Complications inBone Grafting

Alan S. Herford, DDS, MD*, Jeffrey S. Dean, DDS, MD

KEYWORDS

� Bone grafts � Autogenous grafts � Bone harvest� Graft complications

s.com

Bone grafts are often necessary to restore missingtissue and to provide structural support forimplants. Alveolar bone remodeling/resorptionafter tooth extraction can make it difficult to placeimplants in adequate bone. This can result ina poor aesthetic outcome and possible prematureloss of the implants.1,2 The need for maxillary andmandibular bone grafting is often necessary toprovide adequate bone for implant placement.Various types of grafting material can be used toaugment the deficient alveolus, including the useof autogenous bone. Autogenous grafts remainthe gold standard because of their osteogenicproperties and because they are more predictablethan allografts or xenografts, especially for largerdefects.

The uses of cortical and cancellous bone havedifferent indications and require a thorough under-standing of what the indications are for each. Boneheals by cellular regeneration and it is this cellularregeneration that allows bone grafts to form bonerather than forming scar. The osteogenic proper-ties of autogenous bone make it an ideal choicefor bone grafting and is more predictable whengrafting large defects. Selecting an augmentationmaterial for grafting requires knowledge of thematerial being used with regards to biocompati-bility, bioresorbability, structural stability, avail-ability, ease of handling, and costs.

With the biologic and technical demands asso-ciated with bone grafting, various complicationscan occur. It is important to understand andmanage complications associated with bonegrafting to minimize poor outcomes and failure.Complications may result from the harvesting of

Department of Oral and Maxillofacial Surgery, Loma LiCA 92350, USA* Corresponding author. Department of Oral and Mof Dentistry, Room 3306, 11092 Anderson Street, Loma LE-mail address: aherford@llu.edu

Oral Maxillofacial Surg Clin N Am 23 (2011) 433–442doi:10.1016/j.coms.2011.04.0041042-3699/11/$ – see front matter � 2011 Elsevier Inc. All

the bone graft or may develop secondarily at thegrafted site. Donor site complications includedamage to local anatomic structures—teeth,nerves, muscles, vasculature, and infection (iliaccrest bone graft complications have been ashigh as 15%–25%)—and the recipient site withpossible complications of sinus disease, early ordelayed exposure of the graft, or resorption ofthe graft and infection.3–6 Complications associ-ated at the grafted site may lead to larger defectswith loss of bone volume and soft tissue defects.Further interventions to correct the problem(additional grafting with associated donor sitemorbidity) may be necessary.

BIOLOGY OF BONE FORMATION

The biology of bone formation involves osteogen-esis, osteoconduction, and osteoinduction. Os-teoprogenitor cells found within bone are stemcell precursors that can differentiate into variousconnective tissue lines. Corticocancellous blockbone is still a viable choice in grafting and isused successfully. Cancellous bone, consideredthe gold standard in grafting, provides the greatestamount of osteoprogenitor cells and allows forrapid vascularization. Bone morphogenic proteinsare released from the mineral matrix in bone toinduce stem cells within the graft to form maturebone.7

HARVEST SITES

Many sites are available for graft harvest, includinglocal and distant sites (Table 1). Consideration as

nda University, 11092 Anderson Street, Loma Linda,

axillofacial Surgery, Loma Linda University Schoolinda CA 92350.

rights reserved. oralmaxsurgery.theclinic

Table 1Harvest sites

Donor Site Type of Graft Volume Available Possible Complications

Ascending Ramus Cortical 5–10 cc Damage to the neurovascularbundle with resultingtemporary or permanentneurosensory disturbance

Symphysis Corticocancellous 5–10 cc Ectropion of the lower lip andchin ptosis

Damage to the teeth andmental nerve withneurosensory disturbance

Tuberosity Cancellous 2 cc Oroantral communication

Tibia Cancellous 20–40 cc Tibial plateau fractureInterference with growthplate in children

Cranium Cortical 20–40 cc Damage to dura and brain

Anterior Iliac Crest Corticocancellous 50–70 cc Gait disturbanceParesthesia of the lateral thighHerniaHematoma

Posterior Iliac Crest Corticocancellous 80–140 cc Gait disturbanceParesthesia of the posteriorregions

Hematoma

Herford & Dean434

to which site is used depends on the size andgeometry of the defect. The quantity and qualityof the bone needed are important when choosinga donor site. The technique chosen for grafting(particulate or block) also helps determines thepreferred donor site.

