-stage palate repair were selected as group 2. The control group consisted of 20 patients with unilateral incomplete cleft lip (UICL patients) whose age and gender matched with UCCLP patients. A one-sample KolmogoroveSmirnov test was used to analyze the nature of data distribution. Bonferroni test and KruskaleWallis H tests were used for multiple comparisons. Results: Both case groups showed reduced maxillary sagittal length (ANS-PMP, A-PM, p < 0.05) and retrusion of the maxilla (S-Ptm, p < 0.05), A point and ANS point (Ba-N-A, Ba-N-ANS, p < 0.05). Patients treated with two-stage palate repair had a reduced posterior maxillary vertical height (R-PMP, p < 0.05). Conclusions: Our results indicated that maxillary sagittal length and position could be perturbed by both one- and two-stage palate repair. Vomer flap repair inhibited maxilla vertical growth. Delayed hard palate repair showed less detrimental effects on maxillary growth compared to early hard palate repair in UCCLP patients aged 5 years. © 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Cleft palate Facial skeleton growth One-stage palate repair Two-stage palate repair Vomer flap
1. Introduction In order to minimize maxillary growth restriction and achieve normal speech, many different protocols have been proposed to treat patients with cleft lip and/or palate (Neiva et al., 2014). One-stage palate repair was widely performed until Gillies and Fry (Fry, 1921; Gillies and Fry, 1921) proposed a two-stage palate repair (closing the soft palate initially and obturating the hard palate until delayed palatoplasty was performed) almost a century ago. Schweckendiek and Doz (1978) has used the two-stage palate repair protocol since 1939 and has observed excellent facial growth in patients. Similar results were reported by groups in Zürich (Hotz €teborg (Friede and et al., 1978; Hotz and Gnoinski, 1979) and Go * Corresponding author. Department of Oral and Maxillofacial Surgery, West China College of Stomatology, Sichuan University, No. 14, Section 3, Ren Min Nan Road, Chengdu, 610041, People's Republic of China. E-mail addresses: [email protected] (X. Xu), [email protected] (C. Li).
Enemark, 2001; Lilja et al., 2006), achieving sufficient facial growth as well, although the timing of hard palate repair was different (patients were 12e14 years old in the Schweckendiek group, 7 years old in the Zürich group and 9 years old in the € teborg group). The Gillies-Fry protocol was widely used in the Go United States (Dingman and Grabb, 1971; Blocksma et al., 1975) in the 1970s, but this treatment protocol lost most of its attraction after criticism from speech pathologists (Cosman and Falk, 1980; Witzel et al., 1984). Chang Gung Craniofacial Center developed this protocol during 1978e1982. They repaired the soft palate in patients at 1 year of age and obturated the hard palate until it was repaired at 6 years of age. However, Chang Gung Craniofacial Center abandoned this protocol in 1982 because of poor speech articulation (Noordhoff et al., 1987; Gosain, 2010). When it comes to two-stage palate repair, most surgeons consider repairing the soft palate initially and obturating the hard palate with a speech prosthesis until delayed hard palate repair is performed (Zemann et al., 2007, 2011). Few surgeons consider
http://dx.doi.org/10.1016/j.jcms.2014.10.007 1010-5182/© 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
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X. Xu et al. / Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 43e47
repairing the hard palate initially and the soft palate later (Swennen et al., 2002). This study aimed to evaluate which palatal treatment protocol (two-stage palate repair associated with hard palate repair initially or one-stage palate repair) has less effect on craniofacial growth in patients with unilateral complete cleft lip and palate aged 5 years. 2. Materials and methods Patients in this study were selected according to the following inclusion criteria: (1) non-syndromic complete unilateral cleft lip, palate and alveolar ridge without Simonart's band; (2) Han Chinese patients from southwestern China; (3) treatment with both primary cleft lip and palate repair at the West China Hospital of Stomatology, People's Republic of China, during 2005e2009; (4) treatment with cheiloplasty at 6e12 months of age; (5) treatment with palatoplasty according to one- or two-stage palatoplasty at 18e30 months of age; (6) lateral cephalometric radiograph of patients taken at 5e6 years old; (7) no treatment with other surgeries besides cleft lip and palate repair; (8) no preoperative or postoperative orthodontic treatment; (9) no family history or trauma history in the craniofacial area. The study protocol was appraised and approved by the Research Subject Review Board and Ethical Scientific Board of Sichuan University. Informed consent was obtained from all patients or their parents. Included patients were classified into two groups according to palatal treatment protocol (Table 1). Patients who received twostage palate repair were classified as group 1, whose cleft lip and hard palate were closed initially with the vomer flap at 6e12 months of age and soft palate was closed later by the Sommerlad surgical method at 18e30 months of age. Patients who received one-stage palate repair were classified as group 2, whose soft and hard palates were closed by the Sommerlad surgical method at 18e30 months of age. The control group, group 3, was composed of 20 patients with unilateral incomplete cleft lip only (UICL patients) whose age and gender matched with patients with unilateral complete cleft lip and palate (UCCLPs). UICL patients were selected according to the criteria below: (1) Han Chinese; (2) treatment with cheiloplasty at 6e12 months of age; (3) no treatment with any other surgeries besides cheiloplasty; (4) no orthodontic treatments; (5) no family history or trauma history in the craniofacial area. Sample distribution is shown in Table 2. All radiographs were taken by the same professional radiologist using the same equipment. All cephalometric radiographs were obtained with patients positioned in a standardized upright posture with the transporionic axis and Frankfort plane parallel to the floor and their mandible positioned in centric occlusion
(Grummons and Kappeyne, 1987; Nollet et al., 2008). All measurements were traced and measured by two researchers using Winceph 7.0 cephalometric software (Rise Corporation, Sendai, Japan). Tracing was performed twice, with a two-week interval. Intra- and inter-investigator reliability were assessed within 15 randomly selected subjects, and intra-class correlation coefficients (ICC) and kappa index were both above 0.9 in all measurements, suggesting satisfactory level. Mean values were used for analysis. The constructed landmarks used in this study were traced according to Ross (1987). Anatomic landmarks used are shown in Fig. 1. Planes analyzed are shown in Fig. 2. Measurements used, including 13 linear measurements, 11 angular measurements and 2 ratio measurements, are shown in Table 3. The posterior nasal spine (PNS) was not included in the measurements because it was not clear enough in cleft patients to be included for evaluation (Yamanishi et al., 2011). Statistical analysis was performed by using the SPSS 13.0 software package. A one-sample KolmogoroveSmirnov test was used to test the nature of data distribution. Bonferroni test and KruskaleWallis H tests were used for multiple comparisons. Significant differences were defined at 95% level.
