The Cleft Palate–Craniofacial Journal 52(2) pp. 210–218 March 2015 Ó Copyright 2015 American Cleft Palate-Craniofacial Association
ORIGINAL ARTICLE Optimization of Dental Status Improves Long-Term Outcome After Alveolar Bone Grafting in Unilateral Cleft Lip and Palate Fatima Jabbari, D.D.S., Valdemar Skoog, M.D., Ph.D., Eicka Reiser, D.D.S., Ph.D., Malin Hakelius, M.D., Daniel Nowinski, M.D., Ph.D. Objective: To evaluate the importance of dental status for long-term outcome after alveolar bone grafting in patients with unilateral cleft lip and palate. Design: Retrospective longitudinal study. Setting: Cleft lip and palate-craniofacial center, Uppsala University Hospital, Sweden. Patients: A total of 67 consecutive patients with unilateral complete cleft lip and palate. Interventions: Secondary alveolar bone grafting, prior to the eruption of the permanent canine, was performed at the average age of 10.0 years (range, 8.5 to 12.0 years). Main Outcome Measures: Alveolar bone height was evaluated with the modified Bergland index at 1 and 10 years after surgery. Results: Of the patients, 97% had modified Bergland index grade I and the remaining 3% had modified Bergland index grade II at 1 year after surgery. At 10 years’ follow-up, 43% showed modified Bergland index grade I; 55%, modified Bergland index grade II; and 2% (one patient), modified Bergland index grade III. The degree of dental anomalies in the cleft area, such as enamel hypoplasia, incisor rotation, incisor inclination, canine inclination, and oral hygiene registered preoperatively, all correlated negatively to the modified Bergland index at 10 years after surgery. Enamel hypoplasia (q ¼ 0.70195, P , .0001), followed by canine inclination (q ¼ 0.55429, P , .0001), showed the strongest correlation to reduced bone height in the cleft area. Conclusions: In patients with unilateral cleft lip and palate, excellent results from secondary alveolar bone grafting in terms of bone height in the alveolar cleft tend to decrease with time. This seems to be correlated with factors that might to some extent be treated preoperatively through adequate planning and execution of the orthodontic treatment. KEY WORDS:
alveolar bone grafting, cleft lip and palate, orthodontics
Secondary alveolar bone grafting (SABG) in conjunction with orthodontic treatment has evolved into an integral component in the comprehensive treatment of patients with cleft lip and palate. When performed at the end of mixed dentition, before canine eruption, SABG primarily serves to provide bony support for the permanent dentition and to
reconstruct the alveolar process (Troxell et al., 1982; Bergland et al., 1986; Kortebein et al., 1991). Other, secondary goals of this procedure are to close any remaining fistulae and to augment the hypoplastic paranasal maxilla (Boyne and Sands, 1972; Steinberg et al., 1999). Although SABG has been widely accepted, there is still some controversy regarding the timing of the procedure (Bergland et al., 1986), the extension of the grafted region into the hard palate, the flap design (Abyholm et al., 1981), and the amount of the bone that should be grafted in relation to the cleft cavity (Backdahl and Nordin, 1960). ¨ The type of bone graft, cancellous versus cortical, the site from which the bone is harvested (Freihofer et al., 1993), and the influence of orthodontic treatment prior to bone grafting (Long et al., 1995; Kindelan et al., 1997) are other topics that have been discussed. The modified Bergland index (mBI) of bone height has become the criterion standard for assessing outcome of SABG (Kindelan et al., 1997). It has been demonstrated that the outcome is affected by the surgeon’s experience and the type of bone graft used (Lilja et al., 1996), where cancellous bone is favored over cortical bone (Abyholm et al., 1981).
Dr. Jabbari is Scientist and Senior Consultant Orthodontist, Dr. Resier is Consultant Orthodontist, Department of Surgical Sciences and Department of Plastic and Maxillofacial Surgery, Uppsala University; Dr. Skoog is Senior Consultant Plastic Surgeon, Dr. Hakelius is Consultant Plastic Surgeon, Chairman of Cleft Lip and Palate Unit, and Dr. Nowinski is Consultant Plastic and Reconstructive/Craniofacial Surgeon, Chairman of Cranio-Maxillo-Facial Unit, Akademiska Hospital, Uppsala, Sweden. Dr. Nowinski is Craniofacial Surgeon, Dr. Hakelius is Craniofacial Surgeon, and Dr. Jabbari is Consultant Orthodontist, Craniofacial Center, Department of Surgical Sciences, Uppsala University, Uppsala, Sweden. Submitted May 2013; Revised August 2013, September 2013; Accepted October 2013. Address correspondence to: Dr. Fatima Jabbari, D.D.S., Department of Surgical Sciences and the Department of Plastic and Maxillofacial Surgery, Uppsala University Hospital, 751 85 Uppsala, Sweden. E-mail [email protected]. DOI: 10.1597/13-118 210
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TABLE 1
Surgical Protocol of UCLP in Uppsala*
Age 3 mo 6 mo 2y 8–10 y
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Surgery Primary lip plasty according to Skoog and primary rhinoplasty according to McComb Soft palatoplasty Two-layer hard palate closure Secondary alveolar bone grafting
* UCLP ¼ unilateral cleft lip and palate.