Local Sites for Bone Harvesting

Bone harvested from local sites has advantagesover other more distant donor sites (Fig. 1). Theproximity of the graft is of convenience and

Fig. 1. Local sites commonly used for harvest of grafts.

eliminates the possible complications from an ex-traoral site, such as scarring, gait disturbance, orneed for hospitalization. The grafts also providebone with similar architecture as the bone at therecipient site. A disadvantage is the limited amountof bone available compared with other extraoralsites.

Maxillary tuberosityBone harvested from the maxillary tuberosity haslimited use as a donor graft because of the smallvolume available. The graft material is cancellousand can be harvested with simultaneous thirdmolar removal. Complications associated withthis site include oral/antral communication andhematoma formation from disruption pterygoidvenous plexus.

Ascending ramusThe anterior portion of the ascending ramus hasbeenused for grafting in a variety of clinical applica-tions (Fig. 2). Bone harvested from the ascendingramusprovidesmainly a cortical graftwith avolumeof approximately 5 to 10 cc. The bone obtainedfrom the ramus is a good option for horizontaldefects requiring onlay grafting. These grafts healquickly, exhibit minimal resorption, and maintaintheir dense quality. Possible complications ofmandibular ramus graft site include damage to

Fig. 2. (A) Outline of graft to be harvested. (B) Use of a chisel to harvest ramus bone. The chisel should not bedirected toward the neurovascular bundle. (C) The uninjured neurovascular bundle is visualized after harvestof the graft. (D) Thickness of the graft. (E) Bone graft secured into place with screws. (F) Bone graft is wellintegrated with surrounding bone.

Complications in Bone Grafting 435

the neurovascular bundle with neurosensorydisturbance, infection, damage to tooth roots if ex-tending into an area of molar teeth, and trismus.The lingual nerve is also at risk during harvestfrom the ramus, either due to poor incision place-ment, aggressive retraction of a lingual flap, or

damage during suturing. Misch8 compared intrao-ral donor sites for onlay grafting before implantplacement and found that the ramus was associ-ated with fewer complications than the symphysisgraft as a donor site (Fig. 3). Silva and colleagues9

found that 8.3% of patients who had had bone

Fig. 3. Harvest area of the ramus and symphysisregion.

Herford & Dean436

harvested from the mandibular ramus reporteda sensory deficit whereas 16% of patients under-going harvest from the symphysis had a sensorydeficit.

Mandibular symphysisThe mandibular symphysis allows ease of accessto bone for grafting, good bone quality for local-ized repair, a corticocancellous block graftmorphology, and minimal graft resorption(Fig. 4).10,11 The graft can provide either a blockor particulate graft material. Bone harvestedcontains more cancellous bone than other intrao-ral sites, thus providing a greater amount of osteo-progenitor cells. The lower lip/soft tissue chin maybecome ptotic after surgery in this area with poormentalis muscle suspension.12 Incision in the

Fig. 4. Harvest of corticocancellous graft from thesymphyseal region.

labial vestibule rather than a sulcular approachallows preservation of the crestal bone andallows a more secure closure with reapproxima-tion of the mentalis muscle, resulting in less riskof chin ptosis. Clavero and Lundgren13 comparedsymphysis and ramus harvest sites and reporteda higher rate of altered sensation in patients inwhom bone was harvested from the symphysis.In their series of patients, 52% of patients(symphysis) still had some decreased sensitivityat 18 months after surgery. Patients who hadbone harvested from the ramus had what wasconsidered a permanent nerve injury. Infectionsare minimal for these harvest sites (<1%).14