Table 1 Treatment history of samples. Age
Group 1
Group 2
Group 3
Cheilotoplasty þ vomer Cheilotoplasty only Cheilotoplasty flap repair 12e24 months Hard palate repair Hard and soft palate none repair 3e6 months
Table 2 Sample distribution. Gender
Group 1
Group 2
Group 3
Male Female Total Mean age (years)
13 5 18 5.43 ± 0.10
15 7 22 5.59 ± 0.12
15 5 20 5.79 ± 0.15
Fig. 1. Landmarks traced on lateral cephalometric radiographs. S (Sella) ¼ midpoint of sella turcica determined by inspection; N (Nasion) ¼ most anterior part of nasofrontal suture; Or (Orbitale) ¼ most inferior point on infra-orbital margin; Po (Porion) ¼ superior border of external auditory meatus; ANS (anterior nasal spine) ¼ most anterior point on nasal spine; PNS (posterior nasal spine) ¼ most posterior point on nasal plane; A ¼ point of the greatest concavity of the alveolar process of the maxilla; B ¼ point of the greatest concavity of the alveolar process of the mandible; Ba (basion) ¼ median point of anterior margin of foramen magnum; Go (gonion) ¼ most inferior and posterior point at angle formed by ramus and body of mandible; Ar (articular) ¼ point of intersection between shadow of zygomatic arch and posterior border of mandibular ramus; Pog (pogonion) ¼ most anterior point on bony chin; Gn (gnathion) ¼ point on symphysis between pogonion and menton farthest from condyle; Me (menton) ¼ most inferior point on midsagittal plane of symphysis of mandible; R (registration point) ¼ point of crossing of greater wing of sphenoid and planium sphenoidale; PMP (posterior maxillary point) ¼ constructive created by dropping perpendicular line to maxillary plane from pterygomaxillary fissure; ptm (pterygomaxillary fissure) ¼ inferior point in fissure.
X. Xu et al. / Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 43e47
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Fig. 3. Craniofacial skeleton features in unilateral complete cleft lip and palate (UCCLP) patients with two-stage palate repair. Broken line indicates group 1, whereas solid line indicates control group. Diagrams are oriented along S-Ba line and recorded at S.
Fig. 2. Planes traced on lateral cephalometric radiographs. ①SN ¼ (anterior cranial basal plane); ② PP ¼ (palatal plane); ③MP ¼ mandibular plane.
3. Results There was no significant difference when comparing gender ratio among groups. There was no significant difference when comparing measurements between males and females within each group. Therefore, data for male and female patients were combined in each group for analysis and discussion. Results in this study showed that both case groups showed decreased maxillary sagittal length (ANS-PMP, A-PMP, p < 0.05), retrusive A point and ANS point (Ba-N-A, Ba-N-ANS, p < 0.05), retroposed maxilla (S-Ptm, p < 0.05) and shallow bony pharynx depth (Ba-PMP, p < 0.05) (Figs. 3 and 4). Patients who received twostage palate repair showed decreased posterior maxillary height (RPMP, p < 0.05). Anterior facial height (ANS-Me, p > 0.05), full and lower facial height (N-ANS, N-Me, p > 0.05) and anterior facial height to full facial height ratio (N-ANS/ANS-Me, p > 0.05) showed no significant difference between the case and control groups. Mandible morphology likewise showed no significant difference between the case and control groups. Statistical results are shown in Table 4.
at 3 months of age and repairing the soft palate at 18 months of age) showed a retrusive maxilla and mandible, and reduced posterior facial height (Semb, 1991). Among 6 European centers, patients treated in the Oslo center were considered to gain the best facial morphology (Mølsted et al., 1992). Del Guercio et al. (2010) compared to patients treated in the Oslo center and the Milan center (Milan center repaired the lip, nose and soft palate at 4e6 months and performed gingivoalveoloplasty and hard palate repair at 18e36 months, and 60 percent of its patients received presurgical orthodontic treatment), finding that no significant difference was observed between the two centers in patients at age 5 years. Patients repaired the soft palate at 6e10 months of age, and the hard palate at 4e6 years of age showed a severe growth impairment of the midface (Gaggl et al., 2003). These data showed that patients who received two-stage palate repair were associated with reduced posterior facial height (R-PMP), reduced sagittal maxilla length (A-PMP, ANS-PMP), retrusive A point and ANS point (Ba-NA, Ba-N-ANS, S-N-ANS), retroposed maxilla (S-Ptm), and disordered facial height ratio (R-PMP/N-ANS), which is similar to results of the study by Semb cited earlier. The main purpose of closing the hard palate initially is to turn complete the cleft palate into an incomplete cleft palate, to reduce the releasing incision around maxillary tuberosity, and consequently to reduce the detrimental effects on craniofacial growth in cleft palate patients. In this study, closing the hard palate initially
4. Discussion Previous studies have been conflicting and confusing about palatal treatment protocols with regard to both techniques used and the timing of repair. Patients treated with the Oslo treatment protocol (closing cleft lip and hard palate with a one-layer vomer flap simultaneously without any presurgical orthodontic treatment Table 3 Measurements analyzed in this study. 13 Linear measurements (mm) 11 Angular measurements (degrees) S-N, S-Ba, N-Ba, N-ANS, N-Me, ANS-Me, ANS-PMP, PMP-A, R-PMP, S-Ptm, Pog-Go, Ar-Go, Ba-PMP
2 Ratio measurements
N-ANS/N-Me, Ba- S-N, SNA, SNB, ANB, Ba-N-ANS, Ba-N-A, Ar-Go-Me, R-PMP/N-ANS S-N-ANS, S-N-Pog, MP-SN, SN-PP
Fig. 4. Craniofacial skeleton features in unilateral complete cleft lip and palate (UCCLP) patients with one-stage palate repair. Broken line indicates group 2, whereas solid line indicates control group. Diagrams are oriented along S-Ba line and recorded at S.