Cancellous bone may be harvested from the anterior iliac crest, posterior iliac crest, and tibia, with the anterior iliac crest being the most frequently practiced donor site (Beirne et al., 1996). The abnormal development of the alveolar process in the cleft area may cause hypodontia, supernumerary teeth, peg-shaped teeth, crown and root malformation, and delay in tooth formation and eruption (Ranta, 1986; Lopes et al., 1991; Suzuki and Takahama, 1992; Tsai et al., 1998; Shapira et al., 1999). It is generally accepted that these dental anomalies should be addressed in connection to the SABG procedure. However, the impact of dental anomalies as well as other dental irregularities, such as dental retention, rotation/ inclination, enamel status, and oral hygiene on the outcome of SABG is largely unknown. The aim of the present investigation was to study the impact of dental anomalies in the cleft area on the longterm outcome of secondary bone grafting in patients with unilateral cleft lip and palate (UCLP). MATERIAL
AND
METHODS
Subjects In the present retrospective study, 94 consecutive patients with UCLP who underwent secondary alveolar bone grafting between 1987 and 1997 were recruited from the database of the Cleft Lip and Palate Team, Craniofacial Center, Uppsala University Hospital, Sweden. The inclusion criteria were complete UCLP; patients were white; nonsyndromic patients; treatment according to the Uppsala protocol (Table 1); and all patients operated upon by the same surgeon (V.S.) (Fig. 1). A total of 67 patients were found to meet these criteria. Approval from the Uppsala Ethics Committee was obtained. Orthodontic Preparation and Surgery Eleven patients had a quad helix as an expansion device for the upper arch prior to SABG, 10 patients had a fixed appliance to align the rotated and inclined central incisor adjacent to the cleft, and 2 patients had received both expansion of the upper jaw and a fixed appliance. The remaining 44 patients did not receive any presurgical orthodontics.
FIGURE 1 Distribution of patients with unilateral complete cleft lip and palate.
The mean age at the time of SABG was 10.0 years (range, 8.5 to 12.0 years). The procedure was performed by the same surgeon (V.S.) in all patients. The cleft was exposed through bilateral palatal mucoperiosteal flaps and gingivoperiosteal flaps in the oral vestibulum. Deciduous teeth projecting into the cleft space were removed. The bony cleft in the hard palate was completely exposed. Great care was taken to close the nasal mucoperiosteal layer meticulously with interrupted 4.0 Vicryl sutures. Cancellous bone was harvested from the iliac crest and grafted to the entire cleft space, including the hard palate, and all the way up to the piriform aperture and as an onlay to improve the maxilla. The flaps were sutured back with interrupted 4.0 Vicryl sutures. Great care was taken to provide adequate soft tissue coverage over the bone graft. This was facilitated by scoring the periosteum over the maxilla and medializing the lateral gingivoperiosteal flap. Mean operative time was 153 6 24.5 minutes and the mean amount of bleeding was 284 6 122.3 mL. The mean hospitalization time was 6.2 6 0.81 days; this length of hospital stay was motivated by the relatively long travel distance for most of our patients. Antibiotics were administered as three doses of intravenous cefuroxime during the day of surgery. All patients were seen within 2 to 3 weeks for removal of sutures. At this point, eight (12%) patients showed slight dehiscence in the cleft space and were treated with a secondary suture. In five (7%) patients, minimal granulation tissue was noticed that did not require revision. There were no infectious complications either at the graft site or at the donor site. METHODS Alveolar Bone Height According to Bergland Anterior occlusal radiographs were available for analysis of the alveolar bone height prior to SABG 1 year postoperatively and at 10 years’ follow-up.
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¨ TABLE 2 Tooth Status Index According to Brattstrom (Brattstrom and McWilliam, 1989) Grade
Condition
0 1 2 3 4
Normal teeth Teeth requiring minor restoration Teeth requiring major restoration Teeth malformed to extent of extraction. Missing teeth
The bone formation in the grafted area was assessed according to the mBI (Bergland et al., 1986), which measures the height of the interdental septum adjacent to the erupted canine. Tooth Status Intraoral radiographs obtained prior to surgery were used to determine the tooth status of the central incisor in the cleft area according to the tooth status index. This is a grading of tooth quality previously described and used to evaluate tooth status in the cleft area (Brattstrom and McWilliam, 1989) (Table 2). Furthermore, the presence or absence of the permanent lateral incisor was evaluated and scored as follows: Grade 0, hypodontia; Grade 1, extraction at the time of bone grafting; Grade 2, late extraction (.2 years’ postSABG); Grade 3, persistent lateral incisor. Canine Inclination Inclination of the canine in the cleft area was evaluated from panoramic radiographs obtained at 8 years of age (6 0.5 months) and scored according to a scale previously described by Warford et al. (2003) and Tortora et al. (2008). The patients were stratified into three groups: Grade 0, canine inclination 08 to 158 to the perpendicular of the occlusal plane; Grade 1, canine inclination 158 to 458; and Grade 2, canine inclination .458.
Central Incisor Inclination Inclination of the central incisor on the cleft side in relation to a line perpendicular to the occlusal plane was measured on panoramic radiographs at 8 years of age (6 0.5 months) (Fig. 2). One of three scores was given: Grade 0, incisor inclination 08 to 308; Grade 1, incisor inclination 308 to 508; and Grade 2, incisor inclination .508. Central Incisor Rotation Rotation of the central incisor adjacent to the cleft was measured on dental casts at 8 years of age (6 0.5 months) (Fig. 3). Three different scores were given: Grade 0, incisor rotation 08 to 308; Grade 1, incisor rotation 308 to 508; and Grade 2, incisor rotation .508. Oral Hygiene All patients were categorized into two groups, good and poor, with respect to oral hygiene prior to SABG. This was performed by studying comments in patient charts, clinical observation, and intraoral photographs. Oral hygiene was categorized as good when there was no or limited amount of plaque and no apparent gingivitis adjacent to the cleft. All patients with clear plaque formation and gingivitis were categorized as having poor oral hygiene. All panoramic radiographs used in this study were examined by one trained consultant orthodontist (F.J.) and were analyzed a second time after 6 months. Reproducibility of Recordings The reliability and intraoperator reproducibility of the measurements/scorings were determined from randomized duplicate recordings in 20 UCLP children. Weighted kappa coefficients were calculated. The
FIGURE 2 Incisor inclination was assessed from panoramic radiographs. The inclination of the central incisor in the cleft area was given three different scores. Left panel: grade 0, incisor inclination ,308 to occlusal plane; middle panel: grade 1, incisor inclination 308 to 508 to occlusal plane; right panel: grade 2, incisor inclination .508 to occlusal plane.
