CRANIOMAXILLOFACIAL DEFORMITIES/SLEEP DISORDERS/COSMETIC SURGERY

Optimal Timing of Secondary Alveolar

Bone Grafting: A Literature Review
Artur Fahradyan, MD,* Michaela Tsuha, BS,y Erik M. Wolfswinkel, MD,z
Kerry-Ann S. Mitchell, MD, PhD,x
Jeffrey A. Hammoudeh, MD, DDS,k and William Magee III, MD, DDS{
Purpose: Secondary alveolar bone grafting (SABG) during mixed dentition is the standard of care for
alveolar clefts. However, early SABG at 4 to 7 years of age before the eruption of lateral incisors versus
late SABG at 8 to 12 years of age before the eruption of maxillary permanent canines is still debated.
The purpose of this study was to perform a systematic review of the literature to evaluate the outcomes
of early SABG in residual bone volume or degree of bone resorption, maxillary canine movement or impac-
tion rate, complications, and esthetic outcomes and to compare outcomes of early versus late SABG.
Materials and Methods: A comprehensive search of the PubMed database was performed according to
PRISMA guidelines. Keywords for alveolar cleft repair and inclusion criteria were used to screen articles for
final review.
Results: The initial search yielded 6,278 articles, of which 4 retrospective and 4 prospective studies
were chosen for final review. Of these, 7 studies compared outcome variables between early and late
SABG and 1 looked at bone formation of patients who underwent only early SABG. For outcome variables,
3 studies assessed bone volume with radiographic evaluation, 2 estimated maxillary permanent canine
impaction rate, 1 evaluated surgical complications, operative time, and length of hospital stay, and 1
looked at anterior incisor crown length. Overall, 6 studies concluded that early SABG provides a better
outcome than late SABG and 2 found comparable results across the aforementioned variables.
Conclusions: This review suggests that the existing data support the concept of early SABG; however,
the data are not sufficient for a definitive conclusion. A well-planned prospective study is needed to further
investigate the rationale for early SABG.
Ó 2018 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg -:1.e1-1.e7, 2019

Alveolar cleft affects 75% of patients with cleft lip or alveolar ridge in patients with alveolar clefts.2-5 The
cleft lip and palate.1 Alveolar bone grafting is a goal of surgery is to repair the bony defect of the
commonly performed procedure to reconstruct the alveolar ridge, the floor of the nose, and alar base,

*Resident Physician, Division of Plastic and Reconstructive Los Angeles; Associate Professor of Clinical Surgery, Keck School of
Surgery, Keck School of Medicine, University of Southern Medicine of the University of Southern California, Los Angeles, CA.
California, Los Angeles, CA. Conflict of Interest Disclosures: None of the authors have any
yResearch Assistant, Division of Plastic and Maxillofacial Surgery, relevant financial relationship(s) with a commercial interest.
Children’s Hospital Los Angeles, Los Angeles, CA. This paper was presented at the 2018 annual meeting of the Amer-
zResident Physician, Division of Plastic and Reconstructive ican Association of Oral and Maxillofacial Surgeons, Chicago, IL;
Surgery, Keck School of Medicine, University of Southern and the abstract was published in the Journal of Oral and Maxillo-
California, Los Angeles, CA. facial Surgery 76:340, 2018.
xResident Physician, Division of Plastic and Reconstructive Address correspondence and reprint requests to Dr Fahradyan:
Surgery, Keck School of Medicine, University of Southern Division of Plastic and Reconstructive Surgery, Keck School of Med-
California, Los Angeles, CA. icine of the University of Southern California, 1510 San Pablo Street,
kDirector, Jaw Deformities Center; Attending Physician, Division Suite 415, Los Angeles, CA 90033; e-mail: [email protected]
of Plastic and Maxillofacial Surgery, Children’s Hospital Los Angeles, Received July 28 2018
Los Angeles; Associate Professor of Clinical Surgery, Keck School of Accepted November 19 2018
Medicine of the University of Southern California, Los Angeles, CA. Ó 2018 American Association of Oral and Maxillofacial Surgeons
{Director, International Programs; Attending Physician, Division 0278-2391/18/31285-0
of Plastic and Maxillofacial Surgery, Children’s Hospital Los Angeles, https://doi.org/10.1016/j.joms.2018.11.019

