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SCIENTIFIC FOUNDATION

Autogenous Bone Graft: Basic Science and


Clinical Implications
Gary F. Rogers, MD, JD, MBA, MPH* and Arin K. Greene, MD, MMScÞ

craniofacial center in the United Kingdom may be considerably dif-


Abstract: No single biomaterial is optimum for every craniomax- ferent than what might be available to a surgeon operating in a remote
illofacial application. Instead, surgeons should consider the advan- hospital in Haiti. Thus, the wide range of clinical and socioeconomic
tages and disadvantages of each alternative in a given clinical circumstances that one might encounter contravenes the idea that
situation, and select the material with lowest overall cost and mor- there is a ‘‘best’’ biomaterial for all situations.
bidity, and the highest likelihood of success. Autogenous bone is In general, materials for bone replacement or augmentation
still considered the gold standard for most applications; it becomes fall into 3 categories: organic, synthetic organic, and inorganic.
vascularized and osseointegrates with surrounding bone, thus min- Organic substances include autograft (from the same individual),
allograft (from another individual), and xenograft (from another
imizing the risk of infection, dislodgement, or break-down. Lim-
species). Synthetic organics include hydroxyapatite and osteoin-
itations include added operative time for graft harvest, donor site ductive biologics such as bone morphogenic protein. Examples of
morbidity, graft resorption, molding challenges, and limited avail- inorganic substances are methylmethacrylate, silicone, porous poly-
ability, especially in the pediatric population. Numerous alternatives ethylene, titanium mesh, and bioactive glass.
to bone graft have become available to address these limitations; Autogenous bone has been considered the criterion stan-
unfortunately, most of these products are expensive, do not dard for osseous reconstruction and is still widely used.1,2 The most
osseointegrate, and have unpredictable biologic activity. Under- common donor areas are the cranium, iliac bone, and ribs. Grafts
standing the physiologic behavior of autogenous bone graft can help become vascularized and osseointegrate with surrounding bone,
clarify the indications for its use and provide a conceptual frame- minimizing infection, dislodgement, or breakdown. Nevertheless,
work for achieving the best possible outcome when this alternative harvest requires added operative time and donor-site morbidity.
Autogenous bone has unpredictable resorption and can be difficult
is chosen.
to mold to meet the requirements of the craniofacial skeleton. In
Key Words: Autologous bone graft, craniofacial, addition, the supply of autogenous graft is limited, particularly in the
basic science, particulate pediatric population.
Many alternatives to autogenous bone graft have become
(J Craniofac Surg 2012;23: 323Y327) available and share 2 advantages: (1) the supply is limitless, and (2) a
donor site is not required. Some materials can be molded or cus-
tom manufactured to fit the deformity. Although nonautogenous
products offer certain advantages, these substances are not osteo-
A ugmentation or replacement of bone is one of the most com-
monly performed procedures in craniomaxillofacial surgery. A
number of biomaterials are available, and the choice depends on the
genic (capable of new bone formation). Bone morphogenic pro-
tein and demineralized bone matrix are osteoinductive (able to
clinical situation, personal preference, availability, and cost. Some induce transformation of undifferentiated mesenchymal cells to
experts dogmatically favor one biomaterial over another, but each osteoblasts), but the absence of structural integrity limits their ap-
substance has advantages and disadvantages, and a more rational plicability. The remaining substrates either are osteoconductive
approach is to choose the appropriate material for a given applica- and provide a scaffold for bony ingrowth (eg, allograft, hydroxy-
tion. For example, the preferred biomaterial to reconstruct a cranial apatite, ceramics) or have no biologic activity (eg, methylmetha-
defect in a healthy 2-year-old would likely differ from what would crylate, titanium, porous polyethylene). These compounds undergo
be indicated for a 71-year-old with major comorbidities. Similarly, incomplete revascularization and osseointegration and are suscep-
the material used for malar augmentation in a major metropolitan tible to latent infection, foreign body reaction, displacement, and
breakage.3Y8 Consequently, the use of alloplastic materials in grow-
ing children generally is not recommended. With the exception of
methylmethacrylate, the high cost of these materials renders them
From the *Division of Plastic and Reconstructive Surgery, Children’s unavailable in all but the wealthiest parts of the world. In an era of
National Medical Center, Washington, District of Columbia; and increasing scrutiny of health care costs, the arguments for consider-
†Department of Plastic and Oral Surgery, Children’s Hospital Boston, ing autogenous bone graft for most craniofacial application seem
Boston, Massachusetts. even more compelling.
Received August 23, 2011. Unfortunately, academic interest in autogenous bone graft
Accepted for publication August 27, 2011. has waned recently as researchers and clinicians have clamored to
Address correspondence and reprint requests to Gary F. Rogers, MD, JD, study and use more sophisticated biomaterials. The majority of the
MBA, MPH, Division of Plastic and Reconstructive Surgery, Children’s
literature regarding the biology and outcomes of autogenous bone
National Medical Center, 111 Michigan Ave NW, Washington, DC
22102; E-mail: grogers@cnmc.org
graft predates this millennium. Certainly, some of this trend can
The authors report no conflicts of interest. be rightly attributed to a genuine desire on the part of surgeons to
Copyright * 2012 by Mutaz B. Habal, MD overcome perceived limitations of autogenous bone graft. How-
ISSN: 1049-2275 ever, an equally potent and more insidious force is the aggressive
DOI: 10.1097/SCS.0b013e318241dcba product marketing tactics by the biotechnology industry. It is no

