The Journal of Craniofacial Surgery
14. Zhang H, Lan Q, Wang X. Neuronavigation-based quantitative study of
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 Volume 29, Number 4, June 2018 Brief Clinical Studies
patients with CL/P, there is a relatively high amount of skeletal
the far-lateral keyhole approach following partial removal of the occipital
condyle and jugular tubercle. J Clin Neurosci 2011;18:678–682
15. Masuoka J, Matsushima T, Hikita T, et al. Cerebellar swelling after sacrifice
of the superior petrosal vein during microvascular decompression for
trigeminal neuralgia. J Clin Neurosci 2009;16:1342–1344
16. Rhoton AL. The temporal bone and transtemporal approaches.
Neurosurgery 2000;47(suppl):S211–S265
Long-Term Skeletal Changes
After Maxillary Distraction
Osteogenesis in Growing
Children With Cleft Lip/Palate
Kai Liu, MM and Nuo Zhou, MD
Purpose: To systematically evaluate the skeletal changes after
maxillary distraction osteogenesis (DO) in growing patients with
cleft lip with or without cleft palate (CL/P).
Materials and methods: Electronic databases, gray literature, and
reference list searches were conducted. Articles reporting prospec-
tive and retrospective studies that included patients <16 years old
(N  6) who had received DO surgery for correction of a midfacial
hypoplasia due to CL/P, and the period of follow-up persisted >1
year were reviewed. The original articles were evaluated by 2
investigators to ensure that they met the selection criteria. A
methodologic quality assessment tool was used to evaluate the
quality of selected studies. Twenty-six studies met the initial search
criteria, and 9 articles included 101 growing patients with maxillary
hypoplasia due to CL/P who received DO surgery were finally
selected and analyzed.
Results: The results showed that long term after maxillary advance-
ment with DO, the horizontal relapse in A-point was <15% in 3
studies, 20% to 25% in 1 study, 30% to 35% in 3 studies, and >40%
in 1 study. Totally, the range of horizontal relapse in A-point was
11.9% to 45.9%. Similarly, the relapse in SNA angle was <30% in 1
study, 30% to 40% in 3 studies, and >40% in 2 studies. Totally, the
range of relapse in SNA was 25.7% to 77%. Two studies showed
that the vertical relapse in A-point were 137% and 208%, and in the
PNS point were 65% and 62.7%.
Conclusion: Although findings demonstrated that DO is an effec-
tive treatment method for severe maxillary hypoplasia in growing
From the Department of Oral and Maxillofacial Surgery, College of
Stomatology, GuangXi Medical University, Nanning Guangxi, China.
Received August 4, 2017.
Accepted for publication November 10, 2017.
Address correspondence and reprint requests to Nuo Zhou, MD,
Department of Oral and Maxillofacial Surgery, College of Stomatol-
ogy, GuangXi Medical University, 10 Shuangyong Road, Nanning
530021, Guangxi, China; E-mail: Briannuo@hotmail.com
The authors report no conflicts of interest.
Copyright # 2018 by Mutaz B. Habal, MD
ISSN: 1049-2275
DOI: 10.1097/SCS.0000000000004294
# 2018 Mutaz B. Habal, MD
Copyright © 2018 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
relapse both in horizontal and vertical dimension. Thus, the first
proposed alternative for CL/P patients would be to select the correct
primary procedure to decrease damage and avoid unnecessary scars.
Then appropriate preoperative and postoperative care is necessary
to prevent postoperative relapse. In addition, overcorrection also
may be a possible alternative for compensation of postoperative
relapse.
Key Words: Cleft lip, cleft palate, distraction osteogenesis,
skeletal changes
M idfacial hypoplasia, a common dentofacial deformity in
patients with cleft lip with or without palate (CL/P), usually
lead to asymmetrical depression in the midface, narrowing maxil-
lary dental arch, and resulting in class III malocclusion.1,2 Approxi-
mately 25% to 40% of CL/P patients exhibit a class III malocclusion
that requires surgical intervention.3 Due to the disharmonious facial
appearance and occlusal dysfunction that usually appears during the
period of growth, patients or their parents usually exhibit a high
expectation of deformity correction in the adolescence.4 The treat-
ment method for deformity includes conventional orthognathic
surgery and internal or external distraction osteogenesis (DO).5
There were multiple scars in palate or upper lip in these patients that
would limit the stretching of the soft tissues, and often lead to the
failure of traditional osteotomy,6 whereas DO has become an
effective and reliable alternative technique for the treatment of
maxillary hypoplasia in CL/P patients.1
Since McCarthy et al first succeed in lengthening the mandible
using DO in 1992, the DO has been used in the field of oral and
maxillofacial surgery more frequently.7 The advantages of DO
technique is that bone regeneration accompanied by simultaneous
expansion of the functional soft tissue, including blood vessels,
nerves, muscles, skin, mucosa, and periosteum,8 which is import-
ant in midfacial hypoplasia treatment, especially for CL/P
patients who had strong soft tissue tensions due to scar con-
tracture.
DO is still a complicated procedure, and is important to assess
both the immediate and long-term postoperative effects. How-
ever, to our knowledge, no evidence-based evaluation for the
effects of maxillary advancement with DO in growing patients
with CL/P has been published. This article tried to systematically
provide evidence-based data on the clinical outcomes and
skeletal stability for applications of DO in growing CL/P
patients.
MATERIALS AND METHODS
Literature Retrieval
A computerized database based literature retrieval was con-
ducted in PubMed (1968 to July 2017), Embase (1988 to July 2017),
Google Scholar (all available articles until July 2017), Medline
(1966 to July 2017), Scopus (all available articles until July 2017),
Web of Science (1950 to July 2017), Health STAR (1966 to July
2017), and all EBM reviews (Cochrane Database of Systematic
Reviews, ACP Journal Club, DARE, and CCTR) up to July 2017.
Terms used in the literature retrieval were distraction osteogenesis,
cleft OR cleft palate, skeletal changes OR stability OR follow-up
studies, and growth OR children OR adolescent. The retrieval also
confined to the English language and limited to human studies. The
selection and specific use of each term with their respective
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 Brief Clinical Studies The Journal of Craniofacial Surgery  Volume 29, Number 4, June 2018