1.e1
1.e2 ALVEOLAR BONE GRAFTING

close any residual oronasal fistula, facilitate the impaction rate, complications, and esthetic outcomes
development of a periodontally sound environment and to compare outcomes of early versus late DBGCM.
for the eruption of lateral incisors or canine teeth
into the newly formed alveolar bone, improve the
morphology of the alar base, and increase bone Materials and Methods
volume for dental implants.2,3,6-15 In addition to
LITERATURE SEARCH
achieving the immediate goals, it is important to
consider the effect of surgery and timing on A comprehensive search of the PubMed database
continued midface development. was performed according to the Preferred Reporting
Historically, alveolar bone grafting has been per- Items for Systematic Reviews and Meta-Analyses
formed at 3 different age periods relative to teeth (PRISMA) guidelines. All English- and non–English-lan-
development. According to Stellmach,16 primary alve- guage articles with available English translations from
olar bone grafting is performed in the deciduous stage January 1980 to December 2017 were obtained using
of dental development, secondary alveolar bone graft- the following keywords: alveolar cleft, alveolar bone
ing (SABG) is performed during mixed dentition, and grafting, alveolar cleft bone grafting, alveolar cleft
tertiary alveolar bone grafting is performed after repair, secondary bone grafting of alveolar cleft, early
mixed dentition.17 These 3 methods have been exten- secondary bone grafting of alveolar cleft, late second-
sively studied and, when compared with one another, ary bone grafting of alveolar cleft, late secondary alve-
the literature suggests that SABG has marked advan- olar cleft grafting, and early secondary alveolar cleft
tages over primary and tertiary alveolar bone graft- grafting. After removing duplicate articles according
ing.18-21 Therefore, SABG has become the current to PMID number, titles and abstracts were reviewed
standard of care in most centers for patients with by an initial research group. Articles that were unre-
alveolar clefts since it was first described by Boyne lated to DBGCM or studies that involved nonhuman
and Sands7 in 1972.22 subjects were excluded. The remaining full-text arti-
Although the term alveolar bone grafting has been cles were evaluated and those that did not meet each
used extensively, it is actually a misnomer because the inclusion criterion for early DBGCM were removed
defect and its reconstruction often extend beyond the from the study. The screened articles were presented
maxillary alveolus. Therefore, a more appropriate to a secondary research group with considerable expe-
term would be bone graft reconstruction of the cleft rience in pediatric craniofacial and plastic surgery
maxilla (BGCM). For this reason, the term delayed research for further evaluation. Only articles that con-
bone graft reconstruction of the cleft maxilla tained sufficient early DBGCM outcome data that
(DBGCM), rather than SABG, is used in this review. could be reviewed and compared were selected for
Despite advances in maxillary cleft repair, the au- final review (Table 1). The inclusion criteria were
thors’ group has documented in 3 separate studies limited to articles that specifically studied the out-
that, although clinical and plain radiographic results comes of early DBGCM or compared early with late
of DBGCM are promising with up to 90% bone take, DBGCM to remain consistent with the purpose of
the actual 3-dimensional bone fill of the alveolar cleft this review. In addition, the authors did not limit their
space is only approximately 30 to 40% using cone- review with a specific outcome variable because they
beam computed tomography (CT).23-25 The anticipated finding very few studies on early DBGCM;
difference in measured outcomes suggests the need this in turn allowed them to include all available early
for further insight into treatment protocols for DBGCM articles in the current literature.
alveolar cleft grafting.
One factor that can affect surgical outcome is the
INCLUSION CRITERIA
timing of bone grafting.2 Although most centers,
including the authors’, currently perform DBGCM at
8 to 12 years of age before canine eruption (late  Diagnosis: cleft maxilla (alveolar cleft)
DBGCM), some argue that early DBGCM at 4 to 7 years  Type of intervention: DBGCM (SABG)
of age before eruption of the lateral incisors might pro-  Patients’ age at surgery: 4 to 7 years
vide better outcomes.26 Although specific indications  Types of outcome: any outcome variable after
and outcomes of late DBGCM have been studied DBGCM at 4 to 7 years of age or comparison of
extensively, specific criteria are not well established various outcome variables in patients undergoing
for early DBGCM. DBGCM at 4 to 7 years of age (early DBGCM)
The purpose of this study was to perform a system- versus 8 to 12 years of age (late DBGCM).
atic review of the literature to evaluate the outcomes  Study types: prospective and retrospective hu-
of early DBGCM in residual bone volume or degree man outcome studies
of bone resorption, maxillary canine movement or  Article types: full articles in the English language
FAHRADYAN ET AL 1.e3