The Journal of Craniofacial Surgery & Volume 23, Number 1, January 2012 323

Copyright © 2012 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Rogers and Greene The Journal of Craniofacial Surgery & Volume 23, Number 1, January 2012

surprise that our journals are inundated with advertisements and the recipient bed is suboptimal, vascularized bone graft is a more
industry-sponsored research, touting the virtues of the latest bio- reliable option. Rapid and predictable revascularization of the bone
material to replace bone. results in a high rate of osteocyte survival. The living bone maintains
its inherent properties: rapid healing, osseointegration, resistance to
infection, and adaptation to mechanical forces. Over the last decade,
AUTOGENOUS BONE GRAFT: FACTORS vascularized bone grafts have become more widely used in cra-
niofacial reconstruction.
AFFECTING VOLUME RETENTION AND
CLINICAL OUTCOME
The 2 most important clinical outcomes after transfer of Graft Type and Microarchitecture
an autogenous bone graft are volume retention and the biologic Many sources of autogenous bone graft exist, but there are
behavior of the graft. The final volume of bone graft that remains only a few sites where bone can be removed without causing a
after implantation is the net effect of osteolysis (caused by revas- significant functional or aesthetic deficit. The most common areas
cularization and remodeling) and osteogenesis in and around the are the cranium, ribs, or iliac crest. Donor-site morbidity for rib graft
graft. If the former process exceeds the latter, the graft will lose includes possible contour irregularity, pleuritic pain, and pneumo-
volume. Conversely, if the rate of osteogenesis exceeds the rate of thorax.13 Iliac harvest causes discomfort and risks injury to the
resorption, graft volume will increase. The biologic behavior of a lateral femoral cutaneous nerve. In young children, overzealous iliac
graft includes its ability to heal and integrate with surrounding bone, bone harvest may damage the apophysis.
resist infection, and tolerate mechanical load. These characteristics In contrast to iliac or rib donor sites, which require a second
of any osseous graft are largely related to the survival of bone- incision, the cranium is often exposed in most craniomaxillofacial
producing cells after transfer. Failure to identify and compensate procedures. The cranial donor site causes minor discomfort, and the
for variables that can adversely influence the volume retention scar is well concealed. Cranial bone can be harvested full thickness,
and survival of a bone graft will result in a suboptimal clinical partial (split) thickness, or as particulate corticocancellous graft.
outcome. Although full-thickness bone is excellent for structural purposes, it
leaves a donor defect that must be repaired. Consequently, most
surgeons use split cranial bone graft through the diploic space to
Osteocyte and Osteoblast Survival obtain 2 pieces of mostly cortical boneVone to perform the re-
Living bone contains viable bone-producing cells (ie, osteo- construction and the other to repair the donor site. Limitations of
cytes and osteoblasts). Although osteocytes are capable of only split cranial bone grafting include (1) the segments over the donor
limited bone formation, they are very important in orchestrating and recipient sites do not heal to a normal thickness over time, and
and regulating the activity of bone-producing osteoblasts and bone (2) the technique requires a well-developed diploic space, which
healing.9,10 The ability to initiate new bone growth is one of the rarely occurs in children younger than 5 years.
greatest advantages of autologous bone graft over other substrates, An attribute of cranial bone compared with other autoge-
and surgeons should strive to protect these cells. Furthermore, os- nous bone sources is its superior volume retention when used to
teocyte death may promote bone resorption through induction of augment existing bone. Historically, this phenomenon was at-