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X. Xu et al. / Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 43e47
Table 4 Statistical descriptions of all the measurements and results of statistical analysis. Variables
G1
Cranial base N-S (mm) 55.78 ± 1.79 N-Ba (mm) 81.84 ± 2.17 S-Ba (mm) 33.96 ± 2.18 Ba-S-N ( ) 130.31 ± 5.72 Liner measurements (mm) ANS-Me 52.90 ± 4.52 N-ANS 41.17 ± 2.95 N-Me 94.07 ± 5.30 S-Ptm 13.18 ± 1.96 Pog-Go 56.48 ± 3.30 Ar-Go 34.03 ± 3.14 R-PMP 33.68 ± 3.40 Ba-PMP 32.38 ± 1.92 PMP-ANS 37.89 ± 2.91 PMP-A 37.70 ± 2.91 Angular measurements ( ) :SNA 76.96 ± 3.46 :SNB 75.78 ± 3.21 :ANB 1.19 ± 3.74 Ba-N-ANS 58.88 ± 3.24 Ba-N-A 58.54 ± 3.10 S-N-ANS 77.29 ± 3.66 S-N-Pog 75.22 ± 3.30 SN-PP 13.84 ± 4.47 MP-SN 36.87 ± 6.02 Ar-Go-Me 124.22 ± 5.28 Proportions (%) N-ANS/N-Me 0.42 ± 0.04 R-PMP/N-ANS 0.82 ± 0.07
G2
G3
G1 vs G2
G1 vs G3
G2 vs G3
54.86 81.40 34.61 129.74
± ± ± ±
2.78 4.38 2.51 5.28
57.45 83.71 34.43 129.78
± ± ± ±
2.64 3.89 2.52 5.07
NS NS NS NS
NS NS NS NS
** NS NS NS
54.47 39.89 94.34 12.56 56.46 32.22 35.09 32.24 38.84 38.57
± ± ± ± ± ± ± ± ± ±
3.04 1.92 3.68 2.01 3.58 2.93 1.97 2.77 3.12 3.40
53.52 40.32 93.84 15.03 57.55 35.18 36.21 34.75 41.26 40.04
± ± ± ± ± ± ± ± ± ±
3.03 2.58 4.48 2.53 4.28 3.65 2.36 2.83 2.36 2.40
NS NS NS NS NS NS NS NS NS NS
NS NS NS * NS NS * * ** *
NS NS NS ** NS * NS ** * *
79.22 75.69 3.51 60.66 60.15 79.72 74.88 12.75 38.62 125.61
± ± ± ± ± ± ± ± ± ±
3.86 3.68 3.50 3.66 3.54 3.82 3.77 3.92 5.46 6.47
81.45 75.82 5.65 64.63 63.01 83.07 75.16 11.93 36.48 123.58
± ± ± ± ± ± ± ± ± ±
4.70 3.18 3.32 3.72 3.58 4.69 3.33 3.05 5.77 6.78
NS NS NS NS NS NS NS NS NS NS
** NS ** ** ** ** NS NS NS NS
NS NS NS ** * * NS NS NS NS
0.42 ± 0.03 0.90 ± 0.08
NS NS
NS *
NS NS
0.41 ± 0.02 0.88 ± 0.07
*The mean difference is significant at the 0.05 level. **The mean difference is significant at the 0.01 level.
does turn complete cleft palate into incomplete cleft palate, but fails to diminish the detrimental effects on maxillary growth. In fact, the effects are larger than those observed with the one-stage palate repair in patients aged 5 years. The essential point is the timing of hard palate repair rather than the sequencing of hard and soft palate repair (Liao et al., 2010). Mommaerts et al. (2006) and Richard et al. (2006) demonstrated that there was no difference between one- and two-stage palate repair because the timing of hard palate repair was similar. Treatment protocols for hard cleft palate have a significant influence on craniofacial growth and development (Kulewicz and Dudkiewicz, 2010), while Swennen et al. (2002); Rohrich et al. (2000) and Zemann et al. (2011) demonstrated that no significant difference was found in maxillary growth between patients treated with early and delayed hard palate closure. Ross (1987) confirmed that variations in the timing of hard and soft palate repair within the first decade do not influence midfacial growth in the sagittal dimension. However, in our previous study, we came to a different conclusion (Xu et al., 2012). Rohrich et al. (2000) demonstrated that surgery itself, not the timing of palatoplasty, may cause deformity. Pichler (1926) introduced vomer flap into cleft palate repair in 1926, and a high incidence of maxillary retrusion and high fistula rate were reported later (Friede and Johanson, 1977; Mølsted et al., 1987). However, similar problems have not been found in the modified vomer flap (dissecting the nasal septal mucosa close to the cleft margin with limited dissection to allow adequate closure of the nasal mucosa) (Leow and Lo, 2008). Patients in Aarhus, Denmark, received hard palate repair with vomer flap at 3 months of age and soft palate repair with push-back method at 22 months of age. €teborg center When compared with patients treated in the Go (closing the cleft lip and soft palate at 6e8 months of age and the €teborg hard palate at 15e18 months of age), patients in the Go
center gained better midfacial growth, and fewer of them needed surgical maxillary advancement later (Friede and Enemark, 2001). Vomer flap performed in this study was done according to the modified method mentioned above. Patients treated with onestage palate repair showed a reduced maxillary sagittal length. Patients treated with two-stage palate repair showed both reduced maxillary sagittal length and decreased posterior vertical dimension. Swennen et al. (2002), (2004) also observed reduction in maxillary vertical height, and Hannover and Malek group reported excellent anteroposterior maxillary morphology and a more open mandible, patients in both groups being treated with vomer flaps. Maxilla growth occurs in both the sutures and the periosteal lining (Friede, 1978, 1988). The scar in the maxillaryevomerine suture adheres the vomer to the palatal shelves and alters the vertical growth of the hard palate and the maxilla. These adhesions were distantly, superiorly positioned (Delaire and Precious, 1985). The resulting scar may inhibit or even prevent normal sliding of the vomer along the maxilla, in turn perturbing the balanced reconciliation of maxillary forward growth, nasal septum growth, and downward and forward growth of the lost vomer (Delaire and Precious, 1985, 1987); as a result, the vertical and sagittal growth of maxilla is reduced. Tanino et al. (Tanino et al., 1997a, 1997b) compared two groups of patients treated with different procedures (the hard palate was repaired with a vomer flap covered with a fullthickness skin graft in the first group and by a push-back of mucoperiosteal flaps in the second group), and found that the first group displayed satisfactory maxillary growth due to the absence of remaining denuded bone and less formation of palatal scar. Barutca et al. (2014) came to the same conclusion. Therefore, decreased maxillary vertical growth results from the scar in the maxillaryevomerine suture (Friede and Johanson, 1977; Mølsted et al., 1987).