Table 1. BRIEF SUMMARY OF RELEVANT STUDIES INCLUDED IN THIS REVIEW

Sample Assessment
Study Design Size, N Diagnosis Donor Site Outcome Measure Method

Kortebein et al (1991) R 135 UCLP, BCLP Iliac crest, Bone bulk and Plain radiography
calvarium success rate
Ozawa et al (2007)* P 35 UCLP, BCLP Iliac crest Bone resorption CT
Precious (2009) R 145 UCLP Iliac crest Central incisor crown length Clinical
difference between
cleft and non-cleft site
Oberoi et al (2010) P 21 UCLP, BCLP Iliac crest Canine movement in CT
mesiodistal and fascial
and palatal directions
Miller et al (2010) R 99 UCLP, BCLP Iliac crest Complications; length Medical records
of stay; operative time
Pepper et al (2014) P 231 UCLP, BCLP Iliac crest, Symptomatic oronasal Direct patient
tibia fistula rate questioning
Dissaux et al (2016) R 28 UCLP, BCLP Iliac crest Bone volume Cone-beam CT
Kleinpoort et al (2017) R 60 UCLP Iliac crest Maxillary canine impaction risk Plain radiography
Abbreviations: BCLP, bilateral cleft lip and palate; CT, computed tomography; P, prospective; R, retrospective; UCLP, unilateral
cleft lip and palate.
* This study categorized patients by whether germs of the lateral incisors were present.
Fahradyan et al. Alveolar Bone Grafting. J Oral Maxillofac Surg 2019.

The included articles also were reviewed and dis- underwent early DBGCM; patients were grouped ac-
cussed for their limitations and weaknesses. cording to whether the germs of the lateral incisors
were present at the time of surgery. For outcome vari-
EXCLUSION CRITERIA ables, 3 articles assessed the bone graft based on radio-
graphic evaluation of bone volume, 2 articles estimated
the maxillary permanent canine impaction rate, 1
 Any article that did not meet the inclusion criteria
article evaluated the surgical complications, operative
listed earlier
time, and length of hospital stay, and 1 article looked at
the anterior incisor crown length. CT was the main
assessment tool in 3 studies, plain radiography was
Results used in 2 studies, and the remaining 3 studies used
direct clinical assessment, patient surveys, and a re-
The PubMed database search identified 6,278 arti- view of medical records. The details of these studies
cles. After duplicates were removed, 3,651 articles re- are presented in Table 1. Overall, all studies concluded
mained. Analysis of titles and abstracts by the first that early DBGCM provides a better outcome than late
review group yielded 109 full-text studies related to DBGCM or comparable results across the different vari-
DBGCM in humans. From these studies, the 76 articles ables mentioned earlier (Table 2).
that did not meet the inclusion criteria were excluded.
After the second group reviewed the remaining 33 ar-
Discussion
ticles, 8 were selected that had sufficient data about
early DBGCM outcome that could be analyzed in the DBGCM is currently the standard of care for patients
final review (Fig 1). with alveolar clefts in most centers.27 However, recent
Of these 8 articles, 4 were retrospective and 4 were studies using cone-beam CT to evaluate bone fill after
prospective; 2 studies enrolled patients with only uni- DBGCM have reported suboptimal results. One of the
lateral cleft lip and palate and the remaining 6 enrolled largest series on DBGCM was recently published by
patients with unilateral and bilateral cleft lip and pal- the authors’ group, which showed an 80 to 90%
ate. Six studies used an iliac crest bone graft, 1 used bone fill success rate when evaluated clinically.24
the iliac crest or tibial bone, and the other used the iliac Similar results were seen in the authors’ previous
crest or calvarial bone. Seven studies compared study evaluating the success of DBGCM on plain radio-
outcome variables between early and late DBGCM, graphs.25 However, the authors’ most recent work
and 1 evaluated bone formation only in patients who using cone-beam CT to evaluate the 3-dimensional
1.e4 ALVEOLAR BONE GRAFTING