Mandibular coronoid processBone harvested from the mandibular coronoidprocess is primarily cortical bone similar to calva-rial bone and can be used for up to 1-tooth and 2-tooth sites. The harvest can extend up to 5 mmbelow the sigmoid notch so as to not interferewith the inferior alveolar neurovascular bundle.5

Harvesting the bone is relatively easy and donethrough an intraoral approach dissecting the tem-poralis from its attachment. A side cutting bur orreciprocating saw is used to perform an osteotomyof the coronoid process.Advantages of this harvest site include no facial

scarring or damage to teeth. Possible complica-tions include trismus or damage to the buccalbranch of the trigeminal nerve.

Distant Sites for Harvesting Bone

Calvarial boneCalvarial bone can be used for facial, maxillary,and mandibular reconstruction (Fig. 5). It wasdescribed as an autogenous bone graft by Tessierin 1982.15 Calvarial bone is mainly cortical innature and generally used for onlay grafting. Har-vesting calvarial bone is relatively easy and safe.Partial-thickness and full-thickness calvarial grafts

Fig. 5. Harvest of a monocortical calvarial graft fromthe parietal bone.

Fig. 7. Harvest of bone from a medial approach.

Complications in Bone Grafting 437

can be used. The skull has 3 layers the outercortex, medullary space (diploe), and an innercortex. Gonzalez and colleagues16 found that theaverage thickness of the skull was 6.3 mm witha range of 5.3 to 7.5 mm. The posterior parietalbone having the greatest thickness and is thepreferred site for harvesting bone for grafting.The harvest site is covered by tissue that is usuallyhair bearing, which camouflages scarring.

Complications associated with harvesting cal-varial bone include the possibility of dural tear,epidural hematoma, alopecia, hematoma, infec-tion, contour deformity, and scarring with alopeciathe most common complication.

Tibial boneCatone and colleagues17 described the proximaltibia as a source for cancellous bone used inmaxillary reconstruction in 1992. It is relativelyeasy to harvest and can be done in the office asoutpatient surgery (Fig. 6). The volume of availablecancellous bone harvested from the proximal tibiacan be up to 40 cc. The lateral approach to thetibia for cancellous bone is over Gerdy tubercle.Gerdy tubercle is easily palpated, located betweenthe tibial tuberosity and the fibular head andhas no vital structures overlying it. A medialapproach has also been described. Herford andcolleagues18 compared the medial with the lateralapproach and found no statistical difference in the

Fig. 6. Proximal tibia anatomic structures.

mean volume of bone harvested from either site(Fig. 7). They also reported that the bone is closerto the skin and is more distant to vital structurescompared with the lateral approach.

The incidence of complications for tibial boneharvest ranges from 1.3% to 3.8%, whichcompares favorably with the 8.6% to 9.2% inci-dence of complications associated with harvestof iliac crest bone.17,18 Complications associatedwith tibial bone harvest may include prolongedpain, gait disturbance, wound dehiscence, osteo-myelitis, wound infection, hematoma, seroma,paresthesia, fracture, and violation of the jointspace. No tibial fractures have been reported.The risks of this procedure need to be discussedwith patients and, because gait disturbances

Fig. 8. Harvest site for the anterior iliac bone harvest.

Herford & Dean438

have been reported, patients should be consentedappropriately. Contraindications for harvestingbone from the tibia include the need for a blockgraft, growing patients, patients with a history ofknee injury or surgery, or patients with advancedarthritic disease.

