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ORIGINAL ARTICLE

Long-term stability of alveolar bone grafts


in cleft palate patients
Dominique Toscano,a Ugo Baciliero,b Antonio Gracco,c and Giuseppe Sicilianid
Ferrara, Vicenza, and Padova, Italy

Introduction: Many authors have examined the surgical bone treatment of cleft palate patients, but no study has
emphasized the role of orthodontic therapy. The aims of this study were to evaluate the long-term stability of bone
grafts when using an orthodontic-surgical protocol, to determine the success of bone grafts in minor vs severe
clefts, and to develop a qualitative method for assessing the success of bone grafting. Methods: Forty-nine pa-
tients were included in this study. Occlusal x-rays were taken before (T0), immediately after (T1), and at least 1
year after bone grafting (T2). Two radiographic parameters were analyzed adjacent to the cleft side: the vertical
bone level (Bergland scale) and the horizontal bone level (Witherow-derived scale). Results: The bone graft
success at T2 was 91.84% (95% confidence interval, 84.55-96.41). The severity of the cleft before grafting
was not statistically correlated with success at T2 (P \0.05). The concordance rate between Bergland and With-
erow values was 87.07% (95% confidence interval, 82.69-90.69). The variables analyzed (sex, age, type of cleft,
lateral incisor agenesis) were not statistically correlated (P \0.05) with the stability of bone graft. Based on the
results, the only factor involved in the stability of the graft seems to be dental age at the time of bone grafting and
the orthodontic therapy before and after grafting. Conclusions: It seems appropriate to recommend early appli-
cation of a surgical-orthodontic protocol to treat cleft lip and palate patients, prevent postoperative bone
resorption, and guarantee correct positioning of the teeth. (Am J Orthod Dentofacial Orthop 2012;142:289-99)

M
any studies have examined the surgical bone fragments, opportunity for a rapid expansion of the
treatment of cleft palate patients; however, midline suture, elimination of oronasal fistulas, and
only a small number of these have addressed overall facial esthetic improvements.17 However, all sur-
the long-term stability of the alveolar grafts.1-20 gical and grafting procedures can cause growth
There is a consensus among academic oral surgeons alterations with bone dysplasias that are more severe
regarding the necessity of postponing bone grafting un- when the procedure is performed early.18,19 For this
til the mixed dentition and then using a technique called reason, Kuijpers-Jagtman and Long5 concluded that
“secondary bone grafting.”1-16 Boyne and Sands15,16 a critical and customized case assessment is necessary
distinguished an “early” secondary bone grafting, to determine the risks and benefits of the procedure.
usually performed between the ages of 2 and 5, and Despite the many studies on the outcomes after
a “late” secondary bone grafting, usually after 5 years secondary bone grafting, they have significant limita-
of age. This surgical technique has many advantages, tions, including reported success rates of less than
including unified maxillary reconstruction and 100%, small sample sizes, inconsistent inclusion and
continuous alveolar formation, physiologic eruption of exclusion criteria, incomplete and heterogeneous clini-
the teeth adjacent to the cleft, stabilization of cleft cal records, limited follow-ups, and subjective methods
a
for assessing the success of bone grafts.17,20-26
Postgraduate student, School of Orthodontics, University of Ferrara, Ferrara,
Italy.
Many factors are involved in the success of alveolar
b
Director, Department of Maxillofacial Surgery, Regional Hospital of Vicenza, bone grafting. The first important factor is the canine
Vicenza, Italy.
c
position and its eruption stage at the time of bone graft-
Assistant professor, School of Dentistry, University of Padova, Padova, Italy.
d
Chairman, Postgraduate School of Orthodontics, University of Ferrara, Ferrara,
ing. Several studies have demonstrated that the success
Italy. of bone grafts decreases if the procedure is performed
The authors report no commercial, proprietary, or financial interest in the prod- after canine eruption on the cleft side.21,23,25,27 The
ucts or companies described in this article.
Reprint requests to: Dominique Toscano, via Montebello, n. 31, 44100, Ferrara,
second fundamental factor is the role of the therapy
Italy; e-mail, dominique_toscano@hotmail.it. protocol and the orthodontic role, which have not
Submitted, July 2011; revised and accepted, April 2012. been explored in the literature.
0889-5406/$36.00
Copyright ! 2012 by the American Association of Orthodontists.
The aims of this study were to evaluate the long-term
doi:10.1016/j.ajodo.2012.04.015 stability of bone grafts with an orthodontic-surgical
289
290 Toscano et al