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tion between cleft side lateral incisor status and the mBI scores at 10 years’ postsurgery was analyzed with a chi-square test. P values .05 were regarded as statistically significant. RESULTS Alveolar Bone Height
FIGURE 3 Incisor rotation was assessed on dental casts. The rotation of central incisor in the cleft area was given three different scores as described in the ‘‘Materials and Methods’’ section, here exemplified by grade 1 rotation.
kappa coefficients varied from .58 (moderate) to .90 (almost perfect) agreement of repeated measurements. The intraoperator reproducibility was considered good. Statistical Analysis Mean, standard deviation, median, and range were calculated for all parameters. The relation between preoperative scoring of enamel hypoplasia, oral hygiene, inclination of the canine, and inclination and rotation of the central incisor adjacent to the cleft and the mBI scores at 10 years postsurgery were analyzed with Spearman rank correlation. The rela-
FIGURE 4
At 1 year after surgery, 97% of the patients had a bone height of mBI grade I (Fig. 4) and the remaining 3%, mBI grade II. Thus, at 1 year postoperatively the radiological outcome after SABG was excellent. At 10 years after surgery the share of patients with mBI grade I had dropped to 43%; whereas, 55.0% had mBI grade II, and 2% (one patient) had mBI grade III (Fig. 4). Thus, the bone height in the alveolar cleft was reduced with time. Association Between Dental Status and Alveolar Bone Height at 10 Years After SABG Tooth Status Among the 46 patients (69%) who had enamel hypoplasia of the central incisor adjacent to the cleft area, 21 patients had grade 1 hypoplasia and 25 patients had grade 2 (Fig. 5). All patients with grade 2 enamel hypoplasia had mBI grade II, and 9 out of 21 patients with grade 1 enamel hypoplasia had mBI grade II (Fig. 5). The one patient with mBI grade III had grade 1 enamel hypoplasia. The degree of enamel hypoplasia was correlated with reduced bone height as assessed by the mBI at 10 years’ follow-up (Spearman correlation q ¼ .70195, P , .0001).
Alveolar bone height according to the modified Bergland index at 1 and 10 years after secondary alveolar bone grafting.
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FIGURE 5 Enamel hypoplasia of central incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
Lateral Incisor In 8% of the patients the permanent lateral incisor was extracted at the time of bone grafting, 31% of the patients had late extraction, 39% of the patients had hypodontia, and the remaining 22% had presence of the permanent lateral incisor. We did not find an association between late extractions of laterals and mBI at 10 years’ follow-up (P ¼ .4309). Canine Inclination Prior to bone grafting, 39 patients (58%) had grade 1 canine inclination (158 to 458), 18 (27%) patients had grade 2 canine inclination (.458), and 10 (15%) patients
FIGURE 6
had a grade 0 canine inclination (,158) (Fig. 6). There was a correlation between a high degree of canine inclination preoperatively and reduced bone height mBI (q ¼ .55429, P , .0001) after 10 years. Incisor Rotation and Inclination Preoperatively, 10 patients (15%) had grade 0 incisor rotation (08 to 308), 25 patients (37%) had grade 1 incisor rotation (.308 to 508), and 32 patients (48%) had grade 2 incisor rotation (.508). Eight patients (12%) had grade 0 incisor inclination (08 to 308), 45 patients (67%) had grade 1 incisor inclination (.308 to 508), and 14 patients (21%) had grade 2 incisor inclination (.508) preoperatively (Figs. 7 and 8).
Inclination of the canine in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
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FIGURE 7 Rotation of the incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
A high degree of both central incisor rotation (q ¼ .29123, P , .0168) and inclination (q ¼ .29430, P , .0156) in the cleft area was related to reduced bone height at 10 years’ post-SABG. Oral Hygiene Seventeen patients (25%) had poor oral hygiene, and 16 of these patients had mBI grade II. Of the 50 patients with good oral hygiene, 28 (56%) had mBI grade I; 21(42%) had mBI grade II; and one patient had mBI grade III (Fig. 9). Poor oral hygiene correlated to reduced bone height as assessed by the mBI at 10 years’ follow-up (q ¼ .41965, P , .0004). Tables 3 and 4 summarize the statistical analysis of the correlation between the above described parameters and the bone height at 10 years after SABG.
DISCUSSION Although several studies have reported good or excellent results in terms of bone height in the alveolar cleft at 1 year after SABG, this study presents long-term data on bone graft survival. Moreover, this is the first study describing how the severity of dental anomalies and status are related to long-term outcome. The surgical method for SABG was introduced at our ˚ unit in 1984 after a visit by Frank Abyholm from Oslo. Fundamentally, the surgical procedure has been maintained according to the same basic principles. We routinely perform wide exposure through both palatal and vestibular accesses and graft ample amounts of bone, filling the entire three-dimensional cleft space in the hard palate and alveolus up to the piriform aperture. The philosophy has been that a more complete approach, aiming to reconstruct the entire bony cleft, is warranted for a reliable graft take
FIGURE 8 Inclination of the incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
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FIGURE 9 Oral hygiene and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
and to predictably achieve all treatment goals: tooth support, fistula closure, and maxillary stability. We find support for this approach in the excellent 1-year results presented here, with 97% of patients having an mBI grade of I. It has previously been demonstrated that the surgeon’s experience correlates positively with outcomes after SABG. Thus, the fact that one senior plastic surgeon (V.S.) performed all SABGs in this study population is most probably another important factor behind the excellent results obtained. The importance of the orthodontist in planning, preparations, and follow-up around the SABG procedure is widely recognized. However, the negative impact of the various dental anomalies and poor oral hygiene has to our knowledge not previously been investigated. Dental anomalies occur with higher frequency in patients born with UCLP (Ranta, 1982, 1988; Shapira et al., 2000), and their importance for treatment outcomes warrants close investigation. The data presented here show that, with time, there is a gradual reduction of the grafted bone in the alveolar cleft (57% of the cases). In this study the preoperative degree of oral hygiene and enamel hypoplasia, as well as the degree of canine inclination, incisor inclination, and rotation, were shown to be related to reduced alveolar bone height after 10 years. Several studies have shown that the most common enamel alteration in patients with complete cleft lip and palate is enamel hypoplasia due to a deficiency in enamel TABLE 3
formation and absence of the enamel surface (Suckling et al., 1984; Suckling, 1989; Ellwood and O’Mullane, 1994; Seow, 1997). These defects occur mainly in teeth close to the cleft (Malanczuk et al., 1999; Maciel et al., 2005), and when affecting the central incisor, the hypoplasia has an aesthetic implication. Moreover, it increases the susceptibility to plaque accumulation and increases the risk for decay and gingivitis (Dean, 1934; Ellwood and O’Mullane, 1994; Malanczuk et al., 1999). Furthermore, correction of central incisor rotation and inclination prior to SABG facilitates oral hygiene and prevents plaque formation. Pertaining to this, a plausible explanation for the reduction in bone height could be local infection with the presence of a chronic, low-grade inflammatory process, with activated proteases degrading the grafted bone. Indeed, it is likely that such an inflammatory state would coincide with the factors that were found to be overrepresented in the group of patients with less-favorable outcomes: poor oral hygiene, enamel hypoplasia, and different types of uncorrected dental malalignment. The general complication rate was low, and thus the long-term maintenance of bone grafts in the alveolus could not be linked to earlier complications in the postoperative course. Implementation of regular maintenance therapy is important and beneficial for these patients, and bone grafting should not be performed until the gingiva is healthy (Samman et al., 1994).