Iliac crest boneBone harvested from the anterior or posteriorpelvis can provide a great quantity of graftingmaterial. The anterior iliac crest is a good sourceof cortical and cancellous bone for grafting. Upto 50 cc of cancellous bone can be harvestedfrom the anterior iliac crest. This approach canbe done in the operating room or in the ambulatorysetting. The bone is harvested with or withouta cortical segment. The incision is made approxi-mately 1 cm posterior to the anterior superior iliacspine and is carried down to the crest of the ilium.The skin is retracted medially to keep the incisionfrom lying directly over the crest, thus preventingirritation from clothing resting on the incision.Complications associated with iliac crest bone

grafts range from 0.76% to 25% (major) and9.4% to 24% (minor).19 These include bleeding,hematoma, perforation of the bowel, hernia, ileus,pain, gait disturbance, cosmetic deformity, injuryto sensory nerves, and infection. Fractures of theiliac crest can also be seen and are treatedconservatively.20 Care must also be taken to avoidinjury to the sensory nerves (Fig. 8). The nervesthat may be injured include the iliohypogastric,lateral femoral cutaneous, and the subcostal,which is a branch of the lateral cutaneousnerve.21–23 Joshi and Kostakis24 found in theirseries of 114 patients that 10% experienced painfor greater than 16 weeks and 23% experiencedsome difficulty in ambulation 6 weeks postopera-tively. In a prospective study by Rudman,25

patients did not have delayed ambulation or pro-longed hospitalization. These patients weretreated for alveolar clefts and represented a youngpatient population. Ahlmann and colleagues26

compared anterior and posterior iliac crest boneharvests in terms of harvest site morbidity. Thisstudy involved 88 consecutive patients (108 graft-ing procedures). The anterior approach was asso-ciated with more complications than the posteriorapproach, 8% versus 2%, respectively (Fig. 9).Postoperative pain was significantly of greaterduration after anterior harvests.

Fig. 9. Harvest site for the posterior iliac bone harvest.

COMPLICATIONS ASSOCIATED WITH THEGRAFTED SITE

Complications can also occur at the recipient site.Possible complications include loosening and/or

Complications in Bone Grafting 439

resorption of the graft, localized infection, ordamage to adjacent anatomic structures, suchas the neurovascular bundle.27 Damage to adja-cent teeth and complete loss of the graft are alsopossibilities. Even with tension-free closure,a significant amount of exposures of the under-lying graft occurs (Figs. 10–13). The earlier theoccurrence after placement of the graft, the morelikely loss of the entire graft may occur.28

Membranes (resorbable and nonresorbable) maybe placed to thicken the tissue over the graft andprevent or at least delay exposure of the graft.Membranes are routinely used as a part of theguided bone regeneration technique and aid inpreventing competing, nonosteogenic tissuefrom infiltrating the grafted bone.

A study by Louis and colleagues29 recentlyevaluated patients who received mandibular ormaxillary reconstruction with autogenous particu-late bone graft and titanium mesh for the purposeof implant placement. The mean augmentationfor all sites was 13.7 mm (12.8 mm in the maxillaand 13.9 mm in the mandible). Totals of 82implants were placed in the maxilla and 92implants were placed in the mandible. In themaxillary group, 7 (55%) sites had exposure ofthe titanium mesh and 16 (36%) sites wereexposed in the mandible (52% total). Thesuccess of the bone grafting procedure was

Fig. 10. (A) Radiograph showing failed implants and inadeand anterior approach. (C) The grafts are secured with scshowing the grafted bone in place.

97.72%. They concluded that titanium mesh isa reliable containment system for grafting andthe mesh tolerates exposure very well and givespredictable results.