X. Xu et al. / Journal of Cranio-Maxillo-Facial Surgery 43 (2015) 43e47
5. Conclusions Both one- and two-stage palate repair inhibited maxillary sagittal growth. Vomer flap repair inhibited both sagittal and vertical growth of the maxilla. Denuded bone resulting from vomer flap repair inhibited maxillary vertical growth. Delayed hard palate repair showed fewer detrimental effects on maxillary growth compared to early hard palate repair in patients at age 5 years. Final evaluation should be delayed until the growth of the facial skeleton is complete. Source of funding There was no source of support in any form of grants for this study. References Barutca SA, Aksan T, Uscetin I, Sahin D, Akan M: Effects of palatine bone denudation repair with periosteal graft on maxillary growth: an experimental study in rats. J Craniomaxillofac Surg 42: 1e7, 2014 Blocksma R, Leuz CA, Mellerstig KE: A conservative program for managing cleft palates without the use of mucoperiosteal flaps. Plast Reconstr Surg 55: 160e169, 1975 Cosman B, Falk AS: Delayed hard palate repair and speech deficiencies: a cautionary report. Cleft Palate J 17: 27e33, 1980 Del Guercio F, Meazzini MC, Garattini G, Morabito A, Semb G, Brusati R: A cephalometric intercentre comparison of patients with unilateral cleft lip and palate at 5 and 10years of age. Eur J Orthod 32: 24e27, 2010 Delaire J, Precious D: Avoidance of the use of vomerine mucosa in primary surgical management of velopalatine clefts. Oral Surg, Oral Med, Oral Pathol 60: 589e597, 1985 Delaire J, Precious D: Interaction of the development of the nasal septum, nasal pyramid and the face. Int J Pediatr Otorhinolaryngol 12: 311e326, 1987 Dingman RO, Grabb WC: A rational program for surgical management of bilateral cleft lip and cleft palate. Plast Reconstr Surg 47: 239e242, 1971 Friede H, Johanson B: A follow-up study of cleft children treated with vomer flap as a part of a three-stage soft tissue surgical procedure. Facial morphology and dental occlusion. Scand J Plast Reconstr Surg 11: 45e57, 1977 Friede H: The vomer-premaxillary suture-a neglected growth site in midfacial development of unilateral cleft lip and palate patients. Cleft Palate J 15: 398e403, 1978 Friede H: Growth sites and growth mechanisms at risk in cleft lip and palate. Acta Odontol Scand 56: 346e351, 1988 Friede H, Enemark H: Long-term evidence for favorable midfacial growth after delayed hard palate repair in UCLP patients. Cleft Palate J 38: 323e329, 2001 Fry WK: The dental aspect of the treatment of congenital cleft palates. Proc R Soc Med (Odontol Sect) 14: 57e68, 1921 Gaggl A, Schultes G, Feichtinger M, Santler G, Mossbock R, Karcher H: Differences in cephalometric and occlusal outcome of cleft palate patients regarding different surgical techniques. J Craniomaxillofac Surg 31: 20e26, 2003 Gillies HD, Fry WK: A new principle in the surgical treatment of “congenital cleft palate” and its mechanical counterpart. Br Med J 5: 335e338, 1921 Gosain AK: Discussion: two-stage palate repair with delayed hard palate closure is related to favorable maxillary growth in unilateral cleft lip and palate. Plast Reconstr Surg 125: 1511e1513, 2010 Grummons DC, Kappeyne MA: A frontal asymmetry analysis. J Clin Orthod 21: 448e546, 1987 Hotz MM, Gnoinski WM, Nussbaumer H, Kistler E: Early maxillary orthopedics in CLP cases: guidelines for surgery. Cleft Palate J 15: 405e411, 1978 Hotz MM, Gnoinski WM: Effects of early maxillary orthopaedics in coordination with delayed surgery for cleft lip and palate. J Maxillofac Surg 7: 201e210, 1979 Kulewicz M, Dudkiewicz Z: Craniofacial morphological outcome following treatment with three different surgical protocols for complete unilateral cleft lip and palate: a preliminary study. Int J Oral Maxillofac Surg 39: 122e128, 2010 Leow AM, Lo LJ: Palatoplasty: evolution and controversies. Chang Gung Med J 31: 335e345, 2008
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Influence of different palate repair protocols on facial growth in unilateral complete cleft lip and palate Xue Xu a, Hyuk-Jae Kwon b, Bing Shi a, Qian Zheng a, Heng Yin a, Chenghao Li a, * a b
Department of Oral and Maxillofacial Surgery, West China College of Stomatology, Sichuan University, Chengdu, People's Republic of China Division of Anatomy and Developmental Biology, Department of Oral Biology, Yonsei University College of Dentistry, Seoul, 120-752, Republic of Korea
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 29 May 2014 Accepted 13 October 2014 Available online 25 October 2014
Objective: To address the question of whether one- or two-stage palatal treatment protocol has fewer detrimental effects on craniofacial growth in patients aged 5 years with unilateral complete cleft lip and palate. Materials and methods: Forty patients with non-syndromic unilateral complete cleft lip and palate (UCCLPs) who had received primary cleft lip repair at age 6e12 months and cleft palate repair at age 18e30 months were selected in this study. Eighteen UCCLP patients who received two-stage palate repair were selected as group 1, and 22 UCCLP patients who received one-stage palate repair were selected as group 2. The control group consisted of 20 patients with unilateral incomplete cleft lip (UICL patients) whose age and gender matched with UCCLP patients. A one-sample KolmogoroveSmirnov test was used to analyze the nature of data distribution. Bonferroni test and KruskaleWallis H tests were used for multiple comparisons. Results: Both case groups showed reduced maxillary sagittal length (ANS-PMP, A-PM, p < 0.05) and retrusion of the maxilla (S-Ptm, p < 0.05), A point and ANS point (Ba-N-A, Ba-N-ANS, p < 0.05). Patients treated with two-stage palate repair had a reduced posterior maxillary vertical height (R-PMP, p < 0.05). Conclusions: Our results indicated that maxillary sagittal length and position could be perturbed by both one- and two-stage palate repair. Vomer flap repair inhibited maxilla vertical growth. Delayed hard palate repair showed less detrimental effects on maxillary growth compared to early hard palate repair in UCCLP patients aged 5 years. © 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Cleft palate Facial skeleton growth One-stage palate repair Two-stage palate repair Vomer flap
