You are on page 1of 13

Cobourne MT (ed): Cleft Lip and Palate. Epidemiology, Aetiology and Treatment.

Front Oral Biol. Basel, Karger, 2012, vol 16, pp 124–136

Alveolar Bone Grafting


Gunvor Semb
Dental School, University of Manchester, Manchester, UK

Abstract Prior to the introduction of alveolar bone grafting,


In the 1970s, Boyne and Sands published reports on a closure of the cleft was associated with several limi-
new technique for alveolar bone grafting. They recom- tations for patients with complete cleft lip and palate
mended that only cancellous bone be used and that the [1–3]. Many patients had residual oronasal fistulae
procedure be undertaken in the mixed dentition prior to despite several attempts to close them with soft tis-
canine eruption. Alveolar bone grafting prior to canine sue surgery. In the cleft region, nasal reflux through
eruption soon became a routine part of the protocol for fistulae and/or food impaction in mucosal recess-
90% of European and North American cleft teams. Sev- es caused chronic periodontal inflammation and
eral uncertainties remain however, such as the specifics eventual loss of teeth, despite good oral hygiene [3].
of the surgical and orthodontic procedures, type of bone The bony defect in the alveolus limited orthodontic
and donor site, and the best way to manage the space in treatment, and all patients needed prosthetic resto-
the dental arch. Probably the commonest timing of the ration in the cleft region. In patients with bilateral
bone graft falls between 8 and 11 years, however there clefts the mobility of the premaxilla made the reten-
has been a trend in some centres to graft earlier in the tion of bridgework difficult. The need for prosthetic
hope of better outcome for the unerupted incisors. The restorations had several disadvantages, for in addi-
influence on maxillary growth of earlier grafting has not tion to the general undesirability of artificial teeth
been ascertained. A wide range of donor sites has been for long-term aesthetics and dental health [3–6]
use but iliac crest remains the most popular. Many teams lack of investing bone often precluded the correc-
perform orthodontics prior to grafting to correct severe tion of anterior tooth irregularities.
segment displacement or align incisors to improve sur- The first attempts at autogenous bone grafting
gical access. Following grafting, absence of the lateral to restore the alveolar cleft were made at the be-
incisor may be managed with orthodontic space closure, ginning of the last century [7, 8]. According to
placement of an implant or bridgework. The introduction Koberg [9] the modern era of bone grafting in
of alveolar bone grafting probably represents one of the patients with clefts was introduced by Axhausen
most significant clinical innovations in cleft care. Hope- [10] whose ideas implied a re-establishment of the
fully, advances in tissue engineering will replace the need tooth-bearing function of the cleft site. Shortly
for transplantation of autogenous bone, or will provide an after Axhausen’s publication, reports on primary
in-situ biological solution to the generation of a continu- bone grafting (usually as a split rib graft) in early
ous bone fill across the alveolar cleft. childhood appeared [10–12] and this was adopt-
Copyright © 2012 S. Karger AG, Basel ed in several countries. However, some years after
203.64.11.45 - 3/3/2015 9:50:48 AM
Kainan University
Downloaded by:
a b

c d

Fig. 1. Alveolar bone grafting: (a)


incision lines, (b) the bony cleft wi-
dely exposed, (c) bone chips from
the iliac crest are packed into the
bony defect, and (d) careful su-
turing. Courtesy of Dr. Michael
Matzen, Oslo University Hospital,
Rikshospitalet, Norway.

the introduction of primary bone grafting, sever- only cancellous bone be used and that the proce-
al studies reported serious impairment of subse- dure be undertaken in the mixed dentition prior
quent maxillary growth [13–16] and bone graft- to canine eruption. They maintained that osteo-
ing came to be viewed with great suspicion and genic cells would survive in a fresh autograft and
was abandoned at most centres. heal rapidly. This was confirmed by Albrektson
In 1965, Skoog [17] introduced periosteo- [22] who detected the first vessels in cancellous
plasty as an alternative to bone grafting: by us- bone 5–8 days after grafting and by 21 days ob-
ing double-layer periosteal flaps, bone formation served that the graft was fully vascularised and
across the cleft was induced without the need of exhibited osteogenesis. Boyne and Sands [21]
a donor site. The periosteoplasty technique was initially presented results of 10 patients who had
adopted by a few teams and in the 1990s the tech- received this treatment and reported that with
nique was modified and popularized by Brusati close collaboration between surgeon and ortho-
and Mannucci [18] and Cutting and Grayson [19] dontist, a completely normal interdental septum
as gingivoalveoloplasty. However, concerns about could be achieved and the canine could erupt
reliability and subsequent growth persist. or be orthodontically moved into the new bone.
Thus, a continuous dental arch without the use
of prosthetic restoration, and improved peri-
Bone Grafting in the Mixed Dentition odontal conditions was achieved. This technique
seemed to have great potential and several subse-
In the 1970s, Boyne and Sands [20, 21] pub- quent reports from other centres confirmed good
lished reports on a new technique for alveolar outcome [23–28]. Alveolar bone grafting prior
bone grafting (fig. 1). They recommended that to canine eruption thus became a routine part
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 125