truncation, if applicable, inside every database were performed with

the help of a senior librarian specializing in health sciences data-
base. The selected references were entered into the EndNote
X7 software.

Inclusion Criteria
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Articles reporting prospective and retrospective studies of chil-

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dren or adolescents who were <16 years old (N 6) and undergone
surgical correction of a midfacial hypoplasia in CL/P by DO, and
the period of follow-up was >1 year were included.

Data Extraction and Methodologic Quality

Assessment
Two surgeons independently assessed the literatures and
extracted information eligibility. Once potential abstracts were
selected, full articles were retrieved in a second selection process.
If the abstract did not provide sufficient information for making a
sound decision, then the actual article was obtained to ensure that all
possible available studies were included. Measures were also taken
to ensure that there was no repeated report of patients from the same
center in different publications. Detailed information were retrieved
from each article, including patient demographics, age, sample size,
study design, type of cleft, surgical procedure, device, latency
period, rate of distraction, consolidation period, follow-up period,
and mean movement and mean relapse in the horizontal and vertical
dimensions. A methodological quality checklist and score for the
included studies are modified from previous reference,9 and the
score was calculated using the following criteria: Study design (total
score: 11): objective clearly formulated (1 score), population was
described (1 score), selection criteria was clearly described (1 score)
and adequate (1 score), sample size was considered adequate (1
score) and was estimated before collection of data (1 score),
prospective study (1 score), randomization or consecutive selec-
tion: stated (1 score), follow-up length was clearly described (1
score), type of study: randomized clinical trial (3 score), clinical
trial (2 score), case series (1 score). Study measurements (total
score: 4): measurement method was mentioned (1 score) and
appropriate (1 score), blind measurement (1 score), reliability
was described and was adequate level of agreement (1 score).
Statistical analysis (total score: 4): dropouts included in data
analysis (1 score), statistical analysis was appropriate for data
and combined subgroup analysis (1 score), P value was stated (1
score) and variability measures (SD or CI) were stated (1 score).
Each study was scored by the same 2 investigators, and discre-
pancies were resolved by discussion until consensus was reached.
The maximum quality score possible was 19. A meta-analysis was
planned if the quality of the information retrieved warranted a
meaningful statistical combination.
RESULTS
Three hundred sixty-eight articles were obtained from PubMed,
Embase, Google Scholar, Medlin, Scopus, Web of Science, Health
STAR, and all EBM reviews database, and 256 references are
duplications. Thus, a total of 112 studies met the inclusion criteria.
Of the 112 abstracts, only 26 articles were retrieved after the first set
of selection criteria were applied. No articles were found during
gray literature searches or reference list searches. A flow diagram of
the literature search is given in Figure 1.
At the final selection stage, a total of 17 references were
excluded from the 26 potential articles due to an incomplete report
of data, use of trans-sutural DO surgery, DO in transverse with