1. Introduction In order to minimize maxillary growth restriction and achieve normal speech, many different protocols have been proposed to treat patients with cleft lip and/or palate (Neiva et al., 2014). One-stage palate repair was widely performed until Gillies and Fry (Fry, 1921; Gillies and Fry, 1921) proposed a two-stage palate repair (closing the soft palate initially and obturating the hard palate until delayed palatoplasty was performed) almost a century ago. Schweckendiek and Doz (1978) has used the two-stage palate repair protocol since 1939 and has observed excellent facial growth in patients. Similar results were reported by groups in Zürich (Hotz €teborg (Friede and et al., 1978; Hotz and Gnoinski, 1979) and Go * Corresponding author. Department of Oral and Maxillofacial Surgery, West China College of Stomatology, Sichuan University, No. 14, Section 3, Ren Min Nan Road, Chengdu, 610041, People's Republic of China. E-mail addresses: [email protected] (X. Xu), [email protected] (C. Li).
Enemark, 2001; Lilja et al., 2006), achieving sufficient facial growth as well, although the timing of hard palate repair was different (patients were 12e14 years old in the Schweckendiek group, 7 years old in the Zürich group and 9 years old in the € teborg group). The Gillies-Fry protocol was widely used in the Go United States (Dingman and Grabb, 1971; Blocksma et al., 1975) in the 1970s, but this treatment protocol lost most of its attraction after criticism from speech pathologists (Cosman and Falk, 1980; Witzel et al., 1984). Chang Gung Craniofacial Center developed this protocol during 1978e1982. They repaired the soft palate in patients at 1 year of age and obturated the hard palate until it was repaired at 6 years of age. However, Chang Gung Craniofacial Center abandoned this protocol in 1982 because of poor speech articulation (Noordhoff et al., 1987; Gosain, 2010). When it comes to two-stage palate repair, most surgeons consider repairing the soft palate initially and obturating the hard palate with a speech prosthesis until delayed hard palate repair is performed (Zemann et al., 2007, 2011). Few surgeons consider
http://dx.doi.org/10.1016/j.jcms.2014.10.007 1010-5182/© 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
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repairing the hard palate initially and the soft palate later (Swennen et al., 2002). This study aimed to evaluate which palatal treatment protocol (two-stage palate repair associated with hard palate repair initially or one-stage palate repair) has less effect on craniofacial growth in patients with unilateral complete cleft lip and palate aged 5 years. 2. Materials and methods Patients in this study were selected according to the following inclusion criteria: (1) non-syndromic complete unilateral cleft lip, palate and alveolar ridge without Simonart's band; (2) Han Chinese patients from southwestern China; (3) treatment with both primary cleft lip and palate repair at the West China Hospital of Stomatology, People's Republic of China, during 2005e2009; (4) treatment with cheiloplasty at 6e12 months of age; (5) treatment with palatoplasty according to one- or two-stage palatoplasty at 18e30 months of age; (6) lateral cephalometric radiograph of patients taken at 5e6 years old; (7) no treatment with other surgeries besides cleft lip and palate repair; (8) no preoperative or postoperative orthodontic treatment; (9) no family history or trauma history in the craniofacial area. The study protocol was appraised and approved by the Research Subject Review Board and Ethical Scientific Board of Sichuan University. Informed consent was obtained from all patients or their parents. Included patients were classified into two groups according to palatal treatment protocol (Table 1). Patients who received twostage palate repair were classified as group 1, whose cleft lip and hard palate were closed initially with the vomer flap at 6e12 months of age and soft palate was closed later by the Sommerlad surgical method at 18e30 months of age. Patients who received one-stage palate repair were classified as group 2, whose soft and hard palates were closed by the Sommerlad surgical method at 18e30 months of age. The control group, group 3, was composed of 20 patients with unilateral incomplete cleft lip only (UICL patients) whose age and gender matched with patients with unilateral complete cleft lip and palate (UCCLPs). UICL patients were selected according to the criteria below: (1) Han Chinese; (2) treatment with cheiloplasty at 6e12 months of age; (3) no treatment with any other surgeries besides cheiloplasty; (4) no orthodontic treatments; (5) no family history or trauma history in the craniofacial area. Sample distribution is shown in Table 2. All radiographs were taken by the same professional radiologist using the same equipment. All cephalometric radiographs were obtained with patients positioned in a standardized upright posture with the transporionic axis and Frankfort plane parallel to the floor and their mandible positioned in centric occlusion
(Grummons and Kappeyne, 1987; Nollet et al., 2008). All measurements were traced and measured by two researchers using Winceph 7.0 cephalometric software (Rise Corporation, Sendai, Japan). Tracing was performed twice, with a two-week interval. Intra- and inter-investigator reliability were assessed within 15 randomly selected subjects, and intra-class correlation coefficients (ICC) and kappa index were both above 0.9 in all measurements, suggesting satisfactory level. Mean values were used for analysis. The constructed landmarks used in this study were traced according to Ross (1987). Anatomic landmarks used are shown in Fig. 1. Planes analyzed are shown in Fig. 2. Measurements used, including 13 linear measurements, 11 angular measurements and 2 ratio measurements, are shown in Table 3. The posterior nasal spine (PNS) was not included in the measurements because it was not clear enough in cleft patients to be included for evaluation (Yamanishi et al., 2011). Statistical analysis was performed by using the SPSS 13.0 software package. A one-sample KolmogoroveSmirnov test was used to test the nature of data distribution. Bonferroni test and KruskaleWallis H tests were used for multiple comparisons. Significant differences were defined at 95% level.