Kainan University
Downloaded by:
of the protocol for 90% of European and North many considered it appropriate to postpone graft-
American cleft teams [29–30]. Several uncertain- ing till 8–11 years, and subsequent reports con-
ties remain however, such as the specifics of the firmed that this timing did not impair further
surgical and orthodontic procedures, type of bone facial growth [26, 34]. Some proposed that bone
and donor site, and the best way to manage the grafting could be done even earlier to provide
space in the dental arch. bone for the erupting central incisor and the lat-
eral incisor (when present) [35–38]. It was argued
that this may avoid the gingival recession some-
Terminology and Goals of Bone Grafting times observed on the cleft side central incisor
and allow the lateral incisors, if present, a better
Turvey et al. [31] have suggested that the term ‘al- chance of root development. This timing and sub-
veolar’ grafting is misleading as the nasal floor and sequent growth have yet to be formally investi-
lateral piriform rim are also constructed during gated. Indeed, a broader range of timings is now
the procedure performed today. The term ‘second- common, grafting at around 7 years or earlier for
ary’ bone grafting is certainly misleading as it is those with a useful lateral incisor (about 28–37%
the first attempt to repair the defect in the alveolus of laterals [25, 38]) to just before canine eruption
[32]. However, the term is well established in ev- where retention of a lateral is not intended or the
eryday practice. Accordingly, the following termi- lateral is congenitally missing (fig. 2). It is suggest-
nology has been proposed: (1) primary bone graft- ed that delaying the graft in these circumstances
ing: bone grafting in the first 2 years of life; (2) early may reduce canine impaction [39].
bone grafting: between 4 and 7 years; (3) mixed
dentition bone grafting: between 7 and 12 years,
and (4) late bone grafting: bone grafting after the Pre- and Post-Grafting Orthodontics
eruption of the permanent dentition. The goals of
contemporary alveolar bone grafting are primarily It is generally considered useful to undertake
to eliminate the bony defect, making orthodontic some orthodontic fixed appliance preparation
space closure or implant placement possible; pro- prior to grafting [40]. Where the cleft side cen-
vide bony support for the adjacent teeth to ensure tral incisor has tipped into the cleft site and made
long-term periodontal health; close oronasal fistu- surgical access to the bony defect difficult, this
lae; eliminate mucosal recesses, thus making oral can be corrected with 4–5 months with fixed ap-
hygiene easier; provide support to the alar base, pliances [41]. In patients with severe displace-
and stabilize the premaxilla in patients with com- ment of the lateral segment, rotation of the lateral
plete bilateral cleft lip and palate. segment(s) outwards will facilitate placement of
the graft. Using a quad helix or any other fixed
appliance, segment repositioning is done within
Timing of Bone Graft 6–8 months [41]. Segment reorientation cannot
be obtained after grafting [42] and the expan-
When Boyne and Sands reported their experi- sion is also thought to reduce the frequency of
ence of bone grafting in the mixed dentition in canine impaction. Stabilizing a mobile premax-
1972 and 1976 [20, 21], some were cautious about illa with orthodontic arch wire is common in pa-
its adoption, given the adverse facial growth ob- tients with complete bilateral cleft lip and palate.
served following primary bone grafting. As the Typically the arch wires will be removed during
sagittal and transverse growth of the anterior surgery, and replaced at the end of the operation
maxilla continues until the age of 8–9 years [33], to provide retention for around 3 months [40].
203.64.11.45 - 3/3/2015 9:50:48 AM

126 Semb
Kainan University
Downloaded by:
a b c

Fig. 2. Permanent canine eruption through a bone graft: (a) before alveolar bone grafting, (b) 2.6
years later, and (c) after orthodontic treatment.

However, when a substantial outward movement should be made to avoid traumatizing the thin
of the lateral segment(s) has been necessary, clini- bone lamellae that cover the dental roots adjacent
cal experience suggests that bone grafting alone to the cleft. The nasal floor has to be carefully re-
cannot be relied upon to maintain the expansion. constructed when a fistula is present and most
In these circumstances, stabilisation in the form commonly cancellous bone from the iliac crest is
of a simple palatal arch would be advisable until packed high into the defect to give as much sup-
the permanent dentition has erupted. Resting the port to the alar base as possible. Meticulous clo-
patient from appliance therapy is highly desirable sure of the nasal floor and suturing of the flaps
at this stage. Occasional observation is general- without tension is important to avoid contamina-
ly all that is necessary in the years between bone tion from the nasal and/or oral cavity. In patients
grafting and eventual eruption of the permanent with bilateral clefts, both sides are normally oper-
dentition. The status of unerupted teeth, especial- ated at the same time [43].
ly the cleft side canine, does however need careful
monitoring.
Type of Donor Bone and Donor Site Morbidity

Surgical Technique Many sources of bone, both autogenous and al-


loplastic, have been studied and compared, some
Surgical technique varies in detail, especially with highly profiled then abandoned, but fresh autolo-
regard to flap design, but there is general agree- gous cancellous bone is ideal because it supplies
ment that muco-periosteal flaps including the at- living immunocompatible bony cells to integrate
tached gingiva should cover the marginal part of fully with the maxilla and stimulate osteogenesis.
the graft [31, 43] (see fig. 1). This provides nor- The question of donor site has been debated for
mal periodontal conditions around the teeth in many years, with choice influenced by surgeon
the grafted region. It is important that the bony experience and preference, the volume of bone
cleft is widely exposed to the level of the nasal cav- required, and the morbidity associated with the
ity and that all scar tissue is removed. Every effort harvest [44]. The commonest donor sites are iliac
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 127