maxillary arch deficiency, non-growing patients are included, study
FIGURE 1. Flow diagram of the literature retrieval.
of presurgical evaluation, or cases report study. Finally, only 9
articles that met all of the inclusion criteria were included.8,10–17
Methodological quality assessment of the finally selected articles
showed that the scores ranging from 39.5% to 81.6% of the possible
total maximum score (7.5/19 to 14.5/19), and the average score was
64.1% (12.2/19).
The study designs of the 9 articles included as follows: 2
retrospective randomized clinical trials,10,13 1 retrospective clinical
trials,16 2 prospective case series studies,8,11 and 4 retrospective
case series studies.12,14,15,17
In these studies, total of 101 patients with bilateral or unilateral
CL/P were included, and the age was 7 to 14.1 years. All patients
received lateral cephalograms examination, and received high
LeFort I osteotomy using rigid external distraction device. The
period of follow-up was >2.23 years. The latency period after
surgery was 2 to 5 days, and the rate of distraction was 1 to 1.5 mm/
d. The consolidation period after distraction was 19 days to 3
months. The detailed information of patients in selected articles,
including sample size, type of cleft, mean age, latency period, rate
or distraction, consolidation period are summarized in Table 1.
All studies showed obvious skeletal relapse in the postoperative
period in horizontal and vertical dimension during the long-term
follow-up. The horizontal relapse in A-point was <15% in 3 studies,
20% to 25% in 1 study, 30% to 35% in 3 studies, and >40% in 1
study. Totally, the range of horizontal relapse in A-point was 11.9%
to 45.9%. Similarly, the relapse in SNA angle was <30% in 1 study,
30% to 40% in 3 studies, and >40% in 2 studies. Totally, the range
of relapse in SNA was 25.7% to 77%. Two articles also reported
>100% (137% and 208%) of vertical relapse in A-point, and the
PNS relapses in the vertical dimension of 2 studies were 65% and
62.7%, respectively. The detailed relapse information of each
selected article is listed in Table 2.
DISCUSSION
Many patients with CL/P present a particularly severe maxillary
hypoplasia in childhood. Instead of waiting until skeletal matur-
ity, some surgeons suggest that DO can be used in adolescence to
permit an early treatment for these severe deficiency-based
concerns of psychological, functional, and esthetic profiles.1,10

e350 # 2018 Mutaz B. Habal, MD

Copyright © 2018 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
 The Journal of Craniofacial Surgery  Volume 29, Number 4, June 2018 Brief Clinical Studies

TABLE 1. Basic Information and Clinical Application Information of Patients in Selected Articles

Study Sample Size Mean Age Latency Period, Rate of Distraction Consolidation Period, Facial Mask

18 8 (4F, 4M) 11.4 y 3–5 d, 1 mm/d 4–6 w, >6 m

213 10 10.4 y 2–5 d, 0.5 mm  2/d 2–3 m, N/R
316 21 (11F, 10M) 9.1 y 5 d, 1–1.5 mm/d 5–6 w, 6 m
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411 13 (5F, 8M) M 13.6 y 3–4 d, 0.5 mm  2/d 6–8 w, 3 m

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F 12.8 y
515 12 (3F, 9M) 11.1 y 2–5 d, 1 mm/d 3 m, 0 w
610 10 (2F, 8M) 11.9 y 3–4 d, 1.5 mm/d 4–6 w, 6 w
712 6 (3F, 3M) 10.5 y 5 d, 1 mm/d 6–8 w, N/R
814 8 (4F, 4M) 12.2 y 5 d, 0.5 mm  2/d 19–37 d, 2–3 m
917 13 (4F, 9M) 10.8 y 5 d, 1 mm/d 8–12 w, N/R
Total 101 7–14.1 y 2–5 d, 1 mm/d 19 d to 3 m

Information of non-growing group and nonunion group patients in these studies are not included in this table. d, day; F, female; M, male; m, month; N/R, not reported; w, week; y, year.