Data From Scoring of Bone Height and Parameters of Dental Status
Variable
N
Mean
SD
Maximum
Median
Minimum
Modified Bergland index Enamel hypoplasia Oral hygiene Canine inclination Incisor inclination Incisor rotation
67 67 67 67 67 67
1.58 1.06 0.51 1.12 37.09 60.82
0.53 0.83 0.88 0.64 13.00 29.27
3.00 2.00 2.00 2.00 70.00 90.00
2.00 1.00 0.00 1.00 40.00 45.00
1.00 0.00 0.00 0.00 0.00 0.00
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TABLE 4
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Coefficients for the Correlation Between the Different Parameters of Dental Status and Bone Height at 10 Years After SABG
Enamel hypoplasia Oral hygiene Canine inclination Incisor inclination Incisor rotation
Correlation Coefficient
Lower 95% Confidence Limit
Upper 95% Confidence Limit
P
.70 .42 .55 .29 .29
0.55 0.20 0.36 0.05 0.05
0.80 0.60 0.70 0.50 0.50
,.0001 ,.0004 ,.0001 ,.0156 ,.0168
Impacted permanent maxillary canine occur in merely 1% to 3% of the general population (Peck et al., 1994). However, it is seen with higher frequency in the cleft lip and palate population due to canine inclination (Baccetti, 1998). Therefore, canine inclination should be anticipated in patients with cleft lip and palate before SABG and during follow-up. High degrees of canine inclination indicate risk for altered eruption and impaction. The reduction in bone height observed here, in patients with a high degree of canine inclination, underscores the importance of early diagnosis and possible need for interceptive treatment. From an orthodontic point of view, the most important benefit of secondary alveolar bone grafting is that the newly grafted bone allows for spontaneous eruption of the adjacent canine and orthodontic movement of teeth into ˚ the grafted bone (Abyholm et al., 1981; Long et al., 2000). It could, therefore, be argued that the observed bone graft reduction, from mBI grade I to mBI grade II, lacks clinical significance, as long as adequate support for the permanent dentition has been achieved. This view may be valid in the short-term perspective; however, we believe that maintaining the alveolar bone height in the cleft area is important to prevent long-term complications, such as gingival retractions and periodontitis. Moreover, maintenance of the grafted bone is important for a long-term prognosis of dental survival and especially for patients requiring dental implants. Therefore, it is highly important for the outcome to provide adequate assessment and appropriate interceptive management, entailing the identification of enamel defects and other related dental abnormalities, in order to achieve optimal dental rehabilitation prior to the SABG. In conclusion, excellent results from SABG in UCLP patients in term of bone-height in the alveolar cleft tend to deteriorate with time. This seems to be correlated to factors of dental status. It is important that some of these factors may be improved by meticulous execution of the preoperative orthodontic planning and treatment. Taken together, poor dental status was correlated with a lower bone height at 10 years’ follow-up. The strongest correlation was seen for enamel hypoplasia, followed by canine inclination. Acknowledgments. The authors would like to thank Lars Berglund, statistician, for his valuable statistical advice and calculations. We also
thank Vivecca Brattstrom ¨ for highly valuable mentorship and advice, and Andreas Svee, plastic surgery resident, for data management.