Kainan University
Downloaded by:
crest, cranium, mandibular symphysis, tibia and when comparing cranial bone to bone from the
rib. The assumption that membranous bone is iliac crest [54, 55]. Complications by harvesting
superior to endochondral was previously used cranial bone are relatively rare, the most common
to justify the use of cranial bone and mandibular being haematomas or seromas and dural tear or
bone, however this has not been confirmed [44]. exposure [54–56]. It is not possible for two teams
Iliac crest: Bone from the iliac crest is easy to to operate simultaneously when harvesting cra-
access and large quantities of cancellous bone con- nial bone, which lengthens the operation. Two
taining osteogenic cells that can support osteogen- percent of European and 8% of North-American
esis in the early days of healing can be harvested. teams use cranial bone for alveolar bone grafting
Because of its higher content of osteogenic cells, [29, 30].
cancellous bone is superior to cortico-cancellous Mandibular symphysis: Good results of alveo-
bone, and the process of compacting the bony chips lar bone grafting with bone from the chin have
into the defect is thought to increase its reliability been reported [38, 57–58], and being an intraoral
further. Bone from the iliac crest can be harvested site it is associated with short hospital stay, mini-
by an open approach or with a trephine. Some au- mal pain and invisible scar. The main disadvan-
thors have reported concern with the trauma of tage of the symphysis as a donor site is the limited
traditional open harvesting and minimal invasive bone available, making it unsuitable for large bi-
techniques have been suggested as alternatives lateral clefts [57–59]. Some instances of damage
[45, 46]. It is difficult to compare morbidity from to adjacent teeth, injury to the mental nerve and
different sites but the main criticism for using the disturbance or sensitivity of adjacent teeth, and
iliac crest as a donor site is that postoperative pain soft tissue have been reported [38, 57, 59]. It has
would limit mobility and may require prolonged been argued that bone grafts of cortico-cancellous
hospital stay. Two recent studies conclude that bone (as from the chin) will give more cleft side
harvesting bone from the iliac crest appears to be canine impaction though this has been contra-
well tolerated by patients, has few important com- dicted [38]. Four percent of European teams use
plications, two teams can operate simultaneously chin as the donor site [29].
which reduces operating time, gives aesthetically Tibia: Proponents of tibial bone report that
acceptable scars at the donor site and the hospi- there is enough bone, it is quick to harvest, has
tal stay is a mean of 3 days [47, 48]. Indeed dis- a short operation time, little blood loss, mini-
charge after 24 h has been suggested provided the mal scarring, and early mobility though patients
child can eat, drink and walk, the pain control is should avoid contact sports for 3 weeks [32, 45, 60].
in place, and reliable carers are available [49, 50]. Others argue that the amount of bone available in
Iliac crest remains the most popular donor site, tibia is limited and patients must be warned that
being favoured by 87% of European and 83% of it may be necessary to harvest from both legs [61,
North-American teams [29, 30]. 62]. In young children the proximal tibia is small
Cranium: Both cortical and cancellous bone and the epiphyseal cartilage is growing, which
can be harvested from the calvarium in young means that access located inferiorly to avoid pos-
patients and there are different harvesting tech- sible damage to a growth centre [60–62]. Three
niques described. Several authors claim that that percent of European and 2% of North-American
the cranium is a donor site with low morbidity, teams use tibia as donor site [29, 30].
minimal postoperative pain, a scar that is hidden Rib: Rib grafts are rarely used for alveolar bone
in the hair, early discharge of the patient is possi- grafting today, as the limitations of rib as donor
ble and the outcomes are good [51–53]. However, site are: unsatisfactory amount of bone, risk of
some authors have reported poorer outcomes chest infections, unpleasant long-term discomfort
203.64.11.45 - 3/3/2015 9:50:48 AM

128 Semb
Kainan University
Downloaded by:
and possibly visible scars [58]. In Europe 0.5 and after primary bone grafting have been published
3% of North-American teams use rib as the donor and the technique has been abandoned in some
site [29–31]. centres [72–74]. One centre continues to use the
Autogenous bony substitutes: Demineralised technique despite growth disturbances as this is
bone has been tried, but has limited use because considered to be balanced by the avoidance of
unpredictability in resorption and the amount of mixed dentition bone grafting [75].
bone that is formed [63].
Bone morphogenetic protein: In a systematic
review of results of bone formation obtained by Outcome Evaluation
bone morphogenetic protein, van Hout et al. [64]
identified three papers that compared BMP-2 with Evaluation of bone grafts has traditionally been
iliac crest bone grafting assessed by clinical and done on occlusal radiographs and several scales
radiographic examinations [65–67]. Bone qual- have been suggested [23, 26, 27, 76–78]. Some
ity appeared comparable between the two meth- scales are almost identical, while others differ to
ods in patients treated in the mixed dentition, and the extent that comparisons between reports are
bone quantity appeared superior in the BMP-2 impossible. The reproducibility of three of the
group in skeletally mature patients. However, the published scales has been tested and found to be
sample sizes are small and more research needs to reliable [79]. The use of panoramic films to assess
be done to confirm the benefits of BMP-2. The ad- grafts is unreliable, while periapical films often fail
vantages of using BMP-2 are shortening of opera- to cover the field of interest. Radiographic assess-
tion time, absence of donor site morbidity, shorter ment performed before full eruption of the teeth
hospital stay and reduction of overall cost [64]. in the cleft site including the canine is especially
Boneless-bone grafting: As noted above, Skoog unreliable.
introduced periosteoplasty in 1965 [17] and this Two-dimensional radiography in general ap-
procedure has been adopted by a few cleft teams pears to overestimate the extent of bony infill.
in a modified form [68–70]. The proponents of Studies using three-dimensional computed to-
gingivoperiosteoplasty state that if healthy perios- mography (3D CT) or three-dimensional cone-
teum is closed over the alveolar defect, favourable beam computed tomography (3D CBCT) have
osteogenic conditions will allow bone to bridge shown than especially in the bucco-palatal di-
it. Presurgical orthopaedics for 6 months preop- mension there can be substantial bone loss after
eratively is usually necessary to align the maxil- alveolar bone grafting [80–85]. Bone loss however
lary segments before the surgery. This operation appears significantly lower in patients with orth-
is usually done before the child is 2 years old and odontic space closure [82, 84, 85]. A large increase
is reported to be a delicate operation, ‘not for the in bone volume when teeth erupt or are orthodon-
occasional operator’ [70]. The degree of ossifi- tically moved into the bone-grafted region is ob-
cation after gingivoalveoloplasty varies between served [82, 84, 85] and the authors argue that the
10 and 100% [69–71]. Matic and Power [71] in a absolute figure of bone volume may not be so im-
large material with long-term follow-up reported portant. Clinically, the most important outcome is
poor outcome in 90% and that a failed procedure the presence of sufficient bone to allow orthodon-
was detrimental to subsequent bone grafting. A tic movement of teeth, survival of the teeth and
high incidence of naso-alveolar fistula after gin- a functional and aesthetic arch alignment. In 18
givoalveoloplasty and poor facial growth were consecutive patients with orthodontic space clo-
found [71–73]. Further reports on severe impair- sure assessed 20 years after bone grafting, 3D CT
ment of subsequent growth similar to that found scans confirmed that there was full bony support
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 129


Kainan University
Downloaded by:
for all teeth in the cleft area for all patients, but incisor (from the smaller lateral segment) had been
there was less bone on the cleft side compared to aligned. Surprisingly, better interdental bone fill
the non-left side [86]. It is questionable whether were found in patients with bilateral rather than
3D CT or 3D CBCT should be used regularly to unilateral complete cleft lip and palate.
asses pre- and post-surgery except where it is vital
for further treatment planning.
Canine Impaction