The objective of this systematical review was to evaluate the
long-term stability in the maxilla morphology after DO in
growing children with CL/P. All of these randomized clinical
trial, clinical trials, and case series about long-term skeletal
changes after DO for maxillary advancement were included.
Skeletal changes were monitored based on the horizontal and
vertical positions of 3 points registered on the maxilla (A, ANS,
PNS).3 The standardized lateral cephalometric analyzed were
taken preoperatively and postoperatively in all studies,8,10 – 17 and
one of them added volumetric analysis of bone using 3-dimen-
sional computed tomography (3D CT) scan.15 In these selected
studies, the high LeFort I osteotomy was made above the un-
erupted teeth and tooth roots in all patients. All of the maxillary
DO were undertaken using the rigid external distraction device
(RED), which was first designed and reported by Polley and
Figueroa.18,19 Distraction was initiated after a latency period of 2
to 5 days in these studies. The rate of activation period began at
1 mm/d in 5 studies,8,12,15,17 at a rate of 0.5 mm every 12 hours in
2 studies,11,13,14 at 1.5 mm/d in 1 study,10 at 1 to 1.5 mm/d in 1
study.16 The RED was left in place ranged from 3 to 12 weeks for
consolidation and replaced with a facial mask for 0 to 6 months.
Whether these different latency period and rate of distraction
would influence the relapse should be investigated in future.
Most of the finally included studies demonstrated DO was an
effective technique for correction of maxillary hypoplasia in CL/P
patients. The mean A-point horizontal movement was >7 mm, and
the largest movement was >22 mm. An average SNA angle
increased was 08 to 208. There were only 2 studies that recorded
the date of PNS, which moved backward 10.5 and 6.2 mm, respect-
ively.11,12 However, in the horizontal dimension, maxillary DO in
growing CL/P patients also showed an obvious relapse in A-point,
SNA angle, and PNS point after long-term follow-up, which may
due to the soft tissue scar in the palate and the tightness of the upper
lip. To some extent, the N point grows at a faster rate than the A
point, which could explain the fact that the SNA angle gradually
diminishes with growth in CL/P patients.20 In addition, these
findings also further confirmed that there is a relatively high amount
of skeletal relapse, and overcorrection may be an alternative method
for compensation of postoperative relapse in growing patients with
CL/P who received maxillary DO surgery.

TABLE 2. Long-Term Skeletal Changes in Horizontal Dimension and Vertical Dimension

Study Mean Horizontal Movement Mean Horizontal Changes Mean Vertical Movement Mean Vertical Changes

18 Ant: 12.31 mm Ant: 31% (3.81) Ant: 2.31 mm Ant: 208% (4.81 mm)
SNA: 11.288 SNA: 45.5% (5.138)
213 Ant: 22.2 mm Ant: 45.9% (10.2 mm) N/R N/R
SNA: 16.58 SNA: 77% (12.78)
316 SNA: 13.18 SNA: 40% (5.18) N/R N/R
411 Ant: 12.1 mm Ant: 24% (2.9 mm) Ant: 2.1 mm Ant: 9.5% (0.2 mm)
SNA: 12.48 SNA: 33% (4.18) Post: 2.6 mm Post: 65%(1.7 mm)
Post: 10.5 mm Post: 40% (4.3 mm)
515 Ant: 9.41 mm Ant: 30% (2.83 mm) N/R N/R
SNA: 4.78 SNA: 36.8% (1.738)
610 Ant: 17.4 mm Ant: 12.6% (2.2) N/R N/R
SNA: 10.98 SNA: 25.7% (2.88)
712 Ant: 9.4 mm Ant: 34% (3.2 mm) Ant: 3.5 mm Ant: 137%(4.8 mm)
Post: 6.2 mm Post: 43.5% (2.7 mm) Post: 6.7 mm Post: 62.7%(4.2 mm)
814 Ant: 10.1 mm Ant: 12% (1.2 mm) N/R N/R
917 Ant: 12.84 mm Ant: 11.9% (1.53 mm) N/R N/R
Total Ant: 11.9% to 45.9% Ant: 137% to 208%
SNA: 25.7% to 77% Post: 62.7% to 65%
Post: 40% to 43.5%

Information of non-growing group and nonunion group patients in these studies are not included in this table. –, relapse; Ant, anterior; N/R, not reported; Post, posterior; SNA,
angle of Sella-Nasion-A point.