FIGURE 1. Flow diagram of studies included and excluded from this review. *DBGCM, delayed bone graft reconstruction of cleft maxilla.
Fahradyan et al. Alveolar Bone Grafting. J Oral Maxillofac Surg 2019.

bone fill of the cleft site 6 months after DBGCM One factor that can affect the surgical outcome is
showed only a 30 to 40% success rate,23 which is the timing of DBGCM in relation to the eruption of
consistent with other studies using the same technol- lateral incisors or permanent canines. Although most
ogy.27-30 Although this outcome might have been centers, including the authors’, perform late DBGCM
considered optimal or at least adequate in the past, (8 to 12 years of age before eruption of permanent
currently it is questionable given the evolving goals canines), some suggest that early DBGCM (4 to 7 years
of patient care and the increasing popularity of of age before eruption of lateral incisors) might pro-
osseointegrated dental implants in this patient vide better residual bone volume outcomes at the cleft
population.31,32 site.26 Since the landmark article published by Boyne
FAHRADYAN ET AL 1.e5

Table 2. SUMMARY OF DATA COMPARING OUTCOME VARIABLES IN EARLY VERSUS LATE DBGCM

Outcome Early DBGCM Late DBGCM P Value

Bone volume, %
Dissaux et al (2016) 63.3 46.2 .012
Kortebein et al (1991) 97.2 58.2-92.5* .025
Bone resorption, %
Ozawa et al (2007) lateral incisor (+) 33.65 vs () 48.63 — <.05
Maxillary permanent canine impaction rate, %
Kleinpoort et al (2017) 14.29 21.88 .45
Symptomatic oronasal fistula rate, %
Pepper et al (2014)
UCLP 6.25 10.0 .194
BCLP 8.93 12.8 .61
Complications, length of stay, operative time
Miller et al (2010)
Complications, % 9.8 13.2 >.05
Length of stay, days 1.06 1.06 .05
Operative time, minutes 86.2 103.1 .0025
Central incisor crown length difference
between cleft and non-cleft sites, %
Precious (2009) 99.4 125.4 —
Canine movement
Oberoi et al (2010)
Mesial or distal — — .39
Facial or palatal — — .20
Abbreviations: BCLP, bilateral cleft lip and palate; DBGCM, delayed bone graft reconstruction of cleft maxilla; UCLP, unilateral
cleft lip and palate.
* DBGCM was further subdivided into 4 age groups (5 to 7, 8 to 11, 12 to 15, and >15 yr) in this study. The data showed a
relevant trend to decreasing bone volume with increasing age.
Fahradyan et al. Alveolar Bone Grafting. J Oral Maxillofac Surg 2019.