Factors Influencing the Success of Alveolar Canine impaction following bone grafting in pa-
Bone Grafting tients with clefts is much higher than in children
without clefts, the frequency ranging from 6 to
Generally the results of mixed dentition bone 73% [24–26, 28, 38, 88–90] and is more frequent
grafting have been found to be good, with a high in unilateral than bilateral clefts [38, 88–90]. Semb
success rate [23–28, 35, 38, 76, 77, 87]. All authors and Schwartz [89] compared impaction rates in
have found that the result is better when bone grafted patients and in patients with the same cleft
grafting is performed before eruption of the per- types who were too old to receive grafts following
manent canine. A review of 992 grafted sites where the procedure’s introduction. In the grafted group
the teeth adjacent to the cleft were in their final po- (n = 191) 25% of patients with UCLP had canine
sition, on consecutive patients treated by the Oslo impaction compared with 14% of the non-grafted
cleft team, has been carried out by a panel of two group (n = 80, p = 0.06). However, for BCLP, im-
internal and two external assessors. Good results paction occurred in 3% for the grafted (n = 88)
(more than 3/4 of normal septum height) were and 6% for non-grafted (n = 50). As judged by 3D
found in 96% when the operation was done before CBCT, neither the amount of root development
canine eruption, and 85% when grafting was done nor the presence of the lateral incisor appeared to
after canine eruption [43]. A complete dental arch influence the direction of canine eruption [91].
without having to resort to prosthetic restorations
was found in 93%. Similar findings were reported
by Lilja et al. [35] and Enemark et al. [38]. Management of Space in the Dental Arch
In a study of factors that influence the outcome
of alveolar bone grafting, logistic regression anal- The optimal treatment for missing lateral incisors
ysis for 825 patients with 22 possible explanatory (in about 45% of patients with alveolar clefts [92])
variables was performed [Semb, unpubl. data]. A is a controversial issue and has been discussed at
panel of external and internal assessors used a mod- length in the orthodontic literature.
ified Bergland scale to score the amount of bone in Orthodontic space closure: The major benefit in
the interdental septum and in the naso-apical re- the author’s opinion is that the end of the orthodon-
gion. The most important factor associated with tic treatment marks an end-point in major dental
outcome was the individual surgeon who carried procedures for most patients. Re-contouring the
out the procedure, both for the interdental septum canine to a more ideal lateral incisor shape and
and the naso-apical area. Better outcome was ob- size following orthodontic space closure provides
served in narrower clefts compared to large clefts, long-term results that are as good as, or superior
in clefts where the root of the canine was about to space opening for prosthetic replacement [93–
half developed at the time of grafting, and when 95]. The periodontal conditions are significantly
orthodontic space rather than prosthetic space clo- better with orthodontic space closure than with
sure was performed. It was worse when the lateral prosthetic replacement, the temporomandibular
203.64.11.45 - 3/3/2015 9:50:48 AM

130 Semb
Kainan University
Downloaded by:
a b c d

Fig. 3. Tooth transplantation into an alveolar bone graft: (a) before bone grafting, (b) 6 months
after bone grafting, a small premolar from the non-cleft side has been transplanted into the bone
graft, (c) 12 months after tooth transplantation, and (d) 12 years after tooth transplantation.

joint function is not impaired and patient satisfac- Single tooth implants: Unfortunately, the max-
tion is high [4–6]. illary lateral incisor region may be an unsuitable
Tooth transplantation: Tooth transplantation is site for single tooth implant. A 10-year follow-up
a good option in selected patients (fig. 3) who oth- study of non-cleft patients with single tooth im-
erwise would have had to have a prostheses and the plants showed a progressive reduction of margin-
procedure is a safe and reliable if done at an op- al bone level for the tooth adjacent to the implant
timal time [96, 97]. The survival rate at a mean [99]. The mean bone loss for the central incisor
follow-up of 26.4 years (range 17–41 years) post- adjacent to the implant was 4.3 mm after 10 years.
transplantation of 33 teeth in a Norwegian non- Other problems observed were gingival recessions,
cleft sample was 90% [96]. Premolars in a crowded age changes in position of adjacent teeth, and the
lower jaw are suitable candidates for transplanta- crown shape and colour of the implant crown.
tion to the upper arch. Periodontal and pulp heal- However, many authors favour keeping the
ing is best achieved if transplantation is carried out space open for implant placement in adulthood
when root development is half to three-quarters [100]. An additional bone grafting will generally
complete [96]. Experimental research suggests that be required. Implant placement immediately after
simultaneous bone grafting and tooth transplanta- bone grafting has a high risk of failure due to lack
tion should not be performed [98]. A 4- to 6-month of stable anchorage. According to several reports
period should be allowed for graft consolidation be- the optimal time for implant placement should not
fore tooth transplantation is done. Transplantation exceed 6 months after augmentation bone graft-
of ectopic teeth is also possible [40]. ing. If this is followed, the success rate is reported
Space opening for prosthetic replacement: When to be 70–99% at a follow-up time of 28–66 months
the space in the cleft region is kept open for lat- [100–104]. One study with a control group showed
er prosthetic replacement this will lead to loss of that implant success was less in patients with cleft
the interdental alveolar bone height and thick- [103]. Marginal bone loss was not mentioned in
ness. The long-term maintenance/replacement of two of these studies, and for the other two seemed
prostheses is a major disadvantage, and as noted quite substantial. The most important factor for
above, periodontal health is less favourable. successful implant placement seems to be limiting
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 131


Kainan University
Downloaded by:
a b c

d e f

g h i

Fig. 4. Patient with unilateral cleft lip and palate: (a) at 3 months, before lip and palate closure, (b, c) anterior crossbite
at 7 years of age, (d) after correction of the crossbite, (e) cleft site before grafting at 9.7 years (the lateral incisor is mis-
sing), (f) canine eruption following grafting, (g, h) 1.5 years after orthodontic treatment, and (i) 12.5 years following
bone grafting.