Table 1 Treatment history of samples. Age
Group 1
Group 2
Group 3
Cheilotoplasty þ vomer Cheilotoplasty only Cheilotoplasty flap repair 12e24 months Hard palate repair Hard and soft palate none repair 3e6 months
Table 2 Sample distribution. Gender
Group 1
Group 2
Group 3
Male Female Total Mean age (years)
13 5 18 5.43 ± 0.10
15 7 22 5.59 ± 0.12
15 5 20 5.79 ± 0.15
Fig. 1. Landmarks traced on lateral cephalometric radiographs. S (Sella) ¼ midpoint of sella turcica determined by inspection; N (Nasion) ¼ most anterior part of nasofrontal suture; Or (Orbitale) ¼ most inferior point on infra-orbital margin; Po (Porion) ¼ superior border of external auditory meatus; ANS (anterior nasal spine) ¼ most anterior point on nasal spine; PNS (posterior nasal spine) ¼ most posterior point on nasal plane; A ¼ point of the greatest concavity of the alveolar process of the maxilla; B ¼ point of the greatest concavity of the alveolar process of the mandible; Ba (basion) ¼ median point of anterior margin of foramen magnum; Go (gonion) ¼ most inferior and posterior point at angle formed by ramus and body of mandible; Ar (articular) ¼ point of intersection between shadow of zygomatic arch and posterior border of mandibular ramus; Pog (pogonion) ¼ most anterior point on bony chin; Gn (gnathion) ¼ point on symphysis between pogonion and menton farthest from condyle; Me (menton) ¼ most inferior point on midsagittal plane of symphysis of mandible; R (registration point) ¼ point of crossing of greater wing of sphenoid and planium sphenoidale; PMP (posterior maxillary point) ¼ constructive created by dropping perpendicular line to maxillary plane from pterygomaxillary fissure; ptm (pterygomaxillary fissure) ¼ inferior point in fissure.
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Fig. 3. Craniofacial skeleton features in unilateral complete cleft lip and palate (UCCLP) patients with two-stage palate repair. Broken line indicates group 1, whereas solid line indicates control group. Diagrams are oriented along S-Ba line and recorded at S.
Fig. 2. Planes traced on lateral cephalometric radiographs. ①SN ¼ (anterior cranial basal plane); ② PP ¼ (palatal plane); ③MP ¼ mandibular plane.
3. Results There was no significant difference when comparing gender ratio among groups. There was no significant difference when comparing measurements between males and females within each group. Therefore, data for male and female patients were combined in each group for analysis and discussion. Results in this study showed that both case groups showed decreased maxillary sagittal length (ANS-PMP, A-PMP, p < 0.05), retrusive A point and ANS point (Ba-N-A, Ba-N-ANS, p < 0.05), retroposed maxilla (S-Ptm, p < 0.05) and shallow bony pharynx depth (Ba-PMP, p < 0.05) (Figs. 3 and 4). Patients who received twostage palate repair showed decreased posterior maxillary height (RPMP, p < 0.05). Anterior facial height (ANS-Me, p > 0.05), full and lower facial height (N-ANS, N-Me, p > 0.05) and anterior facial height to full facial height ratio (N-ANS/ANS-Me, p > 0.05) showed no significant difference between the case and control groups. Mandible morphology likewise showed no significant difference between the case and control groups. Statistical results are shown in Table 4.
at 3 months of age and repairing the soft palate at 18 months of age) showed a retrusive maxilla and mandible, and reduced posterior facial height (Semb, 1991). Among 6 European centers, patients treated in the Oslo center were considered to gain the best facial morphology (Mølsted et al., 1992). Del Guercio et al. (2010) compared to patients treated in the Oslo center and the Milan center (Milan center repaired the lip, nose and soft palate at 4e6 months and performed gingivoalveoloplasty and hard palate repair at 18e36 months, and 60 percent of its patients received presurgical orthodontic treatment), finding that no significant difference was observed between the two centers in patients at age 5 years. Patients repaired the soft palate at 6e10 months of age, and the hard palate at 4e6 years of age showed a severe growth impairment of the midface (Gaggl et al., 2003). These data showed that patients who received two-stage palate repair were associated with reduced posterior facial height (R-PMP), reduced sagittal maxilla length (A-PMP, ANS-PMP), retrusive A point and ANS point (Ba-NA, Ba-N-ANS, S-N-ANS), retroposed maxilla (S-Ptm), and disordered facial height ratio (R-PMP/N-ANS), which is similar to results of the study by Semb cited earlier. The main purpose of closing the hard palate initially is to turn complete the cleft palate into an incomplete cleft palate, to reduce the releasing incision around maxillary tuberosity, and consequently to reduce the detrimental effects on craniofacial growth in cleft palate patients. In this study, closing the hard palate initially
4. Discussion Previous studies have been conflicting and confusing about palatal treatment protocols with regard to both techniques used and the timing of repair. Patients treated with the Oslo treatment protocol (closing cleft lip and hard palate with a one-layer vomer flap simultaneously without any presurgical orthodontic treatment Table 3 Measurements analyzed in this study. 13 Linear measurements (mm) 11 Angular measurements (degrees) S-N, S-Ba, N-Ba, N-ANS, N-Me, ANS-Me, ANS-PMP, PMP-A, R-PMP, S-Ptm, Pog-Go, Ar-Go, Ba-PMP
2 Ratio measurements
N-ANS/N-Me, Ba- S-N, SNA, SNB, ANB, Ba-N-ANS, Ba-N-A, Ar-Go-Me, R-PMP/N-ANS S-N-ANS, S-N-Pog, MP-SN, SN-PP
Fig. 4. Craniofacial skeleton features in unilateral complete cleft lip and palate (UCCLP) patients with one-stage palate repair. Broken line indicates group 2, whereas solid line indicates control group. Diagrams are oriented along S-Ba line and recorded at S.