REFERENCES ˚ Abyholm FE, Bergland O, Semb G. Secondary bone grafting of alveolar clefts. A surgical/orthodontic treatment enabling a nonprosthodontic rehabilitation in cleft lip and palate patients. Scand J Plast Reconstr Surg. 1981;15:127–140. Baccetti T. Tooth rotation associated with aplasia of nonadjacent teeth. Angle Orthod. 1998;68:471–474. Backdahl M, Noedin KE. Replacement of the maxillary bone defect in ¨ cleft palate: a new procedure. Acta Chir Scand. 1960;122–131. Beirne JC, Barry HJ, Brady FA, Morris VB. Donor site morbidity of the anterior iliac crest following cancellous harvest. Int J Oral Maxillofac Surg. 1996;25:268–271. Bergland O, Semb G, Abyholm FE. Elimination of the residual alveolar cleft by secondary bone grafting and subsequent orthodontic treatment. Cleft Palate J. 1986;23:175–205. Bergland O, Semb G, Abyholm F, Borchgrevink H, Eskeland G. Secondary bone grafting and orthodontic treatment in patients with bilateral complete clefts of the lip and palate. Ann Plast Surg. 1986;17:460–474. Boyne PJ, Sands NR. Secondary bone grafting of residual alveolar and palatal clefts. J Oral Surg. 1972;30:87–92. Brattstrom V, McWilliam J. The influence of bone grafting age on ¨ dental abnormalities and alveolar bone height in patients with unilateral cleft lip and palate. Eur J Orthod. 1989;11:351–358. Ellwood RP, O’Mullane DM. Association between dental enamel opacities and dental caries in a north Wales population. Caries Res. 1994;28:383–387. Freihofer HP, Borstlap WA, Kuijpers-Jagtman AM, Borstlap-Engels VM. Bone repair in unilateral cleft: when? With what? [in Language]. Fortschr Kiefer Gesichtschir. 1993;38:30–32. Kalaaji A, Lilja J, Friede H, Elander A. Bone grafting in the mixed and permanent dentition in cleft lip and palate patients: long-term results and the role of the surgeon’s experience. J Craniomaxillofac Surg. 1996;24:29–35. Kindelan JD, Nashed RR, Bromige MR. Radiographic assessment of secondary autogenous alveolar bone grafting in cleft lip and palate patients. Cleft Palate Craniofac J. 1997;34:195–198. Kortebein MJ, Nelson CL, Sadove AM. Retrospective analysis of 135 secondary alveolar cleft grafts using iliac or calvarial bone. J Oral Maxillofac Surg. 1991;49:493–498. Long RE Jr, Semb G, Shaw WC. Orthodontic treatment of the patient with complete clefts of lip, alveolus, and palate: lessons of the past 60 years. Cleft Palate Craniofac J. 2000;37:533–546. Long RE Jr, Spangler BE, Yow M. Cleft width and secondary alveolar bone graft success. Cleft Palate Craniofac J. 1995;32:420–427. Lopes LD, Mattos BS, Andre M. Anomalies in number of teeth in patients with lip and/or palate clefts. Brazil Dent J. 1991;2:9–17. Maciel SP, Costa B, Gomide MR. Difference in the prevalence of enamel alterations affecting central incisors of children with complete unilateral cleft lip and palate. Cleft Palate Craniofac J. 2005;42:392–395.
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ORIGINAL ARTICLE Optimization of Dental Status Improves Long-Term Outcome After Alveolar Bone Grafting in Unilateral Cleft Lip and Palate Fatima Jabbari, D.D.S., Valdemar Skoog, M.D., Ph.D., Eicka Reiser, D.D.S., Ph.D., Malin Hakelius, M.D., Daniel Nowinski, M.D., Ph.D. Objective: To evaluate the importance of dental status for long-term outcome after alveolar bone grafting in patients with unilateral cleft lip and palate. Design: Retrospective longitudinal study. Setting: Cleft lip and palate-craniofacial center, Uppsala University Hospital, Sweden. Patients: A total of 67 consecutive patients with unilateral complete cleft lip and palate. Interventions: Secondary alveolar bone grafting, prior to the eruption of the permanent canine, was performed at the average age of 10.0 years (range, 8.5 to 12.0 years). Main Outcome Measures: Alveolar bone height was evaluated with the modified Bergland index at 1 and 10 years after surgery. Results: Of the patients, 97% had modified Bergland index grade I and the remaining 3% had modified Bergland index grade II at 1 year after surgery. At 10 years’ follow-up, 43% showed modified Bergland index grade I; 55%, modified Bergland index grade II; and 2% (one patient), modified Bergland index grade III. The degree of dental anomalies in the cleft area, such as enamel hypoplasia, incisor rotation, incisor inclination, canine inclination, and oral hygiene registered preoperatively, all correlated negatively to the modified Bergland index at 10 years after surgery. Enamel hypoplasia (q ¼ 0.70195, P , .0001), followed by canine inclination (q ¼ 0.55429, P , .0001), showed the strongest correlation to reduced bone height in the cleft area. Conclusions: In patients with unilateral cleft lip and palate, excellent results from secondary alveolar bone grafting in terms of bone height in the alveolar cleft tend to decrease with time. This seems to be correlated with factors that might to some extent be treated preoperatively through adequate planning and execution of the orthodontic treatment. KEY WORDS:
alveolar bone grafting, cleft lip and palate, orthodontics
Secondary alveolar bone grafting (SABG) in conjunction with orthodontic treatment has evolved into an integral component in the comprehensive treatment of patients with cleft lip and palate. When performed at the end of mixed dentition, before canine eruption, SABG primarily serves to provide bony support for the permanent dentition and to
reconstruct the alveolar process (Troxell et al., 1982; Bergland et al., 1986; Kortebein et al., 1991). Other, secondary goals of this procedure are to close any remaining fistulae and to augment the hypoplastic paranasal maxilla (Boyne and Sands, 1972; Steinberg et al., 1999). Although SABG has been widely accepted, there is still some controversy regarding the timing of the procedure (Bergland et al., 1986), the extension of the grafted region into the hard palate, the flap design (Abyholm et al., 1981), and the amount of the bone that should be grafted in relation to the cleft cavity (Backdahl and Nordin, 1960). ¨ The type of bone graft, cancellous versus cortical, the site from which the bone is harvested (Freihofer et al., 1993), and the influence of orthodontic treatment prior to bone grafting (Long et al., 1995; Kindelan et al., 1997) are other topics that have been discussed. The modified Bergland index (mBI) of bone height has become the criterion standard for assessing outcome of SABG (Kindelan et al., 1997). It has been demonstrated that the outcome is affected by the surgeon’s experience and the type of bone graft used (Lilja et al., 1996), where cancellous bone is favored over cortical bone (Abyholm et al., 1981).
Dr. Jabbari is Scientist and Senior Consultant Orthodontist, Dr. Resier is Consultant Orthodontist, Department of Surgical Sciences and Department of Plastic and Maxillofacial Surgery, Uppsala University; Dr. Skoog is Senior Consultant Plastic Surgeon, Dr. Hakelius is Consultant Plastic Surgeon, Chairman of Cleft Lip and Palate Unit, and Dr. Nowinski is Consultant Plastic and Reconstructive/Craniofacial Surgeon, Chairman of Cranio-Maxillo-Facial Unit, Akademiska Hospital, Uppsala, Sweden. Dr. Nowinski is Craniofacial Surgeon, Dr. Hakelius is Craniofacial Surgeon, and Dr. Jabbari is Consultant Orthodontist, Craniofacial Center, Department of Surgical Sciences, Uppsala University, Uppsala, Sweden. Submitted May 2013; Revised August 2013, September 2013; Accepted October 2013. Address correspondence to: Dr. Fatima Jabbari, D.D.S., Department of Surgical Sciences and the Department of Plastic and Maxillofacial Surgery, Uppsala University Hospital, 751 85 Uppsala, Sweden. E-mail [email protected]. DOI: 10.1597/13-118 210
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TABLE 1
Surgical Protocol of UCLP in Uppsala*
Age 3 mo 6 mo 2y 8–10 y
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Surgery Primary lip plasty according to Skoog and primary rhinoplasty according to McComb Soft palatoplasty Two-layer hard palate closure Secondary alveolar bone grafting
* UCLP ¼ unilateral cleft lip and palate.