the time between the bone grafting and the im- teeth must be considered carefully, taking account
plant placement. Patients who have bone grafting of possible gingival retraction, lack of interdental
in the mixed or early adult dentition and the space papilla and buccal alveolar bone loss leading to
have been kept open for a later implant, should be gingival discolouring, but especially the continu-
regrafted using autogenous graft from the retro- ous bone loss along adjacent teeth.
molar area, mental symphysis or iliac crest. The
implant is then placed 4–6 months later [100]. The
length of the implant is significantly correlated to The Future
survival; the implant should be 13 mm or longer.
In patients with alveolar clefts this is clearly more For most cleft teams, alveolar bone grafting has
difficult to attain than in individuals without a become a core element in the management of
cleft. Using implants to replace missing anterior patients with cleft involving the alveolus (fig. 4).
203.64.11.45 - 3/3/2015 9:50:48 AM

132 Semb
Kainan University
Downloaded by:
Indeed its introduction probably represents one of autogenous bone in the future, or will provide
of the most significant clinical innovations in cleft an in-situ biological solution to the generation of
care in decades. Hopefully advances in tissue en- a continuous bone fill across the alveolar cleft.
gineering will replace the need for transplantation

References
1 Harvold E: Observations on the develop- 11 Nordin KE: Treatment of primary total 22 Albrektsson T: Healing of bone grafts; in
ment of the upper jaw by harelip and cleft palate deformity. Preoperative vivo studies of tissue reactions at
cleft palate. Odontol Tidskr orthopaedic correction of the displaced autografting in the rabbit tibia; thesis
1947;55:289–305. components of the upper jaw in infants Gothenburg, Sweden 1979.
2 Bøhn A: Retention constructions, fol- followed by bone grafting to the alveolar 23 Åbyholm F, Bergland O, Semb G: Sec-
lowing Mr. Harvold’s method of reposi- process clefts. Trans Eur Orthod Soc ondary bone grafting of alveolar clefts. A
tioning of the maxillary complex in cleft Belfast 1957;333–339. surgical/orthodontic treatment enabling
palate cases. Eur Orthod Soc Rep 12 Schmid E: Die Annäherung der Kiefer- a non-prosthodontic rehabilitation in
1951:219–221. stümpfe bei Lippen-Kiefer- cleft lip and palate patients. Scand J Plast
3 Ramstad T: Fixed prosthodontics in cleft Gaumenspalten: Ihre schädlichen Folgen Reconstr Surg 1981;15:127–140.
palate; in McKinstry RE (ed): Cleft Pal- und Vermeidung. Fortschr Kiefer Gesi- 24 Turvey TA, Vig K, Moriarty J, Hoke J:
ate Dentistry. Arlington, ABI Profes- chtschir 1955;1:168–173. Delayed bone grafting in the cleft max-
sional Publications, 1998, chapt 9, pp 13 Kriens O: Primary osteoplasty in illa and palate: a retrospective multidis-
236–262. patients with clefts of lip, alveolus and ciplinary analysis. Am J Orthod
4 Nordquist GG, McNeill RW: Orthodontic palate. Acta Otorhinolaryngol Belg 1984;86:244–256.
vs. restorative treatment of the congeni- 1968;22:687–696. 25 Bergland O, Semb G, Åbyholm F: Elimi-
tally absent lateral incisor – long-term 14 Robertson NRE, Jolleys A: Effect of early nation of the residual alveolar cleft by
periodontal and occlusal evaluation. J bone grafting in complete clefts of the secondary bone grafting and subsequent
Periodontol 1975;46:139–143. lip and palate. Plast Reconstr Surg orthodontic treatment. Cleft Palate J
5 Andlin-Sobocki A, Eliasson LÅ, Paulin 1968;42:414–421. 1986;23:175–205.
G: Periodontal evaluation of teeth in 15 Rehrmann AH, Koberg WR, Koch H: 26 Enemark H, Sindet-Pedersen S,
bone grafted regions in patients with Long-term postoperative results after Bundgaard M: Long-term results of
unilateral cleft lip and palate. Am J primary and secondary bone grafting in secondary bone grafting of alveolar
Orthod Dentofac Orthop 1995;107:144– complete cleft lip and palate. Cleft Palate clefts. J Oral Maxillofac Surg
152. J 1970;7:206–221. 1987;45:913–918.
6 Robertsson S, Mohlin B: The congeni- 16 Friede H, Johanson B: A follow-up study 27 Lilja J, Friede H, Lauritzen C, Petterson
tally missing upper lateral incisor. A ret- of cleft children treated with primary L, Johanson B: Bone grafting at the stage
rospective study of orthodontic space bone grafting. I. Orthodontic aspects. of the mixed dentition in cleft lip and
closure versus restorative treatment. Eur Scand J Plast Reconstr Surg 1974:8:88– palate patients. Scand J Plast Reconstr
J Orthod 2000;22:697–710. 103. Surg 1987;21:73–79.
7 Von Eiselsberg FW: Zür Technik der 17 Skoog T: The use of periosteal flaps in 28 Paulin G, Åstrand P, Rosenquist JB,
Uranoplastik. Arch Klin Chir the repair of clefts in the primary palate. Bartholdson L: Intermediate bone
1901;64:509–529. Cleft Palate J 1965;2:332–339. grafting of alveolar clefts. J Craniomaxil-
8 Lexer E: Die Verwendung der freien 18 Brusati R, Mannucci N: The early gingi- lofac Surg 1988;16:2–7.
Knochenplastik nebst versuchen über voalveoloplasty. Scand J Reconstr Surg 29 Shaw WC, Semb G, Nelson P, Brattström
Gelenkversteifung und Gelenktranspla- Hand Surg 1992;26:65–70. V, Mølsted K, Prahl-Andersen B: The
tation. Acta Klin Chir 1908;939–954. 19 Cutting C, Grayson B: The prolabial Eurocleft Project 1996–2000. Standards
9 Koberg WR: Present view on bone graft- unwinding flap method for one-stage for Care for Cleft Lip and Palate. Amster-
ing in cleft palate (a review of the litera- repair of bilateral cleft lip, nose and alve- dam, IOS Press, 2000.
ture). J Oral Maxillofac Surg 1973;1:185– olus. Plast Reconstr Surg 1993;91:37–47. 30 Murthy AS, Lehman J: Evaluation of
193. 20 Boyne PJ, Sands NR: Secondary bone alveolar bone grafting: a survey of ACPA
10 Axhausen G: Technik und Ergebnisse grafting of residual alveolar and palatal teams. Cleft Palate Craniofac J
der Spaltplastiken. München, Karl defects. J Oral Maxillofac Surg 2005;42:99–101.
Hauser Verlag, 1952. 1972;30:87–92. 31 Turvey TA, Ruiz RL, Tiwana PS: Bone
21 Boyne PJ, Sands NR: Combined graft construction of the cleft maxilla
orthodontic-surgical management of and palate; in Losee JE, Kirschner RE
residual palato-alveolar cleft defect. Am (eds): Comprehensive Cleft Care. New
J Orthod 1976;70:20–37. York, McGraw-Hill, 2009, pp 837–865.
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 133