protocol, to determine the success rate of bone grafts in


Table I. Patients excluded from the study
minor vs severe clefts, and to develop a qualitative
method for assessing the success of bone grafting. Patients (n)
Impossible to find radiographs 5
MATERIAL AND METHODS Preoperative radiographs not exposed 10
Postoperative radiographs not exposed 22
In this retrospective clinical trial, we analyzed the Bone graft unnecessary 8
records of 446 complete cleft lip and palate patients, Bone graft not currently performed 5
recruited from the Regional Hospital of Vicenza (Italy), Digital radiographs not exposed 18
Patients excluded from study 68
Cleft Palate Patients National Reference Centre, between
1994 and 2011. There was only 1 data manager (D.T.),
and all records were digitized. The study population
consisted of white patients matched for sex and age. 4. At 8 to 12 months of age: initiation of speech
Patients were included in the study based on the therapy.
following criteria: (1) congenital complete cleft lip and 5. At 18 to 20 months of age: hard palate surgery30
palate; (2) treatment with the protocol of the Regional and continuation of speech therapy.
Hospital of Vicenza and the University of Ferrara; (3) 6. At 5 years of age: placement of a hyrax-type rapid
digital occlusal radiographs before (T0), immediately af- palatal expander bonded onto the deciduous teeth,
ter (T1), and at least 1 year after bone grafting (T2); (4) with palatal and buccal arms reaching to the canines,
performance of the alveolar bone graft by the same sur- activated at a quarter turn per day. The average
geon; (5) digital occlusal x-rays exposed with a standard- activation period depended on the degree of maxil-
ized radiologic technique (long-cone technique and root lary constriction. A 2- to 3-mm overcorrection at the
direction perpendicular to the palatine midline, com- molars was recommended to counteract relapse.
pared with 2 other projections, to prevent radiologic su- Immediately after the expansion, a maxillary trac-
perimpositions, image artefacts, and interpretation tion device (Delaire mask) was applied with 450 g
errors) by the same radiologist; (6) standardized radio- of force per side for 14 hours per day for 7 months.
graphic evaluations; and (7) informed consent from The rapid palatal expander was passively maintained
each patient. Patients were excluded if they had syn- in the mouth for 1 year after the expansion.
dromic cleft lip and palate. A total of 117 patients 7. At 6 to 9 years of age: placement of a passive trans-
met all inclusion criteria. The study was double- palatal bar (0.036-in wire) bonded onto the first
blinded, and the statistical analysis was performed by permanent molars (to prevent transverse relapse)
an external statistician. Of the 117 patients who met and continuation of speech therapy.
the inclusion criteria, 68 were excluded for various rea- 8. At 9 to 11 years of age: placement of an alveolar
sons, leaving 49 patients in the study cohort (Table I). graft in the cleft side, using bone from the iliac
A flow chart of the study participants is shown in the crest, once canine root development was between
Figure. Table II gives the sex distribution. There were one fourth and two thirds of its final root length as
45 unilateral and 4 bilateral clefts. Among the 45 pa- identified on the occlusal x-ray.18,19,33
tients with unilateral clefts, 15 were right sided, and 9. At 9 to 15 years of age: orthodontic fixed therapy
30 were left sided. Thirty-two patients demonstrated lat- with preadjusted 0.022 3 0.028-in brackets to ob-
eral incisor agenesis, and 8 patients had agenesis of tain alignment, leveling, malocclusion correction,
other teeth, contralateral to their clefts. and canine repositioning in the arch. Orthodontic
All patients had a surgical-orthodontic protocol in therapy began when canine root development
accordance with the Regional Hospital of Vicenza was between one fourth and two thirds of its final
and the Postgraduate School of Orthodontics at the root length. Orthodontic appliances were kept in
University of Ferrara in Italy. The chronologic order of place through the transitional phase of the denti-
the treatment, according to the protocol, is outlined tion until all teeth had erupted and definitive ortho-
below. dontic treatment was completed, when all occlusal
and functional goals of therapy were achieved.
1. At birth: placement of a passive palate plate, con- 10. At 18 years of age: plastic (lip revision, nose revi-
structed of soft resin. sion, rhinoplasty, nasal septum surgery, adenoid
2. At 3 months of age: soft-palate surgery28-30 and surgery, sinus mucous membrane surgery, scar
lip and nostril surgery31 with definitive lip repair. surgery) or maxillofacial surgery and implantation
3. At 6 months of age: unilateral and bilateral rhino- if necessary. In this study, no patient received jaw
plasty.32 surgery, plastic surgery, or implantation.

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Toscano et al 291

Assessed for eligibility (n=446)


Recruited from the Regional Hospital of Vicenza (Italy)
Cleft Palate Patients National Reference
Centre since 1994

Inclusion criteria Exclusion criteria


- Congenital complete cleft lip and palate - Syndromic cleft lip and palate
disease
- Surgical-orthodontic therapy protocol
(Vicenza-Ferrara)
- Digital occlusal X-rays at T0, T1, and T2
under standardized condition
- Same surgeon
- Same radiologist
- Standardized radiographic evaluations
- Patient informed consent

Enroll
Meeting inclusion Not meeting inclusion
criteria (n=117) criteria (n=329)

Follow-up

Lost to follow up (n=68)


Reasons: impossible to find X-rays, preoperative
and postoperative X-rays not exposed,
unnecessary bone graft, bone graft not currently
performed, digital X-rays not exposed

Analysis

Analyzed
(n=49)

Fig. Flow chart of the study participants.