and Sands26 in 1976, several studies have addressed lateral incisor would initiate osteoinductive activities
outcome variables of early DBGCM. Kortebein et al33 in the grafted bone, thus resulting in better bone for-
retrospectively evaluated the plain radiographs of mation and less resorption.14,34 This finding was
171 patients in 1991 and found that those who under- important because up to 50 to 70% of patients are
went DBGCM at 5 to 7 years of age had a higher graft congenitally missing their lateral incisors on the cleft
success rate (97.2%) compared with the groups who site.35-37 Hence, they hypothesized that the optimal
underwent surgery at 8 to 11 (92.5%), 12 to 15 time for BGCM should be before the eruption of
(90.5%), and 16 (58.3%) years of age (P = .025). Graft teeth adjacent to the cleft site. However, if the
success was defined as having sufficient bone volume patient is missing the lateral incisor on the cleft site
to support adjoining teeth or teeth erupting into the congenitally, then bone grafting should be performed
bone graft. Outcomes in this study were based on clin- at a later time before the eruption of permanent
ical and plain radiographic assessments, which might canines.14 Although this seems theoretically logical,
have falsely increased the overall success rate. Howev- their conclusion is only hypothetical because they
er, there was a definite trend toward declining success did not have a comparison group with late DBGCM.
with advancing age at the time of surgery. Some proponents of early DBGCM related the
Fifteen years later, Ozawa et al14 studied the volume timing of the surgery with the eruption of maxillary
of the alveolar bone graft 6 months after early DBGCM central incisors. Precious38 suggested that DBGCM
using a CT image analyzer. They found that patients un- should be performed at approximately 6 years of age
dergoing early DBGCM at 5 to 7 years old with germs at or just before the eruption of maxillary permanent
of the lateral incisors present retained more bone central incisors contralateral to the cleft. He found
stock 6 months after the bone grafting procedure that DBGCM at 6 years provides almost normal symme-
compared with patients in the same age group with try of the clinical crown length of the 2 erupted perma-
missing germs of the lateral incisors. This could be ex- nent maxillary central incisors.38 However, it should
plained by the fact that subsequent eruption of the be noted that although his primary outcome variable
1.e6 ALVEOLAR BONE GRAFTING

might be an important factor, it certainly does not LIMITATIONS

cover many other aspects of BGCM and its outcome.38 A major limitation of this review is that a meta-
Similarly, early DBGCM was advocated by Miller et al39 analysis could not be performed because of the use
at or before the eruption of maxillary central incisors. of different outcome variables and assessment tools
They found no difference between the early and late used in each study. In addition, most articles reported
DBGCM groups in complication rate (9.8 vs 13.2%; on single-center retrospective studies or had small
P > .05) and length of hospitalization (P > .05) but samples; therefore, a well-organized prospective and
found a significantly shorter operative time in the early preferably multicenter study would be needed to
group (86.2 vs 103.1 minutes; P = .0025). They also definitively compare the outcomes between early
suggested that early DBGCM would provide better and late DBGCM.
bone support for dentition, a decreased burden of A thorough review of the literature suggests that
treatment, and improved quality of life. early DBGCM might result in better bone volume of
Soon after, Oberoi et al35 reported their results of the grafted alveolar cleft site compared with late
canine eruption in patients with cleft lip and palate af- DBGCM, with a comparable, perhaps better, complica-
ter DBGCM using cone-beam CT. They found that most tion profile. Although the current data are not suffi-
canines erupted into the bone-grafted alveolar cleft cient for a definitive conclusion to support the
space without impaction. They also noted that there concept of early DBGCM at 4 to 7 years old before
was no difference when comparing early versus late the eruption of the lateral incisors, it does provide ba-
DBGCM groups. This was later confirmed by Klein- ses for further investigation. The authors are currently
poort et al40 in 2017, who studied the impact of timing planning a prospective multicenter study to further
of BGCM on the maxillary permanent canine and investigate this question.
confirmed the findings by Oberoi et al. They
concluded that there was no difference in permanent
canine impaction rate between the 2 groups.40
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