Kainan University
Downloaded by:
32 Walker TWM, Modayil PC, Cascarini L, 43 Åbyholm FE: Secondary bone grafting of 55 LaRossa D, Buchman S, Rothkipf DM,
Williams L, Duncan SM, Ward-Booth P: alveolar clefts; in Berkowitz S (ed): Cleft Mayro R, Randall PA: A comparison of
Retrospective review of donor site com- Lip and Palate. Diagnosis and Manage- iliac and cranial bone in secondary
plications after harvest of cancellous ment. Berlin, Springer, 2006, pp 601– grafting of alveolar clefts. Plast Reconstr
bone from the anteriomedial tibia. Br J 605. Surg 1995;96:789–799.
Oral Maxillofac Surg 2009;47:20–22. 44 Rawashdeh MA, Telfah H: Secondary 56 Kline RM Jr, Wolfe SA: Complications
33 Sillman MA: Dimensional changes of the alveolar bone grafting: the dilemma or associated with the harvesting of cranial
dental arches: longitudinal study from donor site selection and morbidity. Oral bone grafts. Plast Reconstr Surg
birth to 25 years. Am J Orthod Maxillofac Surg 2008;46:665–670. 1995;95:5–20.
1964;50:824. 45 Ilankovan V, Stronczek M, Telfer M, 57 Sindet-Pedersen S, Enemark H: Recon-
34 Semb G: Effect of alveolar bone grafting Peterson W, Strassen LF, Ward-Booth P: struction of alveolar clefts with mandib-
on maxillary growth in unilateral cleft A prospective study of trephine bone ular or iliac crest bone grafts: a compara-
lip and palate patients. Cleft Palate J grafts of the tibial shaft and iliac crest. tive study. J Oral Maxillofac Surg
1988;25:288–295. Br J Oral Maxillofac Surg 1998;36:434– 1990;48:554–560.
35 Lilja J, Kalaaji A, Friede H, Elander A: 439. 58 Freihofer HPM, Borstlap WA, Kuijpers-
Combined bone grafting and delayed 46 Sharma S, Schneider LF, Barr J, Aarabi S, Jagtman AM, Voorsmit RACA, van
closure of the hard palate in patients Chibbaro P, Grayson B, Cutting CB: Damme PA, Heidbuchel KLWM,
with unilateral cleft lip and palate: facili- Comparison of minimally invasive ver- Borstlap-Engels VMF: Timing and trans-
tation of lateral incisor eruption and sus conventional open harvesting tech- plant materials for closure of alveolar
evaluation of indicators for timing of the nique for iliac bone graft in secondary clefts. A clinical comparison of 296
procedure. Cleft Palate Craniofac J alveolar cleft patients. Plast Reconstr cases. J Craniomaxillofac Surg
2000;37:98–105. Surg 2011;128:485–491. 1993;21:143–148.
36 Ozawa T, Omura S, Fukuyama E, Matsui 47 Swan MC, Goodacre TE: Morbidity at 59 Booij A, Raghoebar GM, Jansma J, Kalk
Y, Torikai K, Fujita K: Factors influenc- the iliac crest donor site following bone WWI, Vissink A: Morbidity of chin bone
ing secondary alveolar bone grafting in grafting of the cleft alveolus. Br J Oral transplants used for reconstructing alve-
cleft lip and palate patients: prospective Maxillofac Surg 2006;44:129–133. olar defects in cleft patients. Cleft Palate
analysis using CT image analyzer. Cleft 48 Baqain ZH, Anabtawi M, Karaky AA, Craniofac J 2005;42:533–538.
Palate Craniofac J 2007;44:286–291. Malkawi Z: Morbidity from anterior iliac 60 Kalaaij A, Lilja J, Elander A, Friede H:
37 Precious DS: A new reliable method for crest bone harvesting for secondary Tibia as donor site for alveolar bone
alveolar bone grafting at about 6 years of alveolar bone grafting: an outcome grafting in patients with cleft lip and
age. J Oral Maxillofac Surg assessment study. J Oral Maxillofac Surg palate: long-term experience. Scand J
2009;67:2045–2053. 2009;67:570–575. Plast Reconstr Surg Hand Surg
38 Enemark H, Jensen J, Bosch C: Mandib- 49 Rudman RA: Prospective evaluation of 2001;35:35–42.
ular bone graft material for reconstruc- morbidity associated with iliac crest har- 61 Hughes CW, Revington PJ: The proximal
tion of alveolar cleft defects: long-term vest for alveolar cleft grafting. J Oral tibia donor site in cleft alveolar bone
results. Cleft Palate Craniofac J Maxillofac Surg 1997;55:219–224. grafting: experience of 75 consecutive
2001;38:155–163. 50 Perry CW, Lowenstein A, Rothkopf DM: cases. J Craniomaxillofac Surg
39 Sindet-Pedersen S, Enemark H: Manage- Ambulatory alveolar bone grafting. Plast 2002;30:12–17.
ment of impacted teeth in congenital Reconstr Surg 2005;116:736–740. 62 Chen YC, Chen CH, Chen PL, Huang IY,
clefts; in Alling CC, Helfrick JF, Alling 51 Wolfe SA, Berkowitz S: The use of cra- Shen YS, Chen CM: Donor site morbid-
RD (eds): Impacted Teeth. Philadelphia, nial bone in the closure of alveolar and ity after harvesting of proximal tibia
Saunders, 1993, pp 344–352. anterior palatal clefts. Plast Reconstr bone. Head Neck 2006;28:496–500.
40 Semb G, Shaw WC: Orthodontics; in Surg 1983;72:659–671. 63 Horswell BB, Henderson JM: Secondary
Watson A, Sell D, Grunwell P (eds): 52 Jackson IT, Helden G, Marx R: Skull osteoplasty of the alveolar cleft defect.
Management of Cleft Lip and Palate. bone grafts in maxillofacial and cranio- J Oral Maxillofac Surg 2003;61:1082–
London, Whurr Publishers, 2001, chapt facial surgery. J Oral Maxillofac Surg 1090.
19, pp 299–325. 1986;44:949–955. 64 Van Hout WMMT, van der Molen ABM,
41 Semb G, Rønning E, Åbyholm FE: 53 Denny AD, Talisman R, Bonawitz SC: Breugem CC, Koole R, van Cann EM:
Twenty years follow-up of 50 patients Secondary alveolar bone grafting using Reconstruction of the alveolar cleft: can
with unilateral cleft lip and palate. milled cranial bone graft: a retrospective growth factor-aided tissue engineering
Semin Orthod 2011;17:207–224. study of a consecutive series of 100 replace autologous bone grafting? A lit-
42 Vargervik K: Orthodontic treatment of patients. Cleft Palate Craniofac J erature review and systematic review of
cleft patients: Characteristics of growth 1999;36:144–153. results obtained with bone morphoge-
and development/treatment principles; 54 Kortebein MJ, Nelson CL, Sadove AM: netic protein-2. Clin Oral Invest
in Bardach J, Morris HL (eds): Multidis- Retrospective analysis of 135 secondary 2011;15:297–303.
ciplinary Management of Cleft Lip and alveolar cleft grafts using iliac or calva- 65 Herford AS, Boyne PJ, Rawson R, Wil-
Palate. Philadelphia, Saunders, 1990, rial bone. J Oral Maxillofac Surg liams RP: Bone morphogenetic protein-
chapt 78, pp 642–649. 1991;49:493–498. induced repair of the premaxillary cleft.
J Oral Maxillofac Surg 2007;65:2136–
2141.
203.64.11.45 - 3/3/2015 9:50:48 AM