Each patient had digital occlusal x-rays taken before parallel to the occlusal plane, and the central beam was
the alveolar bone graft surgery (T0). The radiographs directed perpendicular to the cleft side for the first pro-
were taken using an AC Cefla dental machine with jection and at 70" to the film in the mesial and distal
a CEI OXC 070G x-ray tube (Anthos, Imola, Italy). The directions for the second and third projections. Then
machine was set at 65 kV and 7.5 mA. The focus-to- x-rays were processed with a dental vista scan machine
skin distance was 20 cm. Exposure time varied (model 2130-51; D€ urr Dental, Bietigheim-Bissingen,
depending on the size of patient but was consistent Germany) with DBSWIN software (D€ urr Dental).
for preoperative and postoperative x-rays and varied A numeric code was assigned to each patient before
from 0.7, to 0.86, to 1.0 seconds. The film was oriented the evaluations to ensure blinding of the reviewers.

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292 Toscano et al

Table II. Sample distribution by sex Table III. Bergland scale and Witherow-derived grad-
ing system
Sex n
Bergland scale
Male 33
Type I Septal height approximately normal
Female 16
Type II Septal height at least three quarters of normal
Type III Septal height less than three quarters of normal
At T0, qualitative categorizations of cleft severity Type IV Absence of a continuous bony bridge
were made by using occlusal x-rays and based on the Witherow-derived scale
Score 0 No bone from the root surface to the midline of the cleft
amount of bone support on each root adjacent to the Score Some bone but fails to reach the midline
cleft site. A standard for evaluation was adopted ac- 0.5
cording to 2 scales: the Bergland vertical bone evalua- Score 1 Bone extends from the root surface to the midline
tion25 and the Witherow-derived horizontal bone
evaluation.34 These scales are shown in Table III (types
I, II, III, and IV and scores of 1, 0.5, and 0 were qual- Table IV. Severity of cleft distribution before bone
itative values used to indicate gradations in the pres- grafting
ence or absence of bone). We compared each
Severity of cleft n
radiograph with its corresponding 2 other projections Minor 7
(the tube was directed at 70" to the film in the mesial Moderate 30
and distal directions) to prevent image artefacts and in- Severe 12
terpretation errors. Two values were obtained for each Total 49
cleft. The first value was related to the distal surface of
the tooth on the mesial side of the cleft (site 1), and the obtained 216 values, resulting in a total of 1098 evalu-
second represented the mesial side of the tooth on the ations (Tables V and VI).
distal side of the cleft (site 2). In patients with bilateral By using this method, both of the following criteria
clefts, both clefts were evaluated; however, only 1 had to be met for a successful outcome at T2: (1) vertical
value was recorded in the table because of identical re- and horizontal bone values equal to or better than the
sults. bone values at T1; and (2) type I and score 1 (vertical
All evaluations were performed by a blinded examiner and horizontal bone levels approximately normal), with
(D.T.) and repeated 3 times on 3 different days, with a 30- bone support greater at T2 than at T0.
day interval between evaluation sessions, to assess intra- The patients’ records were reviewed for additional
examiner variability. Twelve randomly selected patients biometric data. Particular attention was paid to type of
were assessed by 3 blinded and experienced examiners cleft (unilateral or bilateral); age at the 3 evaluation
(U.B., A.G., G.S.) to evaluate interexaminer variability. times; sex; any supernumerary teeth, diminutive lateral
Based on the results, the patients were divided into incisors, and peg-shaped lateral incisors in the cleft
the following groups (Table IV): (1) minor cleft: type I, area; any supernumerary or diminutive teeth not in the
score 1 or 0.5, on both teeth adjacent to the cleft; (2) cleft area; absence of any teeth adjacent to the cleft
moderate cleft: types II and III, score 0.5, on both teeth and the probable cause thereof; and the incidence of re-
adjacent to the cleft; and (3) severe cleft: type IV, score 0, grafting.
on both teeth adjacent to the cleft. Patients were also in- The average age at the time of bone grafting was
cluded in the gravest group if there was a different value 10.25 years, with a range of 8 to 14.7 years (Table VII).
on the roots adjacent to the cleft. The average age at follow-up was 12.16 years, with
According to the protocol, an alveolar bone graft on a range of 10.1 to 15.6 years. The average time of
the cleft side and an immediate postsurgical occlusal follow-up after grafting was 1.87 years, with a range
x-ray were performed on each patient. The patients of 1 to 4.8 years (Table VIII).
were then examined monthly to monitor the orthodontic At T2, 38 patients (77.55%; 95% confidence interval
therapy. At T2, a long-term occlusal x-ray was obtained, [CI], 63.38-88.23) had not experienced canine eruption,
and a qualitative evaluation of bone level was performed and 11 patients (22.44%; 95% CI, 11.77-36.62) had ca-
on the teeth adjacent to the cleft at T1 and T2. On 12 nine impaction requiring a surgical flap and orthodontic
randomly selected patients, these evaluations were recovery.
made by the first examiner and the 3 other examiners
to evaluate interexaminer variability. Statistical analysis
The first examiner obtained 294 values and repeated The percentage of bone graft success was calculated
each measurement 3 times. The other 3 examiners at T1 and T2. To evaluate whether the severity of the