The use of membranes may also contributeto complications. Chaushu and colleagues30

reported soft tissue complications, includingmembrane exposure (42 [30.7%] of 137); incisionline opening (41 [30%] of 137); and perforation ofthe mucosa over the grafted bone (19 [14%]of 137). Infection of the grafted site occurred in18 (13%) of 137 bone grafts. Alveolar ridgedeficiency location had a statistically significanteffect on the outcome of recipient site complica-tions. More complications were noted in the man-dible compared with the maxilla. Age and genderhad no statistically significant effect. Gielkensand colleagues31 performed a meta-analysis toevaluate the available evidence that barriermembranes prevent bone resorption in autologousonlay bone grafts. The primary outcome measurewas bone resorption. The search yielded 182 arti-cles. Although most investigators concluded thatthey had found evidence for the protective effectof barrier membrane on bone resorption in bonegrafts, the systematic review reveals that theavailable evidence is too weak to support this.Most of the included studies were animal experi-ments; thus, extrapolation to the human situation

quate bone. (B) Harvest of an iliac crest bone graft fromrews to prevent mobility of the graft. (D) Radiograph

Fig. 11. (A) Placement of graft harvested from the ascending ramus. (B) Exposure of the graft postoperatively. (C)Complete loss of the graft.

Herford & Dean440

is difficult. Most studies also had a small number oftest sites, and sample size justification was gener-ally not reported. Furthermore, ambiguity and lackof significance were found in many studies alongwith additional limitations, such as implantation

Fig. 12. Exposure of a titanium mesh within 1 weekpostoperatively.

site, unsuitable designs, and varying outcomemeasures. Gielkens and colleagues felt that basedon a systematic review of the literature, furtherevidence was needed to determine whetherbarrier membranes prevent bone resorption inautologous onlay bone grafts.

Fig. 13. Exposure of the titanium mesh months aftersurgery.

Complications in Bone Grafting 441

SUMMARY

Autogenous bone grafts continue to have wide usefor reconstructing alveolar defects because of themany advantages associated with them. Althoughcomplications are low, the harvest of bone graftsdoes have the risk of morbidity, which variesbased on the harvest site chosen. Patients shouldbe informed of possible complications associatedwith bone harvest as well as complications thatmany develop at the grafted site.

REFERENCES

1. Herford AS, Brown BR. Outpatient harvest of bone

grafts. Selected Readings in Oral and Maxillofacial

Surgery 2007;15:1–14.

2. Zouhary KJ. Bone graft harvesting from distant sites:

concepts and techniques. Oral Maxillofac Surg Clin

North Am 2010;22:301–16.

3. Raghoebar GM, Louwerse C, Kalk WW, et al.

Morbidity of chin bone harvesting. Clin Oral Implants

Res 2001;12:503–7.

4. Beirne JC, Barry HJ, Brady FA, et al. Donor site

morbidity of the anterior iliac crest following cancel-

lous bone harvest. Int J Oral Maxillofac Surg 1996;

25:268–71.

5. Sittitavornwong S, Rajesh G. Bone graft harvesting

from regional sites. Oral Maxillofac Surg Clin North

Am 2010;22:317–30.

6. Larson PE. Morbidity associated with calvarial bone

graft harvest. J Oral Maxillofac Surg 1989;47(8):

110–1.

7. Marx R. Bone and bone graft healing. Oral Maxillo-

fac Surg Clin North Am 2007;19:455–66.

8. Misch CM. Comparison of intraoral donor site for on-

lay grafting prior to implant placement. Int J Oral

Maxillofac Implants 1997;12:767–76.

9. Silva FM, Cortez AL, Morekira RW, et al. Complica-

tions of intraoral donor site for bone grafting prior

to implant placement. Implant Dent 2006;15:420–6.

10. Gapski R, Wang HL, Misch CE. Management of

incision design in symphysis graft procedures:

a review of the literature. J Oral Implantol 2001;27:

134–42.

11. Weibull L, Widmark G, Ivanoff CJ, et al. Morbidity

after chin bone harvesting—a retrospective long-

term follow-up study. Clin Implant Dent Relat Res

2009;11:149–57.

12. Chaushu G, Blinder D, Taicher S, et al. The effect of

precise reattachment of the mentalis muscle on the

soft tissue response to genioplasty. J Oral Maxillofac

Surg 2001;59:510–6.