134 Semb
Kainan University
Downloaded by:
66 Dickinson BP, Ashley RK, Wasson KL, 74 Henkel K-O, Gundlach KKH: Analysis of 83 Iino M, Ishi H, Matsushima R, Masayuki
O’Hara C, Gabbay J, Heller JB, Bradley primary gingivoalveoloplasty in alveolar F, Hamada Y, Kondoh T, Seto K: Com-
JP: Reduced morbidity and improved clefts repair. I. Facial growth. J Crani- parison of intraoral radiography and
healing with bone morphogenetic pro- omaxillofac Surg 1997;25:266–269. computed tomography in evaluation of
tein-2 in older patients with alveolar 75 Meazzini M, Rossetti G, Garattini G, formation of bone after grafting for
defects. Plast Reconstr Surg Semb G, Brusati R: Early secondary gin- repair of residual alveolar defects in
2008;121:209–217. givoalveoloplasty in the treatment of patients with cleft lip and palate. Scand J
67 Alonso N, Tanikawa DY, Freitas RD, unilateral cleft lip and palate patients: 20 Plast Surg Hand Surg 2005;39:15–21.
Canan L, Ozawa TO, Rocha DL: Evalua- years’ experience. J Craniomaxillofac 84 Feichtinger M, Mossböck R, Kärcher H:
tion of maxillary reconstruction using a Surg 2010;38:185–194. Assessment of bone resorption after sec-
resorbable collagen sponge with recom- 76 Long RE, Spangler BE, Yow M: Cleft ondary alveolar bone grafting using
binant human bone morphogenetic pro- width and secondary alveolar bone graft three-dimensional computed tomogra-
tein-2 in cleft lip and palate patients. success. Cleft Palate Craniofac J phy: a three year study. Cleft Palate
Tissue Eng Part C Methods 2010;16: 1995;32:420–427. Craniofacial J 2007;44:142–148.
1183–1189. 77 Kindelan JD, Nashed RR, Bromige MR: 85 Oberoi S, Chigurupati R, Pawandeep G,
68 Santiago PE, Grayson BH, Cutting CB, Radiographic assessment of secondary Hoffman WY, Vargervik K: Volumetric
Gianoutsos MP, Brecht LE, Kwon SM: autogenous alveolar bone grafting in assessment of secondary alveolar bone
Reduced need for alveolar bone grafting cleft lip and palate patients. Cleft Palate grafting using cone beam computed
by presurgical orthopedics and primary Craniofac J 1997;34:195–198. tomography. Cleft Palate Craniofac J
gingivoalveoloplasty. Cleft Palate Cran- 78 Witherow H, Cox S, Jones E, Carr R, 2009;46:503–511.
iofac J 1998;35:77–80. Waterhouse N: A new scale to assess 86 Kolbenstvedt A, Aaløkken TM,
69 Meazzini MC, Tortora C, Morabito A, radiographic success of secondary alveo- Arctander K, Johannesen S: CT appear-
Garattini G, Brusati R: Alveolar bone lar bone grafts. Cleft Palate Craniofac J ances of unilateral cleft palate 20 years
formation in patients with unilateral and 2002;39:255–260. after bone graft surgery. Acta Radiol
bilateral cleft lip and palate after early 79 Nightingale C, Witherow H, Reid FD, 2002;43:567–570.
secondary gingivoalveoloplasty: long- Edler R: Comparative reproducibility of 87 Trindade IK, Mazzottini R, da Silva Filho
term results. Plast Reconstr Surg 2007; three methods of radiographic assess- OG, Trindade IEK, Deboni MCZ: Long-
119:1527–1537. ment of alveolar bone grafting. Eur J term radiographic assessment of second-
70 Cutting CB, Grayson BH: The effects of Orthod 2002;25:35–41. ary alveolar bone grafting outcomes in
gingivoalveoloplasty following alveolar 80 Rosenstein SW, Long RE, Dado DV, Vin- patients with alveolar clefts. Oral Surg
molding with pin-retained Latham son B, Alder ME: Comparison of 2D cal- Oral Med Oral Pathol Oral Radiol Endod
appliance versus secondary bone graft- culations from periapical and occlusal 2005;100:271–277.
ing on midfacial growth in patients with radiographs versus 3D calculations from 88 El Deeb M, Messer LB, Lehnert MW,
unilateral clefts. Plast Reconstr Surg CAT scans in determining bone support Hebda TW, Waite DE: Canine eruption
2008;122:871–873. for cleft-adjacent teeth following early into grafted bone in maxillary alveolar
71 Matic DB, Power SM: Evaluating the alveolar bone grafts. Cleft Palate Cranio- cleft defects. Cleft Palate J 1982;19:9–16.
success of gingivoalveoloplasty versus fac J 1997;34:199–205. 89 Semb G, Schwartz O: The impacted
secondary bone grafting in patients with 81 Van der Meij AJW, Baart JA, Prahl- tooth in patients with alveolar clefts; in
unilateral clefts. Plast Reconstr Surg Andersen B, Valk J, Kostense PJ, Andreasen JO, Petersen JK, Laskin DM
2008;121:1343–1353. Tuinzing DB: Bone volume after (eds) Textbook and Color Atlas of Tooth
72 Matic DB, Power SM: The effects of gin- secondary bone grafting in unilateral Impaction. Copenhagen, Munksgaard,
givoalveoloplasty following alveolar and bilateral clefts determined by 1997, chapt 12, pp 331–348.
molding with a pin-retained Latham computed tomography scans. Oral Surg 90 Matsui K, Echigo S, Kimizuka S, Taka-
appliance versus secondary bone graft- Oral Med Oral Pathol 2001;92:136–141. hashi M, Chiba M: Clinical study on
ing on midfacial growth in patients with 82 Schultze-Mosgau S, Nkenke E, Schlegel eruption of permanent canines after
unilateral clefts. Plast Reconstr Surg AK, Hirschfelder U, Wiltfang J: Analysis secondary alveolar bone grafting. Cleft
2007;122:863–870. of bone resorption after secondary alve- Palate Craniofac Surg 2005;42:309–313.
73 Power SM, Matic DB: Gingivoalveolo- olar bone grafts before and after canine 91 Oberoi S, Gill P, Chigurupati R, Hoffman
plasty following alveolar molding with eruption in connection with orthodontic WY, Hatcher DC, Vargervik K: Three-
Latham appliance versus secondary gap closure or prosthodontic treatment. dimensional assessment of the eruption
bone grafting: the effect on bone pro- J Oral Maxillofac Surg 2003;61:1245– path of the canine in individuals with
duction and midfacial growth in patients 1248. bone-grafted alveolar clefts using cone
with bilateral clefts. Plast Reconstr Surg beam computed tomography. Cleft Pal-
2009;124:573–582. ate Craniofac J 2010;47:507–512.
203.64.11.45 - 3/3/2015 9:50:48 AM