September 2012 ! Vol 142 ! Issue 3 American Journal of Orthodontics and Dentofacial Orthopedics
Toscano et al 293

(2) The effects of type of cleft (unilateral or bilateral)


Table V. Sample distribution for Bergland grading
were assessed by using a binomial test (P \0.05). This
system (first operator's first evaluation)
determines the statistical significance of the deviations
I II III IV from the expected and the observed distributions into
T0 19 48 18 13 2 categories. (3) Lateral incisor agenesis was also as-
T1 96 2 0 0 sessed by using a binomial test (P \0.05). (4) Finally,
T2 97 1 0 0
we used the Wilcoxon signed rank test to determine
the surgical success rates (P \0.05). This is a nonpara-
Table VI. Sample distribution for Witherow-derived metric statistical hypothesis test used to assess whether
grading system (first operator's first evaluation) population means differ when comparing 2 related sam-
ples or repeated measurements of 1 sample. It is useful in
0 0.5 1 evaluations of ordinal-scale variables.
T0 13 85 0 The chi-square test (P \0.05) was used to verify the
T1 0 12 86
correlation between the severity of the cleft palate at T0
T2 0 8 90
and any lost teeth adjacent to the cleft at T2, and
whether site 1 had a different Bergland value than site
Table VII. Sample age at time of bone grafting 2 at any of the 3 measurement times. A binomial test
(P \0.05) was used to evaluate whether lateral incisor
Average age (y) SD n Minimum Maximum Median
agenesis at T0 was correlated with the spontaneous
10.25 1.21 49 8.00 14.70 10.00
eruption of the canines at T2, and whether there was
an association between the type of cleft at T0 and any
Table VIII. Follow-up time lost teeth adjacent to the cleft at T2.
The statistical analysis was performed with the R
Average (y) SD n Minimum Maximum Median 2.12 3 64 software (copyright 1998-2012 by Kurt
1.87 1.10 49 1.00 4.80 1.30 Hornik), and the statistical significance level was set at
95% (P \0.05).
defect was correlated to the success of bone grafting at
T2, the results were subjected to the nonparametric chi- RESULTS
square test. To evaluate whether the Bergland scale was
comparable with the Witherow-derived scale, the Ken- Success rate and grading systems
dall coefficient of concordance was used (0 \ Kendall The success rate at T1 was 70.41% (95% CI, 60.34-
W \1). The Kendall W expresses the level of agreement 79.21). The success rate at T2 was 91.84% (95% CI,
of multiple assessments from the same or different oper- 84.55-96.41). The binomial intervals of confidence did
ators. This coefficient is a real number between 0 (no not intersect; therefore, the T2 success rate was
agreement) and 1 (full agreement). A Kendall W less significantly greater than that at T1.
than 0.7 indicates little agreement and that the mea- The correlation between cleft palate severity and suc-
surement method can lead to inaccurate results, whereas cess rate at T2 was not statistically significant (P 5 0.64).
a Kendall W greater than 0.9 indicates strong agreement The Kendall coefficient of concordance was 0.99 for
and that the results are likely to be accurate. both the Bergland and the Witherow-derived scales (0 \
We calculated the Kendall coefficient of concordance Kendall W \ 1), indicating that these scales were com-
(0 \ Kendall W\ 1) to control for intraexaminer and in- parable.
terexaminer repeatability and reproducibility. It was acceptable to use the Kendall W because the
In addition, we evaluated several variables to deter- concordance rate between the Bergland and With-
mine whether they had statistically significant effects erow-derived values was 87.07% (95% CI, 82.69-
on the long-term stability of the bone grafts at T2. (1) 90.69), and the error method was not relevant.
The potential effects of sex and age (at bone grafting) Table IX shows the cross-tabulation of the Bergland
were analyzed by using a linear regression analysis, and Witherow-derived evaluations by first operator and
which is an approach to modeling the relationship be- first evaluation. It highlights the error point in which 37
tween a scalar variable Y and at least 1 variable called type I Bergland values were classified as a Witherow-
X. Proceeding to the statistical analysis, the patients derived score of 0.5.
were further divided into those who were 10 years or After the alveolar bone graft, there were no oronasal
younger and those older than 10 years, in accordance or palatal fistulae, and bone filling was radiographically
with sample medians equal to 10 years old (P \0.05). evident on occlusal x-rays.