osteoclastic activity.11 Thus, survival of these cells is an important tributed to the embryologic origin of the grafts (endochondral vs
determinant of graft retention and biologic activity after transfer. membranous).14,15 Nevertheless, subsequent studies demonstrated
Osteocyte and osteoblast survival in a nonvascularized graft that volume retention of onlay grafts depends primarily on its cor-
depends on their ability to obtain metabolites from the recipient bed tical-cancellous composition.16Y18 Grafts that are mostly cortical,
during the first few days after transplantation. Eventually, angio- such as cranial bone, resorb less than grafts that have a greater can-
genesis from the recipient site provides critical substrates to the cellous composition, such as rib or iliac crest.17,19Y21
graft. Vessel penetration is relatively slow and cannot be relied on This difference has been largely attributed to revasculariza-
to prevent cellular demise; osteocyte/osteoblast death occurs after tion.18,21,22 Although revascularization is generally considered de-
25 hours of ischemia.12 The diffusion of nutrients and oxygen from sirable for bone cell survival, it proceeds by osteolysis and works to
the environment favors the cells on the surface of the graft. Thick deplete volume. Osteoclasts carve out small channels, termed cut-
or large cortical grafts have a greater percentage of cells on their ting cones, which becomes the conduit for vessel growth. New bone
interior that do not survive. Only viable surface osteocytes and gradually fills the defect as the cutting cone extends deeper into the
osteoblasts participate in bone healing, but the nonviable interior graft. The rate of revascularization and graft replacement de-
remains osteoconductive and serves as a scaffold for new bone pends strongly on the graft microarchitecture, specifically the sur-
growth. It will gradually be replaced with viable bone by the rela- face areaYtoYvolume ratio.21,23,24 This ratio is much higher in
tively slow process of creeping substitution. Until this exchange is cancellous than cortical grafts. Consequently, the rate of revascu-
complete, the dead bone remains more susceptible to infection and larization is much higher in the former than in the latter tissue. Thus,
structural damage. graft revascularization depends on bone microarchitecture and not
Although surface osteocytes are most likely to survive trans- whether the graft is from a cortical or cancellous source per se.17
plantation, they may be compromised during harvest and storage. We recently reported that onlay particulate cranial graft, which is
Thermal injury can result from power instruments used to harvest derived principally from cortical bone, undergoes resorption simi-
or contour the graft. Limiting the use of power tools and irrigating lar to cancellous graft.25 In the orthopedic literature, Tagil et al26
the graft with cold water when such instruments are used can miti- showed that impacting morselized bone graft to make it more cor-
gate heat damage. Desiccation or osmotic damage to the cells can tical decreased revascularization and replacement.
occur while the graft is stored outside the body; the best media is a Although the high surface-to-volume relationship of can-
blood-soaked sponge. cellous bone promotes greater revascularization, it also can have a
Bone cell survival also can be reduced if the recipient bed positive effect relative to the potential for graft osteoinductive and
is impaired. A recipient site complicated by infection, hematoma, osteogenic. These biologic processes are more active in the heal-
radiation, and/or scar will limit the transfusion of nutrients to and ing of cancellous grafts than cortical grafts for 2 reasons. First, the
neovascularization of the graft. When a large graft is required, or relatively large surface areaYvolume relationship of cancellous grafts

324 * 2012 Mutaz B. Habal, MD

Copyright © 2012 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery & Volume 23, Number 1, January 2012 Autogenous Bone Graft