13. Calvero J, Lundgren S. Ramus or chin grafts for

maxillary sinus inlay and local onlay augmenta-

tion: comparison of donor site morbidity and

complications. Clin Implant Dent Relat Res 2003;

5(3):154–60.

14. Pikos M. Mandibular block autografts for alveolar

ridge augmentation. Atlas Oral Maxillofac Surg Clin

North Am 2005;13:91–107.

15. Tessier P. Autogenous bone grafts taken from the

calvarium for facial and cranial applications. Clin

Plast Surg 1982;9:531–8.

16. Gonzalez AM, Papay FE, Zin JE. Calvarial thickness

and its relation to cranial bone harvest. Plast Re-

constr Surg 2006;117(6):1964–71.

17. Catone GA, Reimer BL, McNeir D, et al. Tibia-autog-

enous cancellous bone as an alternative donor site

in maxillofacial surgery: a preliminary report. J Oral

Maxillofac Surg 1992;50:1256–63.

18. Herford AS, King BJ, Audia F, et al. Medial ap-

proach for tibial bone graft: anatomic study and

clinical technique. J Oral Maxillofac Surg 2003;61:

358–63.

19. Fowler BL, Dall BE, Rowe DE. Complications associ-

ated with harvesting autogneous iliac bone graft.

Am J Orthop 1995;24:895–903.

20. Arribas-Garcia I, Alcala-Galiano A, Garcia AF, et al.

Fracture of the anterior iliac crest following mono-

cortical bone graft harvest in bisphosphonate-

related mandibular pathological fracture: a case

report. Oral Surg Oral Med Oral Pathol Oral Radiol

Endod 2009;107:e12–4.

21. Banwart JC, Asher MA, Hassanein RS. Iliac crest

bone graft donor site morbidity. A statistical evalua-

tion. Spine 1995;20:1055–60.

22. Seiler JG 3rd, Johnson J. Iliac crest atogenous bone

grafting: donor site complications. J South Orthop

Assoc 2000;9:91–7.

23. Chou D, Storm PB, Campbell JN. Vulnerability of the

subcostal nerve to injury during bone graft harvest-

ing from the iliac crest. J Neurosurg 2004;1:87–9.

24. Joshi A, Kostakis GC. An investigation of post-

operative morbidity following iliac crest graft har-

vesting. Br Dent J 2004;196:167.

25. Rudman RA. Prospective evaluation of morbidity

associated with iliac crest harvest for alveolar graft-

ing. J Oral Maxillofac Surg 1997;55:219.

26. Ahlmann E, Patzakis M, Roidis N, et al. Comparison

of anterior and posterior iliac crest bone grafts in

terms of harvest-site morbidity and functional

outcomes. J Bone Joint Surg Am 2002;84:716.

27. Rabelo GD, de Paula PM, Rocha FS, et al. Retro-

spective study of bone grafting procedures before

implant placement. Implant Dent 2010;19:342–50.

28. Roccuzzo M, Ramieri G, Bunino M, et al. Autoge-

nous bone graft alone or assoiated with titanium

mesh or vertical alveolar ridge augmentation:

a controlled clinical trial. Clin Oral Implants Res

2007;18:286–94.

29. Louis PJ, Gutta R, Said-Al-Naief N. Reconstruction

of the maxilla and mandible with particulate bone

Herford & Dean442

graft and titanium mesh for implant placement.

J Oral Maxillofac Surg 2008;66(2):235–45.

30. Chaushu G, Mardinger O, Peleg M. Analysis of

complications followingaugmentationwith cancellous

block allografts. J Periodontol 2010;81(12):1759–64.

31. Gielkens PF, Bos RR, Raghoebar GM. Is there

evidence that barrier membranes prevent bone

resorption in autologous bone grafts during the heal-

ing period? A systematic review. Int J Oral Maxillofac

Implants 2007;22(3):390–8.