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294 Toscano et al

Table IX. Cross-tabulation of the first operator's first Table X. Sample distribution for sites 1 and 2 for the
evaluation Bergland bone level types
Type 0 0.5 1 I II III IV
I 0 37 175 Site 1 (n) 8 24 5 12
II 0 50 1 Site 2 (n) 11 24 13 1
III 0 18 0
IV 13 0 0
There were 12 patients (24.48%; 95% CI, 13.34-
In our 3 groups (minor, moderate, and severe clefts), 38.87) with diminutive teeth outside the cleft area.
no regrafting was necessary. None had supernumerary teeth far from the cleft side.
Variables affecting the long-term stability
DISCUSSION
As previously mentioned, we determined the intra-
examiner variability by calculating the Kendall coeffi- The main purpose of this study was to evaluate the
cient of concordance for the 3 series of values. The long-term stability of alveolar bone grafts with an
coefficient was 0.98 for both Bergland and Witherow- orthodontic-surgical protocol. Our success rates were
derived values (0\Kendall W\1), signifying a high de- 70.41% (95% CI, 60.34-79.21) at T1 and 91.84%
gree of repeatability. The interexaminer variability was (95% CI, 84.55-96.41) at T2; these correspond well
also determined by using the Kendall coefficient of con- with results reported in the literature (90%, Bergland
cordance for the 3 series of values. It was 0.99 for both et al25 in 378 patients; 83%, Amanat and Langdon35
Bergland and Witherow-derived values (0 \ Kendall in 34 patients; 91%, Long et al17 in 43 patients; 73%,
W \1), signifying a high degree of reproducibility. Kindelan et al36 in 38 patients; 72%, Da Silva Filho
There was no statistically significant correlation et al37 in 50 patients; 91%, Lilja et al38 in 70 patients;
between the patient's sex or age and the success of the and 95%, Jia and Mars39 in 55 patients).17,25
alveolar bone graft at T2 (P 5 0.08 and P 5 0.94, re- We used the Kendall coefficient of concordance to
spectively). evaluate method error, intraobserver repeatability, and
There was no statistically significant influence of the interobserver reproducibility. The statistical analysis
type of cleft (unilateral or bilateral) on the long-term indicated that the Kendall W value was close to 1, and
stability of the bone graft (P 5 0.84). the method error was insignificant for the study. Fur-
There was no statistically significant influence of lat- thermore, there was 87.07% agreement between the
eral incisor agenesis on the long-term stability of the Bergland and the Witherow-derived values; therefore,
bone graft at T2 (P 5 0.32). we can assume that this is a simple and accurate quali-
The Bergland vertical bone evaluation resulted in P 5 tative method for assessing the success of bone grafting.
0 for T1 vs T0, and P 5 1 for T2 vs T1. The Witherow- Bergland et al25 evaluated the height of the interdental
derived horizontal bone evaluation resulted in P 5 0 for bone ridge adjacent to the erupted canine on the cleft
T1 vs T0 and P 5 0.13 for T0 vs T2. Based on the P values, side, using a qualitative scale and radiographs taken at
there was a statistically significant Bergland and With- least 1 year after surgery. Long et al17 measured contours
erow-derived value improvement only from T0 to T1. of the grafted bone with a qualitative method from the
occlusal or periapical radiographs of 43 patients with 56
Clinical features and bone graft total cleft sites, taken at least 6 months after surgery.
At T0, there was a statistically significant difference The mean follow-up time was 3.1 years (range, 0.6-8.1
between the Bergland bone levels observed at sites 1 years). We focused on the bone adjacent to the cleft
and 2 (P 5 0), with site 2 having a greater bone level side and measured its contours with 2 qualitative scales
than site 1, as shown in Table X. to assess the bone in the vertical and horizontal directions.
At T1 and T2, there was no statistically significant On the occlusal radiographs of 49 patients at least 1 year
difference between Bergland bone levels at sites 1 and after bone graft surgery, 98 cleft sites were analyzed (2 per
2 (Bergland grading system with P 5 0.47). subject). The mean follow-up time was 1.87 years (range,
Spontaneous canine eruption at T2 was not associ- 1-4.8 years). Our follow-up was at least 1 year rather than
ated with lateral incisor agenesis (P 5 0.34) or cleft pal- 6 months after surgery, as reported by Long et al. This 1-
ate severity at T0 (P 5 0.77). year interval after the bone graft was thought to allow for
Teeth lost adjacent to the cleft at T2 did not correlate adequate bone maturation to occur.25
with cleft palate severity (P 5 0.64) or type of cleft at T0 Various studies have confirmed the reliability of qual-
(P 5 1). itative measurements in occlusal and periapical x-rays