Cancellous bone may be harvested from the anterior iliac crest, posterior iliac crest, and tibia, with the anterior iliac crest being the most frequently practiced donor site (Beirne et al., 1996). The abnormal development of the alveolar process in the cleft area may cause hypodontia, supernumerary teeth, peg-shaped teeth, crown and root malformation, and delay in tooth formation and eruption (Ranta, 1986; Lopes et al., 1991; Suzuki and Takahama, 1992; Tsai et al., 1998; Shapira et al., 1999). It is generally accepted that these dental anomalies should be addressed in connection to the SABG procedure. However, the impact of dental anomalies as well as other dental irregularities, such as dental retention, rotation/ inclination, enamel status, and oral hygiene on the outcome of SABG is largely unknown. The aim of the present investigation was to study the impact of dental anomalies in the cleft area on the longterm outcome of secondary bone grafting in patients with unilateral cleft lip and palate (UCLP). MATERIAL
AND
METHODS
Subjects In the present retrospective study, 94 consecutive patients with UCLP who underwent secondary alveolar bone grafting between 1987 and 1997 were recruited from the database of the Cleft Lip and Palate Team, Craniofacial Center, Uppsala University Hospital, Sweden. The inclusion criteria were complete UCLP; patients were white; nonsyndromic patients; treatment according to the Uppsala protocol (Table 1); and all patients operated upon by the same surgeon (V.S.) (Fig. 1). A total of 67 patients were found to meet these criteria. Approval from the Uppsala Ethics Committee was obtained. Orthodontic Preparation and Surgery Eleven patients had a quad helix as an expansion device for the upper arch prior to SABG, 10 patients had a fixed appliance to align the rotated and inclined central incisor adjacent to the cleft, and 2 patients had received both expansion of the upper jaw and a fixed appliance. The remaining 44 patients did not receive any presurgical orthodontics.
FIGURE 1 Distribution of patients with unilateral complete cleft lip and palate.
The mean age at the time of SABG was 10.0 years (range, 8.5 to 12.0 years). The procedure was performed by the same surgeon (V.S.) in all patients. The cleft was exposed through bilateral palatal mucoperiosteal flaps and gingivoperiosteal flaps in the oral vestibulum. Deciduous teeth projecting into the cleft space were removed. The bony cleft in the hard palate was completely exposed. Great care was taken to close the nasal mucoperiosteal layer meticulously with interrupted 4.0 Vicryl sutures. Cancellous bone was harvested from the iliac crest and grafted to the entire cleft space, including the hard palate, and all the way up to the piriform aperture and as an onlay to improve the maxilla. The flaps were sutured back with interrupted 4.0 Vicryl sutures. Great care was taken to provide adequate soft tissue coverage over the bone graft. This was facilitated by scoring the periosteum over the maxilla and medializing the lateral gingivoperiosteal flap. Mean operative time was 153 6 24.5 minutes and the mean amount of bleeding was 284 6 122.3 mL. The mean hospitalization time was 6.2 6 0.81 days; this length of hospital stay was motivated by the relatively long travel distance for most of our patients. Antibiotics were administered as three doses of intravenous cefuroxime during the day of surgery. All patients were seen within 2 to 3 weeks for removal of sutures. At this point, eight (12%) patients showed slight dehiscence in the cleft space and were treated with a secondary suture. In five (7%) patients, minimal granulation tissue was noticed that did not require revision. There were no infectious complications either at the graft site or at the donor site. METHODS Alveolar Bone Height According to Bergland Anterior occlusal radiographs were available for analysis of the alveolar bone height prior to SABG 1 year postoperatively and at 10 years’ follow-up.
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¨ TABLE 2 Tooth Status Index According to Brattstrom (Brattstrom and McWilliam, 1989) Grade
Condition
0 1 2 3 4
Normal teeth Teeth requiring minor restoration Teeth requiring major restoration Teeth malformed to extent of extraction. Missing teeth
The bone formation in the grafted area was assessed according to the mBI (Bergland et al., 1986), which measures the height of the interdental septum adjacent to the erupted canine. Tooth Status Intraoral radiographs obtained prior to surgery were used to determine the tooth status of the central incisor in the cleft area according to the tooth status index. This is a grading of tooth quality previously described and used to evaluate tooth status in the cleft area (Brattstrom and McWilliam, 1989) (Table 2). Furthermore, the presence or absence of the permanent lateral incisor was evaluated and scored as follows: Grade 0, hypodontia; Grade 1, extraction at the time of bone grafting; Grade 2, late extraction (.2 years’ postSABG); Grade 3, persistent lateral incisor. Canine Inclination Inclination of the canine in the cleft area was evaluated from panoramic radiographs obtained at 8 years of age (6 0.5 months) and scored according to a scale previously described by Warford et al. (2003) and Tortora et al. (2008). The patients were stratified into three groups: Grade 0, canine inclination 08 to 158 to the perpendicular of the occlusal plane; Grade 1, canine inclination 158 to 458; and Grade 2, canine inclination .458.