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Table 4 Statistical descriptions of all the measurements and results of statistical analysis. Variables
G1
Cranial base N-S (mm) 55.78 ± 1.79 N-Ba (mm) 81.84 ± 2.17 S-Ba (mm) 33.96 ± 2.18 Ba-S-N ( ) 130.31 ± 5.72 Liner measurements (mm) ANS-Me 52.90 ± 4.52 N-ANS 41.17 ± 2.95 N-Me 94.07 ± 5.30 S-Ptm 13.18 ± 1.96 Pog-Go 56.48 ± 3.30 Ar-Go 34.03 ± 3.14 R-PMP 33.68 ± 3.40 Ba-PMP 32.38 ± 1.92 PMP-ANS 37.89 ± 2.91 PMP-A 37.70 ± 2.91 Angular measurements ( ) :SNA 76.96 ± 3.46 :SNB 75.78 ± 3.21 :ANB 1.19 ± 3.74 Ba-N-ANS 58.88 ± 3.24 Ba-N-A 58.54 ± 3.10 S-N-ANS 77.29 ± 3.66 S-N-Pog 75.22 ± 3.30 SN-PP 13.84 ± 4.47 MP-SN 36.87 ± 6.02 Ar-Go-Me 124.22 ± 5.28 Proportions (%) N-ANS/N-Me 0.42 ± 0.04 R-PMP/N-ANS 0.82 ± 0.07
G2
G3
G1 vs G2
G1 vs G3
G2 vs G3
54.86 81.40 34.61 129.74
± ± ± ±
2.78 4.38 2.51 5.28
57.45 83.71 34.43 129.78
± ± ± ±
2.64 3.89 2.52 5.07
NS NS NS NS
NS NS NS NS
** NS NS NS
54.47 39.89 94.34 12.56 56.46 32.22 35.09 32.24 38.84 38.57
± ± ± ± ± ± ± ± ± ±
3.04 1.92 3.68 2.01 3.58 2.93 1.97 2.77 3.12 3.40
53.52 40.32 93.84 15.03 57.55 35.18 36.21 34.75 41.26 40.04
± ± ± ± ± ± ± ± ± ±
3.03 2.58 4.48 2.53 4.28 3.65 2.36 2.83 2.36 2.40
NS NS NS NS NS NS NS NS NS NS
NS NS NS * NS NS * * ** *
NS NS NS ** NS * NS ** * *
79.22 75.69 3.51 60.66 60.15 79.72 74.88 12.75 38.62 125.61
± ± ± ± ± ± ± ± ± ±
3.86 3.68 3.50 3.66 3.54 3.82 3.77 3.92 5.46 6.47
81.45 75.82 5.65 64.63 63.01 83.07 75.16 11.93 36.48 123.58
± ± ± ± ± ± ± ± ± ±
4.70 3.18 3.32 3.72 3.58 4.69 3.33 3.05 5.77 6.78
NS NS NS NS NS NS NS NS NS NS
** NS ** ** ** ** NS NS NS NS
NS NS NS ** * * NS NS NS NS
0.42 ± 0.03 0.90 ± 0.08
NS NS
NS *
NS NS
0.41 ± 0.02 0.88 ± 0.07
*The mean difference is significant at the 0.05 level. **The mean difference is significant at the 0.01 level.