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Toscano et al 295

for assessing the stability of bone grafts.17,25,34,40 did not find a significant influence of lateral incisor agen-
However, no authors have used 2 scales at the same esis on the long-term stability of bone grafts at T2. This is
cleft site and at the same time. Because of its high consistent with data from Russell and McLeod.43
repeatability and reproducibility, the latter method is Others factors that possibly contribute to the vari-
statistically more accurate. It also allows for a 2- ability in graft success were excluded in this study
dimensional (vertical and horizontal) assessment of the because of these factors: the same surgeon and the
long-term success of bone grafts, exposing the patients same surgical technique were used, the same bone was
to a low dose of cerebral radiation, in accordance with grafted (in contrast, Long et al17 used cancellous bone
the radiation protection rules and the ethical, regulatory, from the iliac crest in 95% of patients and cranial
and scientific principles governing clinical research in the bone in 5% of patients), and the eruption stage of the
Declaration of Helsinki (2004). Furthermore, this qualita- teeth in the distal cleft segment (canine) was identical
tive method eliminates the measurement errors that for all patients. We could also exclude variations due
result from radiographic image distortions. The only er- to surgeon or surgical technique because we found a sta-
ror was on the minor cleft side, where some Bergland tistically significant improvement of Bergland and
type I values were classified as Witherow-derived scores Witherow-derived values from T0 to T1.
of 0.5. Another important clinical finding of our study is
In this study, the average age at bone grafting was that, at T0, there was a statistically significant difference
10.25 years, with a range of 8 to 14.7 years. This is sim- in the Bergland bone levels between site 1 (mesial side of
ilar to the data reported by Paulin et al,41 Brattstr€
om and the cleft) and site 2 (distal side of the cleft). We found
McWilliam,42 and Long et al,17 thereby highlighting the that site 2 had a higher bone level than did site 1; this
consensus about when to perform secondary bone is consistent with the findings of Teja et al44 and Long
grafts. et al.17 Both studies attributed this difference to the
The most important clinical finding in our study was eruption of the mesial tooth into an unfavorable posi-
that cleft severity does not statistically correlate with the tion before the alveolar bone grafting. In addition,
rate of surgical success at T2. This finding is consistent both authors suggested that, unlike the apex of the distal
with the report of Long et al.17 Furthermore, regression tooth, the apex of the mesial tooth was not always cov-
analysis showed a low correlation between the presurgi- ered by bone. In this situation, the clinician should not
cal cleft width and the success of alveolar grafts. There- use orthodontic force to prevent root resorption. At T1
fore, minor, moderate, and severe clefts appear to have and T2, there were no statistically significant differences
the same long-term stability. between the Bergland bone levels at sites 1 and 2. These
Our study did not identify any clinically apparent data correlated with good stability of the bone grafts and
oronasal or palatal fistulae after surgery; this agrees indicated the periodontal health of both mesial and dis-
with the studies of Russell and McLeod43 and Long tal teeth adjacent to the cleft side.
et al,17 who reported only 1 patient with a residual oro- Another interesting finding of this study was that, at
nasal fistula. T2, 38 of the 49 patients (77.55%; 95% CI, 63.38-88.23)
In our 3 groups (minor, moderate, and severe clefts), had spontaneous canine eruption through the grafted
there was no regrafting; this is lower than any rate of bone. The success rate in this sample is comparable
regrafting reported in the literature (less than 2% in with the average percentage reported in the literature
the studies of Hall and Posnick,22 Bergland et al,25 and (75%). Previously reported success rates of bone graft
Long et al17). Helms et al26 reported a higher rate of are 97% (Turvey et al23), 95% (Troxell et al45), 95%
regrafting (19%) in both the secondary early and delayed (Long et al17), 92% (Enemark et al24), 85% (Bergland
graft groups, probably due to the dental age of their pa- et al25), 80% (Boyne and Sands15), 73% (Nicholson
tients at the time of bone grafting. and Plint46), and 72% (Da Silva Filho et al37). Bone graft
Another interesting observation was that linear integration was radiographically and histologically veri-
regression analysis demonstrated no statistically signifi- fied.47 However, El Deeb et al21,48 reported spontaneous
cant correlation between the patient’s sex and age (at eruptions in only 27% and 41% of the canines. They
bone grafting) and graft success at T2. Therefore, sex attributed their findings to the bone graft material and
and age did not influence the long-term stability of the surgical technique used. Bergland et al25 clarified
bone grafts in our patients. Furthermore, there was no that wide flaps of alveolar mucosa impede canine erup-
significant correlation between type of cleft (unilateral tion and increase further surgical exposure.
or bilateral) at T0 and the long-term stability of the We believe that the following factors are involved in
bone graft at T2. This indicates that the type of cleft spontaneous canine eruption in cleft patients: (1) arch
did not influence the success of bone grafts. We also development with previous orthopedic expansion, (2)