means that a high proportion of osteoblasts and osteocytes will sur- ized than cortical bone. Thus, rapid vascularization of an onlay graft
vive transfer and contribute to new bone formation. This is not the is detrimental to volume retention. In support of this tenet, we re-
case for cortical grafts, especially if they are large or thick. Second, cently demonstrated that abrading the cortical surface under onlay
rapid revascularization of cancellous grafts releases osteoinductive cranial graft leads to greater bone resorption through increased re-
mediators, such as bone morphogenic protein, into the recipient vascularization and osteoclast activity. The osteogenic potential of
environment and promotes differentiation of bone-producing cells the recipient bed largely explains the disparate behavior of identi-
around the graft. Bone microarchitecture can explain much, but not cal autogenous materials in different environments and should be
all, of the clinical behavior of an autogenous graft. The remaining considered when choosing a graft.
piece of the puzzle is the interaction of the graft with tissues in the
recipient bed. CLINICAL APPLICATIONS
The biology of autogenous bone graft discussed above forms
the groundwork for its clinical use:
Recipient Bed: Inlay Versus Onlay (1) Bone viability should be ensured throughout the harvest, stor-
The interplay between the recipient bed and bone graft leads age, and placement of the graft. Dead bone has no osteogenic
to interesting and seemingly enigmatic, biologic questions. For ex- potential, has limited osteoinductive capacity, and heals pri-
ample, onlay cancellous grafts undergo significant resorption. How- marily by creeping substitution. Clinically, this can lead to delay
ever, when placed over dura, their volume increases. Rosenthal and in graft healing, a reduced capacity to withstand mechanical
Buchman27 found that both cortical and cancellous inlay grafts in- stresses, and an increased potential for resorption and infection.
crease in volume after placement, but the cancellous bone was found The viability of nonvascularized bone depends on the size and
to have a greater volume increase. However, each graft type undergoes thickness of the graft, as well as the angiogenic/osteogenic po-
some resorption when used to onlay bone. We have noted similar tential of the recipient bed. Vascularized bone may be superior
behavior with particulate cranial bone graft.25,28 Although mechani- for situations where bone viability is critical (eg, load bearing)
cal theories have been proposed to explain this apparent dichot- or when the recipient bed is significantly compromised.
omy, they are too simplistic. One study found that isolating bone (2) Autogenous bone, regardless of its cortical/cancellous compo-
graft from the pericranium with a double-layer collagen membrane sition, generally will retain volume when placed over normal
actually improved graft retention.29 Although this affected revascu- dura (inlay). In the inlay position, the balance between osteo-
larization, it minimally influenced forces applied to the graft from genesis and resorption is weighted toward osteogenesis. Be-
the overlying tissues. cause the dura is important for osteogenesis, graft survival
The principal difference in the environment between inlay should be expected to decrease if the dura is scarred. Cancellous
and onlay grafts used on the cranium is contact with the dura, be- grafts tend to increase in volume more than cortical grafts and
cause both are typically covered by pericranium. Although most hence may have a slight advantage over cortical bone for inlay
surgeons consider pericranium critical for cranial graft healing, it applications.
is considerably less important than the dura.30Y33 The contribution (3) Bone grafts placed over intact bone (onlay) tend to resorb. For
of pericranium to inlay graft healing is limited to the graft surface, onlay grafts, the balance between osteogenesis and resorption
whereas osteogenesis from the dura extends throughout the graft.32 favors resorption. Because cortical bone revascularizes more
Isolation of inlay bone graft from the overlying pericranium has slowly than cancellous bone, the former graft material generally
minimal effect on graft survival or volume retention, whereas iso- has better volume retention than the latter. Abrading the re-
lation from the dura causes a significant decrease in volume.33 cipient site increases revascularization and causes greater, not
Some investigators have noted improved onlay graft survival when less, graft resorption.
the bone is rigidly fixed and the periosteum is included with the Cranial bone is our preferred grafting material because (1)
graft.34Y38 Others have found that periosteum does not effect graft a remote donor site is not required; (2) there is less donor-site
survival39 or may even promote revascularization and resorption.29 morbidity compared with harvesting rib or iliac bone; and (3) cra-
This is particularly true in areas of the craniofacial skeleton that nial graft has better volume maintenance than rib or iliac bone.
exhibit ‘‘resorptive’’ tendencies.40 One misconception regarding cranial bone is that there is a limited
Overall, the impact of dural-mediated osteogenesis super- amount that can be harvested, particularly in young children. This
sedes the osteolytic byproduct of revascularization for inlay graft perception is one reason why endochondral bone and/or alloplas-
and typically leads to a gain in volume. For onlay grafts, the more tic materials are often used for craniofacial reconstruction. Re-
attenuated osteogenic role of the pericranium does not keep pace cently described techniques using cranial particulate bone graft,
with bone resorption consequent to revascularization, and there is however, allow the expansion of the cranial donor site. Almost all
a net loss of bone. The loss of onlay graft volume is more pro- inlay defects, in patients of any age, may now be reconstructed with
nounced for cancellous bone because it is more readily revascular- autologous cranial graft.