Central Incisor Inclination Inclination of the central incisor on the cleft side in relation to a line perpendicular to the occlusal plane was measured on panoramic radiographs at 8 years of age (6 0.5 months) (Fig. 2). One of three scores was given: Grade 0, incisor inclination 08 to 308; Grade 1, incisor inclination 308 to 508; and Grade 2, incisor inclination .508. Central Incisor Rotation Rotation of the central incisor adjacent to the cleft was measured on dental casts at 8 years of age (6 0.5 months) (Fig. 3). Three different scores were given: Grade 0, incisor rotation 08 to 308; Grade 1, incisor rotation 308 to 508; and Grade 2, incisor rotation .508. Oral Hygiene All patients were categorized into two groups, good and poor, with respect to oral hygiene prior to SABG. This was performed by studying comments in patient charts, clinical observation, and intraoral photographs. Oral hygiene was categorized as good when there was no or limited amount of plaque and no apparent gingivitis adjacent to the cleft. All patients with clear plaque formation and gingivitis were categorized as having poor oral hygiene. All panoramic radiographs used in this study were examined by one trained consultant orthodontist (F.J.) and were analyzed a second time after 6 months. Reproducibility of Recordings The reliability and intraoperator reproducibility of the measurements/scorings were determined from randomized duplicate recordings in 20 UCLP children. Weighted kappa coefficients were calculated. The
FIGURE 2 Incisor inclination was assessed from panoramic radiographs. The inclination of the central incisor in the cleft area was given three different scores. Left panel: grade 0, incisor inclination ,308 to occlusal plane; middle panel: grade 1, incisor inclination 308 to 508 to occlusal plane; right panel: grade 2, incisor inclination .508 to occlusal plane.
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tion between cleft side lateral incisor status and the mBI scores at 10 years’ postsurgery was analyzed with a chi-square test. P values .05 were regarded as statistically significant. RESULTS Alveolar Bone Height
FIGURE 3 Incisor rotation was assessed on dental casts. The rotation of central incisor in the cleft area was given three different scores as described in the ‘‘Materials and Methods’’ section, here exemplified by grade 1 rotation.
kappa coefficients varied from .58 (moderate) to .90 (almost perfect) agreement of repeated measurements. The intraoperator reproducibility was considered good. Statistical Analysis Mean, standard deviation, median, and range were calculated for all parameters. The relation between preoperative scoring of enamel hypoplasia, oral hygiene, inclination of the canine, and inclination and rotation of the central incisor adjacent to the cleft and the mBI scores at 10 years postsurgery were analyzed with Spearman rank correlation. The rela-
FIGURE 4
At 1 year after surgery, 97% of the patients had a bone height of mBI grade I (Fig. 4) and the remaining 3%, mBI grade II. Thus, at 1 year postoperatively the radiological outcome after SABG was excellent. At 10 years after surgery the share of patients with mBI grade I had dropped to 43%; whereas, 55.0% had mBI grade II, and 2% (one patient) had mBI grade III (Fig. 4). Thus, the bone height in the alveolar cleft was reduced with time. Association Between Dental Status and Alveolar Bone Height at 10 Years After SABG Tooth Status Among the 46 patients (69%) who had enamel hypoplasia of the central incisor adjacent to the cleft area, 21 patients had grade 1 hypoplasia and 25 patients had grade 2 (Fig. 5). All patients with grade 2 enamel hypoplasia had mBI grade II, and 9 out of 21 patients with grade 1 enamel hypoplasia had mBI grade II (Fig. 5). The one patient with mBI grade III had grade 1 enamel hypoplasia. The degree of enamel hypoplasia was correlated with reduced bone height as assessed by the mBI at 10 years’ follow-up (Spearman correlation q ¼ .70195, P , .0001).
Alveolar bone height according to the modified Bergland index at 1 and 10 years after secondary alveolar bone grafting.
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FIGURE 5 Enamel hypoplasia of central incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
Lateral Incisor In 8% of the patients the permanent lateral incisor was extracted at the time of bone grafting, 31% of the patients had late extraction, 39% of the patients had hypodontia, and the remaining 22% had presence of the permanent lateral incisor. We did not find an association between late extractions of laterals and mBI at 10 years’ follow-up (P ¼ .4309). Canine Inclination Prior to bone grafting, 39 patients (58%) had grade 1 canine inclination (158 to 458), 18 (27%) patients had grade 2 canine inclination (.458), and 10 (15%) patients
FIGURE 6
had a grade 0 canine inclination (,158) (Fig. 6). There was a correlation between a high degree of canine inclination preoperatively and reduced bone height mBI (q ¼ .55429, P , .0001) after 10 years. Incisor Rotation and Inclination Preoperatively, 10 patients (15%) had grade 0 incisor rotation (08 to 308), 25 patients (37%) had grade 1 incisor rotation (.308 to 508), and 32 patients (48%) had grade 2 incisor rotation (.508). Eight patients (12%) had grade 0 incisor inclination (08 to 308), 45 patients (67%) had grade 1 incisor inclination (.308 to 508), and 14 patients (21%) had grade 2 incisor inclination (.508) preoperatively (Figs. 7 and 8).
Inclination of the canine in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
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FIGURE 7 Rotation of the incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
A high degree of both central incisor rotation (q ¼ .29123, P , .0168) and inclination (q ¼ .29430, P , .0156) in the cleft area was related to reduced bone height at 10 years’ post-SABG. Oral Hygiene Seventeen patients (25%) had poor oral hygiene, and 16 of these patients had mBI grade II. Of the 50 patients with good oral hygiene, 28 (56%) had mBI grade I; 21(42%) had mBI grade II; and one patient had mBI grade III (Fig. 9). Poor oral hygiene correlated to reduced bone height as assessed by the mBI at 10 years’ follow-up (q ¼ .41965, P , .0004). Tables 3 and 4 summarize the statistical analysis of the correlation between the above described parameters and the bone height at 10 years after SABG.