does turn complete cleft palate into incomplete cleft palate, but fails to diminish the detrimental effects on maxillary growth. In fact, the effects are larger than those observed with the one-stage palate repair in patients aged 5 years. The essential point is the timing of hard palate repair rather than the sequencing of hard and soft palate repair (Liao et al., 2010). Mommaerts et al. (2006) and Richard et al. (2006) demonstrated that there was no difference between one- and two-stage palate repair because the timing of hard palate repair was similar. Treatment protocols for hard cleft palate have a significant influence on craniofacial growth and development (Kulewicz and Dudkiewicz, 2010), while Swennen et al. (2002); Rohrich et al. (2000) and Zemann et al. (2011) demonstrated that no significant difference was found in maxillary growth between patients treated with early and delayed hard palate closure. Ross (1987) confirmed that variations in the timing of hard and soft palate repair within the first decade do not influence midfacial growth in the sagittal dimension. However, in our previous study, we came to a different conclusion (Xu et al., 2012). Rohrich et al. (2000) demonstrated that surgery itself, not the timing of palatoplasty, may cause deformity. Pichler (1926) introduced vomer flap into cleft palate repair in 1926, and a high incidence of maxillary retrusion and high fistula rate were reported later (Friede and Johanson, 1977; Mølsted et al., 1987). However, similar problems have not been found in the modified vomer flap (dissecting the nasal septal mucosa close to the cleft margin with limited dissection to allow adequate closure of the nasal mucosa) (Leow and Lo, 2008). Patients in Aarhus, Denmark, received hard palate repair with vomer flap at 3 months of age and soft palate repair with push-back method at 22 months of age. €teborg center When compared with patients treated in the Go (closing the cleft lip and soft palate at 6e8 months of age and the €teborg hard palate at 15e18 months of age), patients in the Go
center gained better midfacial growth, and fewer of them needed surgical maxillary advancement later (Friede and Enemark, 2001). Vomer flap performed in this study was done according to the modified method mentioned above. Patients treated with onestage palate repair showed a reduced maxillary sagittal length. Patients treated with two-stage palate repair showed both reduced maxillary sagittal length and decreased posterior vertical dimension. Swennen et al. (2002), (2004) also observed reduction in maxillary vertical height, and Hannover and Malek group reported excellent anteroposterior maxillary morphology and a more open mandible, patients in both groups being treated with vomer flaps. Maxilla growth occurs in both the sutures and the periosteal lining (Friede, 1978, 1988). The scar in the maxillaryevomerine suture adheres the vomer to the palatal shelves and alters the vertical growth of the hard palate and the maxilla. These adhesions were distantly, superiorly positioned (Delaire and Precious, 1985). The resulting scar may inhibit or even prevent normal sliding of the vomer along the maxilla, in turn perturbing the balanced reconciliation of maxillary forward growth, nasal septum growth, and downward and forward growth of the lost vomer (Delaire and Precious, 1985, 1987); as a result, the vertical and sagittal growth of maxilla is reduced. Tanino et al. (Tanino et al., 1997a, 1997b) compared two groups of patients treated with different procedures (the hard palate was repaired with a vomer flap covered with a fullthickness skin graft in the first group and by a push-back of mucoperiosteal flaps in the second group), and found that the first group displayed satisfactory maxillary growth due to the absence of remaining denuded bone and less formation of palatal scar. Barutca et al. (2014) came to the same conclusion. Therefore, decreased maxillary vertical growth results from the scar in the maxillaryevomerine suture (Friede and Johanson, 1977; Mølsted et al., 1987).
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5. Conclusions Both one- and two-stage palate repair inhibited maxillary sagittal growth. Vomer flap repair inhibited both sagittal and vertical growth of the maxilla. Denuded bone resulting from vomer flap repair inhibited maxillary vertical growth. Delayed hard palate repair showed fewer detrimental effects on maxillary growth compared to early hard palate repair in patients at age 5 years. Final evaluation should be delayed until the growth of the facial skeleton is complete. Source of funding There was no source of support in any form of grants for this study. References Barutca SA, Aksan T, Uscetin I, Sahin D, Akan M: Effects of palatine bone denudation repair with periosteal graft on maxillary growth: an experimental study in rats. J Craniomaxillofac Surg 42: 1e7, 2014 Blocksma R, Leuz CA, Mellerstig KE: A conservative program for managing cleft palates without the use of mucoperiosteal flaps. Plast Reconstr Surg 55: 160e169, 1975 Cosman B, Falk AS: Delayed hard palate repair and speech deficiencies: a cautionary report. Cleft Palate J 17: 27e33, 1980 Del Guercio F, Meazzini MC, Garattini G, Morabito A, Semb G, Brusati R: A cephalometric intercentre comparison of patients with unilateral cleft lip and palate at 5 and 10years of age. Eur J Orthod 32: 24e27, 2010 Delaire J, Precious D: Avoidance of the use of vomerine mucosa in primary surgical management of velopalatine clefts. Oral Surg, Oral Med, Oral Pathol 60: 589e597, 1985 Delaire J, Precious D: Interaction of the development of the nasal septum, nasal pyramid and the face. Int J Pediatr Otorhinolaryngol 12: 311e326, 1987 Dingman RO, Grabb WC: A rational program for surgical management of bilateral cleft lip and cleft palate. Plast Reconstr Surg 47: 239e242, 1971 Friede H, Johanson B: A follow-up study of cleft children treated with vomer flap as a part of a three-stage soft tissue surgical procedure. Facial morphology and dental occlusion. Scand J Plast Reconstr Surg 11: 45e57, 1977 Friede H: The vomer-premaxillary suture-a neglected growth site in midfacial development of unilateral cleft lip and palate patients. Cleft Palate J 15: 398e403, 1978 Friede H: Growth sites and growth mechanisms at risk in cleft lip and palate. Acta Odontol Scand 56: 346e351, 1988 Friede H, Enemark H: Long-term evidence for favorable midfacial growth after delayed hard palate repair in UCLP patients. Cleft Palate J 38: 323e329, 2001 Fry WK: The dental aspect of the treatment of congenital cleft palates. Proc R Soc Med (Odontol Sect) 14: 57e68, 1921 Gaggl A, Schultes G, Feichtinger M, Santler G, Mossbock R, Karcher H: Differences in cephalometric and occlusal outcome of cleft palate patients regarding different surgical techniques. J Craniomaxillofac Surg 31: 20e26, 2003 Gillies HD, Fry WK: A new principle in the surgical treatment of “congenital cleft palate” and its mechanical counterpart. Br Med J 5: 335e338, 1921 Gosain AK: Discussion: two-stage palate repair with delayed hard palate closure is related to favorable maxillary growth in unilateral cleft lip and palate. Plast Reconstr Surg 125: 1511e1513, 2010 Grummons DC, Kappeyne MA: A frontal asymmetry analysis. J Clin Orthod 21: 448e546, 1987 Hotz MM, Gnoinski WM, Nussbaumer H, Kistler E: Early maxillary orthopedics in CLP cases: guidelines for surgery. Cleft Palate J 15: 405e411, 1978 Hotz MM, Gnoinski WM: Effects of early maxillary orthopaedics in coordination with delayed surgery for cleft lip and palate. J Maxillofac Surg 7: 201e210, 1979 Kulewicz M, Dudkiewicz Z: Craniofacial morphological outcome following treatment with three different surgical protocols for complete unilateral cleft lip and palate: a preliminary study. Int J Oral Maxillofac Surg 39: 122e128, 2010 Leow AM, Lo LJ: Palatoplasty: evolution and controversies. Chang Gung Med J 31: 335e345, 2008
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