FIGURE 1. Adult, New Zealand white rabbit with 17  17-mm critical-size parietal defect filled with particulate graft harvested from the frontal bone using
a hand-driven brace and bit. Sixteen weeks later, the defect has ossified; the bone is as thick as the surrounding cranium and contains a diploic space.
Note that the partial thickness donor sites have healed and can be used again to harvest additional particulate graft.

* 2012 Mutaz B. Habal, MD 325

Copyright © 2012 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Rogers and Greene The Journal of Craniofacial Surgery & Volume 23, Number 1, January 2012

FIGURE 2. A 24-month-old girl with a cranial defect following resection of a venous malformation. The area was filled with particulate bone graft harvested
from the adjacent ectocortex. The defect was clinically healed in 6 weeks; computed tomography at that time showing healing particulate graft without resorption.

The uses and advantages of particulate corticocancellous cra- defects allows the area to maintain greater strength compared with
nial bone graft have been extensively described (Figs. 1 and 2).41Y44 split cranial bone.
For cranial procedures, the donor site is already in the operative Particulate graft is best used to reconstruct inlay defects.
field so there is no additional operative morbidity. The graft can Similar to other types of cancellous grafts, the bone mass remaining
be harvested from the outer table of the cranium or from the inner after healing is equal to or greater than the mass that was originally
table of any bone segment using a hand-driven Hudson brace and placed into the defect. Over time, the graft becomes indistinguish-
D’Errico craniotomy bit (Codman & Shurtleff, Inc, Raynham, MA). able from the surrounding bone and can even form a diploic space.
The use of a manual drill prevents thermal injury and ensures This observation implies that the graft induces regional osteogenesis
maximal graft viability. The diameter and pitch of the cutting bit from the adjacent dura and pericranium. We refer to this process as
also can affect the graft survival. If the particles are too small, they reparative osteogenesis, because the body responds to the graft as if
will be digested by macrophages; if they are too large, the osteo- it were repairing a fracture. This is analogous to the mechanism of
genic and osteoinductive potential of the graft may be reduced. We bone ‘‘generation’’ used through distraction osteogenesis.
recently have shown that bone ‘‘dust’’ produced with a high-speed Because the dura is critical in this process, we have largely
drill resorbs when used as inlay graft because of osteonecrosis and refrained from placing the particulate graft over scarred dura. In-
diminutive particle size.25 stead, we have used the technique of exchange cranioplasty in these
Because the donor defects created during harvest of par- situations (Fig. 3).44 A full-thickness piece of bone is harvested
ticulate graft are partial thickness and less than critical size, they from the intact calvaria. We have limited harvest to areas behind
fill over time. Consequently, unlike split cranial bone, the donor sites the hairline to avoid any possible contour irregularities. The donor
return to normal thickness and can be used in the future to harvest defect is then back-filled with particulate graft derived from the
additional bone graft. For bone harvested from the ectocortical endocortex of the full-thickness segment or the ectocortex of the
surface, there is no need for neurosurgical assistance because the surrounding intact cranium. This technique can also be used to
inner table remains intact. Particulate graft can be harvested from harvest large segments of full-thickness bone for use as an onlay
areas of the cranium (eg, temporal, greater sphenoid wing, occiput) or in other areas of the craniofacial skeleton. Virtually any area of
that would be difficult to split or in children without a diploic intact cranium can be removed and replaced with particulate graft
space. The lattice of full-thickness bone between the donor-site harvested from the endocortical surface of the graft. In the unusual
situation where additional particulate graft is needed to fill the do-
nor site, it can be obtained from the ectocortex of the surround-
ing cranium. Because the thickness and integrity of the particulate
bone after healing are comparable to the surrounding native bone, it
can be harvested in the future as particulate, split, or full-thickness
donor bone. Thus, through cycles of harvest and healing, the cra-
niofacial surgeon can access a nearly endless supply of autogenous
cranial bone.

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* 2012 Mutaz B. Habal, MD 327

Copyright © 2012 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.

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