DISCUSSION Although several studies have reported good or excellent results in terms of bone height in the alveolar cleft at 1 year after SABG, this study presents long-term data on bone graft survival. Moreover, this is the first study describing how the severity of dental anomalies and status are related to long-term outcome. The surgical method for SABG was introduced at our ˚ unit in 1984 after a visit by Frank Abyholm from Oslo. Fundamentally, the surgical procedure has been maintained according to the same basic principles. We routinely perform wide exposure through both palatal and vestibular accesses and graft ample amounts of bone, filling the entire three-dimensional cleft space in the hard palate and alveolus up to the piriform aperture. The philosophy has been that a more complete approach, aiming to reconstruct the entire bony cleft, is warranted for a reliable graft take
FIGURE 8 Inclination of the incisor in the cleft area and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
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FIGURE 9 Oral hygiene and degree of alveolar bone height according to the modified Bergland index at 10 years’ follow-up.
and to predictably achieve all treatment goals: tooth support, fistula closure, and maxillary stability. We find support for this approach in the excellent 1-year results presented here, with 97% of patients having an mBI grade of I. It has previously been demonstrated that the surgeon’s experience correlates positively with outcomes after SABG. Thus, the fact that one senior plastic surgeon (V.S.) performed all SABGs in this study population is most probably another important factor behind the excellent results obtained. The importance of the orthodontist in planning, preparations, and follow-up around the SABG procedure is widely recognized. However, the negative impact of the various dental anomalies and poor oral hygiene has to our knowledge not previously been investigated. Dental anomalies occur with higher frequency in patients born with UCLP (Ranta, 1982, 1988; Shapira et al., 2000), and their importance for treatment outcomes warrants close investigation. The data presented here show that, with time, there is a gradual reduction of the grafted bone in the alveolar cleft (57% of the cases). In this study the preoperative degree of oral hygiene and enamel hypoplasia, as well as the degree of canine inclination, incisor inclination, and rotation, were shown to be related to reduced alveolar bone height after 10 years. Several studies have shown that the most common enamel alteration in patients with complete cleft lip and palate is enamel hypoplasia due to a deficiency in enamel TABLE 3
formation and absence of the enamel surface (Suckling et al., 1984; Suckling, 1989; Ellwood and O’Mullane, 1994; Seow, 1997). These defects occur mainly in teeth close to the cleft (Malanczuk et al., 1999; Maciel et al., 2005), and when affecting the central incisor, the hypoplasia has an aesthetic implication. Moreover, it increases the susceptibility to plaque accumulation and increases the risk for decay and gingivitis (Dean, 1934; Ellwood and O’Mullane, 1994; Malanczuk et al., 1999). Furthermore, correction of central incisor rotation and inclination prior to SABG facilitates oral hygiene and prevents plaque formation. Pertaining to this, a plausible explanation for the reduction in bone height could be local infection with the presence of a chronic, low-grade inflammatory process, with activated proteases degrading the grafted bone. Indeed, it is likely that such an inflammatory state would coincide with the factors that were found to be overrepresented in the group of patients with less-favorable outcomes: poor oral hygiene, enamel hypoplasia, and different types of uncorrected dental malalignment. The general complication rate was low, and thus the long-term maintenance of bone grafts in the alveolus could not be linked to earlier complications in the postoperative course. Implementation of regular maintenance therapy is important and beneficial for these patients, and bone grafting should not be performed until the gingiva is healthy (Samman et al., 1994).
Data From Scoring of Bone Height and Parameters of Dental Status
Variable
N
Mean
SD
Maximum
Median
Minimum
Modified Bergland index Enamel hypoplasia Oral hygiene Canine inclination Incisor inclination Incisor rotation
67 67 67 67 67 67
1.58 1.06 0.51 1.12 37.09 60.82
0.53 0.83 0.88 0.64 13.00 29.27
3.00 2.00 2.00 2.00 70.00 90.00
2.00 1.00 0.00 1.00 40.00 45.00
1.00 0.00 0.00 0.00 0.00 0.00
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TABLE 4
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Coefficients for the Correlation Between the Different Parameters of Dental Status and Bone Height at 10 Years After SABG
Enamel hypoplasia Oral hygiene Canine inclination Incisor inclination Incisor rotation
Correlation Coefficient
Lower 95% Confidence Limit
Upper 95% Confidence Limit
P
.70 .42 .55 .29 .29
0.55 0.20 0.36 0.05 0.05
0.80 0.60 0.70 0.50 0.50
,.0001 ,.0004 ,.0001 ,.0156 ,.0168
Impacted permanent maxillary canine occur in merely 1% to 3% of the general population (Peck et al., 1994). However, it is seen with higher frequency in the cleft lip and palate population due to canine inclination (Baccetti, 1998). Therefore, canine inclination should be anticipated in patients with cleft lip and palate before SABG and during follow-up. High degrees of canine inclination indicate risk for altered eruption and impaction. The reduction in bone height observed here, in patients with a high degree of canine inclination, underscores the importance of early diagnosis and possible need for interceptive treatment. From an orthodontic point of view, the most important benefit of secondary alveolar bone grafting is that the newly grafted bone allows for spontaneous eruption of the adjacent canine and orthodontic movement of teeth into ˚ the grafted bone (Abyholm et al., 1981; Long et al., 2000). It could, therefore, be argued that the observed bone graft reduction, from mBI grade I to mBI grade II, lacks clinical significance, as long as adequate support for the permanent dentition has been achieved. This view may be valid in the short-term perspective; however, we believe that maintaining the alveolar bone height in the cleft area is important to prevent long-term complications, such as gingival retractions and periodontitis. Moreover, maintenance of the grafted bone is important for a long-term prognosis of dental survival and especially for patients requiring dental implants. Therefore, it is highly important for the outcome to provide adequate assessment and appropriate interceptive management, entailing the identification of enamel defects and other related dental abnormalities, in order to achieve optimal dental rehabilitation prior to the SABG. In conclusion, excellent results from SABG in UCLP patients in term of bone-height in the alveolar cleft tend to deteriorate with time. This seems to be correlated to factors of dental status. It is important that some of these factors may be improved by meticulous execution of the preoperative orthodontic planning and treatment. Taken together, poor dental status was correlated with a lower bone height at 10 years’ follow-up. The strongest correlation was seen for enamel hypoplasia, followed by canine inclination. Acknowledgments. The authors would like to thank Lars Berglund, statistician, for his valuable statistical advice and calculations. We also
thank Vivecca Brattstrom ¨ for highly valuable mentorship and advice, and Andreas Svee, plastic surgery resident, for data management.
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