Alveolar Bone Grafting 135


Kainan University
Downloaded by:
92 Bøhn A: Dental anomalies in harelip and 97 Czochrowska EM, Semb G, Stenvik A: 101 Kearns G, Perrott DH, Sharma A, Kaban
cleft palate. Acta Odontol Scand Non-prosthodontic management of alve- LB, Vargervik K: Placement of endos-
1963;21:1–109. olar cleft with two incisors missing on seous implants in grafted alveolar clefts.
93 Rosa M, Zachrisson BU: Integrating the cleft side. A report of 5 cases. Am J Cleft Palate Craniofac J 1997;34:520–
esthetic dentistry and space closure in Orthod Dentofac Orthop 2002;122:587– 525.
patients with missing maxillary lateral 592. 102 Härtel J, Pögl C, Henkel K-O, Gundlach
incisors. J Clin Orthod 2001;35:221–234. 98 Stenvik A, Semb G, Bergland O, Åby- KKH: Dental implants in alveolar cleft
94 Tuverson DL: Close space to treat miss- holm F, Beyer-Olsen EMS, Gerner N, patients: a retrospective study. J Crani-
ing lateral incisors. Am J Orthod Haanæs HR: Experimental transplanta- omaxillofac Surg 1999;27:354–357.
2004;125:17A. tion of teeth to simulated maxillary alve- 103 Kramer F-J, Baethge C, Swennen G,
95 Zachrisson BU: Improving the esthetic olar clefts. Scand J Plast Reconstr Surg Bremer B, Schwestka-Polly R, Dempf R:
outcome of canine substitution for miss- 1989;23:105–108. Dental implants in patients with orofa-
ing maxillary lateral incisors. World J 99 Thilander B, Odman J, Lekholm U: cial clefts: a long-term follow-up study.
Orthod 2007;8:72–79. Orthodontic aspects of the use of oral Int J Oral Maxillofac Surg 2005;34:715–
96 Czochrowska EM, Stenvik A, Bjercke B, implants in adolescents: a 10-year fol- 721.
Zachrisson BU: Outcome of tooth trans- low-up study. Eur J Orthod 2001;23:715– 104 Matsui Y, Ohno K, Nishimura A, Shirota
plantation: survival and success rates 731. T, Kim S, Miyashita H: Long-term study
17–41 years’ post-treatment. Am J 100 Pena WA, Vargervik K, Sharma A, of dental implants placed into alveolar
Orthod Dentofac Orthop 2002;121:110– Oberoi S: The role of implants in the cleft sites. Cleft Palate Craniofac J
119. management of alveolar clefts. Pediatr 2007;44:444–447.
Dent 2009;31:329–333.

Dr. Gunvor Semb


Dental School
University of Manchester
Higher Cambridge Street
Manchester M15 6FH (UK)
Tel. +44 0161 275 6791
E-Mail Gunvor.semb@manchester.ac.uk
203.64.11.45 - 3/3/2015 9:50:48 AM

136 Semb
Kainan University
Downloaded by:

You might also like