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296 Toscano et al

creation of space for canine eruption with orthodontic We observed a difference between the type of cleft
therapy, and (3) periodontal health of the canine with re- and spontaneous canine eruption on the cleft side. In
spect to the root during the graft surgery. In addition, the patients with bilateral clefts, there was only 1 with a nor-
grafted bone itself plays a basic role by triggering a cyto- mal canine pattern of eruption at T2. But with only 4
kine cascade through interactions between the bone and patients (8.16%, 95% CI, 2.27-19.6) in the bilateral cleft
the canine follicle. The molecular basis of this phenom- group, we cannot use statistics to draw inferences about
enon is not well characterized yet. Occasionally, canines these 2 groups. However, alterations in eruption were
require an orthodontic stimulus to erupt in the correct probably due to a more serious impairment of the max-
position. In our study, 11 patients (22.44%; 95% CI, illary structure. The presence of deciduous teeth, lateral
11.77-36.62) had canine impactions and required a sur- incisor guidance, and interactions between cytokine and
gical flap and orthodontic recovery. The exposure per- bone are all well-characterized factors that influence ca-
centage of the canines varies in the literature, ranging nine eruption, which is usually absent or more compro-
from 9%48 to 17%,21 and the need for orthodontic trac- mised in bilateral than in unilateral cleft patients.
tion is 5% to 56%.21,37,41,48,49 Patients with alveolar In this study, only 3 patients (6.12%; CI, 1.28-16.87)
clefts have a 20-fold increased risk for canine impaction had lost teeth adjacent to the cleft side at T2. Two pa-
(18.9%50-35%51) compared with the general population tients had peg-shaped lateral incisors, and 1 patient
(1%-2%).52 had microdontic supernumerary teeth instead of a lateral
Further research is needed to determine the correla- incisor; these were extracted during the graft surgery.
tion between canine impaction and bone height, This finding concurs with the findings of Long et al,17
because canine impactions might affect the bone height who reported the loss of 3 teeth, accounting for a failure
vs having a canine erupt into the graft. In this study, we rate of 5%. In contrast, Helms et al26 reported failure
found only 1 patient with canine impaction and incom- rates of 22% and 59% in their study. All teeth lost
plete bone height at T2. Therefore, canine impaction were lateral incisors with anomalies in size, root and
seemed not to affect the bone height after the bone crown shapes, and altered periodontal support. Tooth
graft. loss adjacent to the cleft at T2 did not correlate with cleft
In this study, 65.31% (95% CI, 50.36-78.33) of the severity or type of cleft at T0. This finding has not been
patients had lateral incisor agenesis; this is lower than investigated previously.
reported by Akcam et al53 (70.8%-97.1%) but higher We also assessed any supernumerary and diminutive
than reported by Dewinter et al54 (50%). The high rate teeth outside the cleft area. There were 12 (24.48%; 95%
of dental anomalies on the cleft side might be due to CI, 13.34-38.87) patients with diminutive teeth outside
a deficient blood supply or ectodermal and mesodermal the cleft area. None had supernumerary teeth far from
tissues during embryogenesis. We found that spontane- the cleft side. Previously, Dewinter et al54 also reported
ous canine eruption at T2 was not significantly associ- agenesis outside the cleft area in 27.2% of patients,
ated with lateral incisor agenesis. This is in accordance and Brattst€ om and McWilliam42 reported a 27.8% rate
with the study of Gereltzul et al,55 who reported no ef- of agenesis in unilateral cleft lip and cleft palate pa-
fect of the lateral incisor on canine eruption. However, tients. In contrast, Akcam et al53 showed rates from
Russell and McLeod43 studied 101 cleft sides in patients 12.5% to 52.8% for noncleft side agenesis in the ante-
with complete unilateral or bilateral cleft lips and cleft rior, premolar, and molar regions; this was explained
palates and found that 61% of those with abnormally by the severity of the cleft phenotype.
positioned canines also had abnormal lateral incisors. This study confirms the benefit of secondary bone
In addition, there were more canines with an abnormal grafts. By eliminating the gap, rehabilitating the alveolar
vertical position before alveolar bone grafting when morphology, and facilitating the eruption of teeth, bone
the lateral incisor was missing. We concluded that the grafting allows alveolar bone to develop and supports
absence or anomalies of the lateral incisors might influ- the normal functions of the teeth.
ence canine eruption and increase the risk for canine im- Previous studies have confirmed the importance of
paction. However, thus far, no data support this several variables involved in the long-term stability of
relationship. alveolar bone grafts. These include the initial severity
Spontaneous canine eruption at T2 was not signifi- of the cleft, the surgical technique and the surgeon’s
cantly associated with cleft severity at T0. This finding technical skills, the handling of tissues during the graft
was never previously investigated, and it might result procedure, the type of graft material, the periodontal
from complete healing of the cleft side after bone graft- status of teeth in the proximal segment at the bone
ing, allowing a physiologic canine eruption through the grafting, and the eruption stage of the teeth in the distal
remodeled bone. segment.