# 2018 Mutaz B. Habal, MD e351

Copyright © 2018 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
 Brief Clinical Studies The Journal of Craniofacial Surgery
Among the minor vertical dimension described in 3 stu-
dies,8,11,12 the A-point mean movement was l2.1 to 3.5 mm.
Additionally, the PNS mean movement was 2.6 to 6.7 mm. Two
articles reported high vertical relapse in A-point. The PNS relapses
in the vertical dimension of 2 studies were 65% and 62.7%,
respectively.11,12 These 3 studies have also shown that the vertical
relapse after maxillary downward drifting was greater than
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horizontal relapse after advancement.11,12 These finding implied
that surgeons should not only be concerned about the horizontal
relapse, but also pay attention to vertical relapse.
A randomized controlled trial published by Doucet JC et al,10
was aim to compare the effect of maxillary DO during growth
period to after growth spurt, and evaluate the difference of skeletal
relapse between 2 groups. After DO treatment, a greater increase of
SNA angle was shown in growing group; however, a significant
decrease when compared with the patients treated after their growth
spurt (25.7% vs 0.0%). In addition, the A-point relapsed 12.6% in
horizontal dimension in growing patients, whereas 5% for the other
group after a follow-up of 4 years, which was similar to the other
randomized controlled trial published by Meazzini MC et al13; the
average A-point advancement in growing group and non-growing
group was 22.2 and 17.7 mm, respectively. Finally, growing chil-
dren had an average 45% relapse after a 5 year follow-up in contrast
to 8.5% relapse in the non-growing children. Similarly, the SNA
angle increased greatly after distraction in all patients. After the 5-
year follow-up, the non-growing patients showed no clinical change
in the angle of SNA, whereas in growing children showed 12.7%
relapse. These finding implied that the DO exhibited better effect in
treatment of midfacial hypoplasia in growing patients, but relapsed
less in non-growing patients with CL/P.
The presence of multiple scars in the palate and upper lip led to
not only the failure of traditional osteotomy but also relapse of DO.
In addition, these contribute to disturbance of growth and devel-
opment of the midface. Therefore, the first proposed alternative for
CL/P patients would be to select the correct primary procedure to
decrease damage and avoid unnecessary scars. However, for grow-
ing CL/P patients who exhibited serious midfacial hypoplasia, DO
surgery may be necessary. In this condition, an important point to be
considered would be the appropriate preoperative and postoperative
care to prevent postoperative relapse, such as effective alveolar
bone graft for obtaining a favorable maxillary continuity before DO
surgery, sufficient consolidation period after completion of DO
surgery, application of rigid internal fixation with ti-plates after
removal of distractor, using splint to keep the maxillary position,
and immediately starting the orthodontic therapy after removal of
distractor. Sometimes, overcorrection also may be a possible
alternative for compensation of postoperative relapse, but should
avoid aggravation of velopharyngeal insufficiency.
CONCLUSIONS
This article provided an overview of the effect of clinical appli-
cations of early maxillary distraction in growing patients with CL/P
and its associated skeletal changes. The finding showed that DO is
an effective treatment method for severe maxillary hypoplasia in
growing CL/P patients. However, the results also showed that there
is relatively high amount of skeletal relapse both in horizontal and
vertical dimension after maxillary distraction. Thus, the first pro-
posed alternative for CL/P patients would be to select the correct
primary procedure to decrease damage and avoid unnecessary scars.
Then appropriate preoperative and postoperative care is necessary
to prevent postoperative relapse. In addition, overcorrection also
may be a possible alternative for compensation of postoperative
relapse. Of course, future studies to effectively decrease the relapse,
e352 # 2018 Mutaz B. Habal, MD
Copyright © 2018 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
 Volume 29, Number 4, June 2018
and promote the clinical effects of DO for correction of midfacial
hypoplasia in patients with CL/P during the growth stages also
are necessary.
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