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Toscano et al 297

We analyzed the variables of age (at bone graft- dimension and the sagittal projection of the nasal spine
ing), sex, cleft severity and type of cleft, lateral agen- and improves the growth prognosis and the percentage
esis, and grading system by keeping other variables of spontaneous canine eruptions. Even though Russell
constant, such as the surgeon and the surgical and McLeod43 asserted that this conclusion is not sup-
bone-graft technique, the radiologist and the radio- ported by the literature, many studies have confirmed
graphic technique, the type of graft material, the the benefits of rapid maxillary expansion in noncleft pa-
eruption stage of the teeth in the distal segment, tients57-60 and cleft patients.61,62 In noncleft patients,
and the treatment protocol. According to our data, separation occurs in the midpalatal suture. However, in
there was no significant correlation between age or cleft patients, there is a separation between the maxilla
sex and the long-term stability of the bone graft. and the premaxilla without osseous gain, as well as
There was also no significant association between asymmetric bone movement in unilateral cleft patients
cleft severity (minor, moderate, severe) at T0 and the because of their maxillofacial structure. Therefore,
success of the alveolar graft at T2, or between the many authors agree on the necessity and efficiency of
type of cleft (unilateral or bilateral) and the stability early transverse expansion in cleft patients.61,63
of the alveolar graft. Finally, we found no significant After surgery, it is necessary to prevent a relapse by
correlation between lateral incisor agenesis on the preserving the transverse maxillary dimension with
cleft side and the long-term success of bone grafts. a transpalatal bar. It is also necessary to encourage
These findings implicate other factors that might transverse alveolar development through orthodontic
cause the variability in the long-term stability of multi-bracket appliances. The application of biologic
bone grafts. force facilitated tooth eruption on the grafted bone
Based on the evidence from this clinical trial, it is rea- and contributed to its long-term stability. Biology sup-
sonable to assume that factors involved in the success of ports the resorption of bone in the absence of functional
the bone graft are dental age at the time of bone grafting stresses. In this case, the eruption of teeth (lateral incisor
and the surgical and orthodontic protocol. Previous and canine) and their proper placement through bone
studies have emphasized the importance of exploiting grafting are the functional elements of the long-term
the eruptive force of the incomplete canine root on the stability of bone grafts. In the case of diminutive teeth
cleft side and performing appropriate surgical proce- and residual spaces after orthodontic therapy, the
dures to aid in tissue healing and bone-graft stabil- grafted side must be restored with functioning pros-
ity.17,25 However, no prior studies have addressed the thetic teeth (implants) as soon as possible to prevent fur-
importance of orthodontic therapy on the long-term ther bone loss. The long-term stability of dental implants
stability of bone grafts. Only 1 study mentioned ortho- in the cleft side ranges from 82.2%64 to 98.6%.65
pedic treatment as a probable variable in the success A limitation of this study was the absence of a control
of the primary bone graft; however, there was no ortho- group. However, not treating patients with cleft lips and
dontic protocol, and the orthodontic role in the study cleft palates is unethical because of a consensus on the
population was unclear.26 Da Silva Filho et al37 under- therapeutic benefits.
lined the role of the bone graft in canine eruption and It is reasonable to assume that our protocol is an ad-
emphasized that pregraft orthodontic treatments yield equate form of treatment for cleft lip and palate pa-
better access for the surgeon and that postgraft ortho- tients. It reduces the need for maxillofacial surgery at
dontic procedures can correct the positions of the per- the completion of growth, and it positively affects the
manent teeth in the grafted area. However, they did long-term stability of bone grafts with a greater survival
not consider that canines that are protruding through rate of the teeth adjacent to the cleft.
the bone graft have a functional role in the stability of
the bone graft. Feichtinger et al56 reported that the av- CONCLUSIONS
erage loss of bone was 52% in the third year after surgery Based on our data, it seems appropriate to recom-
and clarified the importance of canine and lateral incisor mend the early application of a surgical-orthodontic
eruption through the graft. They did not emphasize the protocol to treat cleft lip and palate patients, prevent
role of orthodontic therapy. postoperative bone resorption, and guarantee correct
We agree with the study by Long et al17 and believe positioning of the teeth.
that it is important to achieve orthopedic maxillary Our findings indicate the following.
protraction and expansion before graft surgery. If
expansion is carried out after bone grafting, fistulae 1. The success rate of bone grafts at T2 was 91.84
can appear, leading to an additional surgical procedure. (95% CI, 84.55-96.41), suggesting a high percent-
The palatal expansion increases the transverse maxillary age of success with this therapy protocol.

American Journal of Orthodontics and Dentofacial Orthopedics September 2012 ! Vol 142 ! Issue 3
298 Toscano et al

2. Cleft severity was not statistically correlated with 14. Berkovitz S. A comparison of treatment results in complete bilat-
success at T2, demonstrating the protocol’s efficacy eral cleft lip and palate using a conservative approach versus
Millard-Latham PSOT procedure. Semin Orthod 1996;2:169-84.
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18. Brattstr€om V, McWilliam J, Larson O, Semb G. Craniofacial devel-
Additional studies involving this surgical- opment in children with unilateral clefts of the lip, alveolus, and
orthodontic protocol need to be conducted with a larger palate treated according to four different regimes. I. Maxillary de-
sample size and a longer follow-up period. velopment. Scand J Plast Reconstr Surg Hand Surg 1991;25:
259-67.
19. Brattstr€om V, McWilliam J, Semb G, Larson O. Craniofacial devel-
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American Journal of Orthodontics and Dentofacial Orthopedics September 2012 ! Vol 142 ! Issue 3

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