Tibial versus iliac bone grafts:a comparative examination in15 freshly preserved adult cadavers

Marcus GerressenAndreas PrescherDieter RiedigerDavid van der VenAlireza Ghassemi

Authors’ affiliations:Marcus Gerressen, Alireza Ghassemi, Departmentof Oral, Maxillofacial and Plastic Facial Surgery,University Hospital of the Aachen University(RWTH), Aachen, GermanyAndreas Prescher, Institute of Neuroanatomy,University Hospital of the Aachen University(RWTH), Aachen, GermanyDieter Riediger, Department of Oral, Maxillofacialand Plastic Facial Surgery, University Hospital ofthe Aachen University (RWTH), Aachen, GermanyDavid van der Ven, Dental Practice, Gelsenkirchen,Germany

Correspondence to:Dr Dr Marcus Gerressen, Department of Oral,Maxillofacial and Plastic Facial Surgery, UniversityHospital of the Aachen University (RWTH)Pauwelsstra�e 30, 52074 Aachen, GermanyTel.: þ 49241 8035438Fax: þ 49241 8082430e-mail: Marcus.Geressen@post.rwth-aachen.de

Key words: tibial bone graft, corticocancellous iliac graft, autogenous bone, graft volume,

histomorphometric bone density

Abstract

Purpose: We compared autogenous bone grafts from the proximal tibia and the anterior

iliac crest under standardized conditions with regard to the attainable bone amount and

the histological bone density.

Material and methods: In 15 freshly preserved adult cadavers, a corticocancellous block

graft from the anterior iliac crest and a purely cancellous transplant from the tibia of the

homolateral side were harvested respectively, with the length of the skin incision set at 6 cm

for the iliac and at 3.5 cm for the tibial approach. The size of the iliac graft was defined to

be between 1/3 and 1/4 of the total iliac length. At the medial tibia the maximum possible

amount of cancellous bone was collected after preparation of a cortical lid. For volume

determination grafts were cautiously cut up and then put in a water-filled measuring

cylinder. In addition, bone density was measured by histomorphometry. The received data

were statistically evaluated using the t-test for related samples at P¼0.05 and Pearson’s

correlation analysis.

Results: From both donor sites approximately equal amounts of bone were available. This

result is neither dependent on age nor on gender. In contrast, bone density turned out

significantly higher in the iliac graft, with the difference showing a significant age

dependence (r¼ �0.556).

Conclusions: Provided that no cortical transplants are needed, cancellous tibial bone grafts

offer an appropriate alternative to the classic iliac bone graft, especially in elderly patients.

Bone deficit and bony defects are frequent

conditions in the maxillofacial region. To

replace the missing hard tissue bone graft-

ing is often necessary with the amount of

bone needed being dependent on the size

and the geometry of the defect (Boyne &

Herford 2001; Herford et al. 2003). Cysts,

traumatic bone loss and congenital bony

defects, such as alveolar clefts, as well as

bony defects subsequent to tumor resection

are major indications for bone transplanta-

tion (Foitzik & Vietor 1996; Besly & Ward

Booth 1999; Aboul-Hosn et al. 2006).

However, in the recent years grafting tech-

niques which provide the atrophic edentu-

lous posterior maxilla with an adequate

bone stock for osseointegrated implants

are gaining more and more importance. In

particular, the sinus floor elevation, as first

described by Tatum at the implant meeting

held in Birmingham, Alabama, in 1976

and published subsequently by Boyne &

James (1980), has become an undisputed

standard pre-implantology procedure for

the maxilla (Boyne & James 1980; Tatum

1986).

Date:Accepted 16 May 2008

To cite this article:Gerressen M, Prescher A, Riediger D, van der Ven D,Ghassemi A. Tibial versus iliac bone grafts: acomparative examination in 15 freshly preserved adultcadavers.Clin. Oral Impl. Res. 19, 2008; 1270–1275doi: 10.1111/j.1600-0501.2008.01621.x

1270 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

Countless grafting materials have been

developed and utilized, but in spite of the

continuous progress of bone-substitute

technologies the autogenous bone graft

is currently still considered the gold

standard (Mendicino et al. 1996; Jensen

et al. 1998; Lundgren et al. 1999;

Jakse et al. 2001; Allegrini et al. 2003;

Tiwana et al. 2006) due to its superior

properties with regard to osteoinductivity,

osteoconductivity and immunogenecity

(Moy et al. 1993; Triplett & Schow

1996;Serra E Silva et al. 2006). Especially,

autogenous spongiosa is attributed to be of

high biological value (Jensen et al. 1990;

Tidwell et al. 1992; Jensen et al. 1998;

Jakse et al. 2001).

Undoubtedly, the ilium is the most

widely used extraoral donor site for auto-

genous bone grafts (Herford et al. 2003;

Tiwana et al. 2006). Nevertheless, the

proximal tibia is likewise a reliable bone

graft donor site (O’Keeffe et al. 1991), and

is becoming more popular also for maxillo-

facial bone defects in the more recent past

(Catone et al. 1992; Besly & Ward Booth

1999; Jakse et al. 2001; Lee 2003; Aboul-

Hosn et al. 2006; Thor et al. 2006; Tiwana

et al. 2006). It offers some distinct advan-

tages. First, the surgical procedure is rela-

tively simple and can be performed under

local anaesthesia. In addition, a sufficient

amount of cancellous bone can be har-

vested with only minimal morbidity

(O’Keeffe et al. 1991; Besly & Ward Booth

1999; Jakse et al. 2001; Herford et al.

2003). However, the cortical bone available

from this donor site is essentially limited to

the access window.

In our current study, bone harvesting

from the proximal medial tibia using the

bone lid method according to Jakse (Jakse

et al. 2001) (Fig. 1) was systematically

compared to the anterior iliac crest donor

site with regard to the attainable bone

amount and histological bone density.

Material and methods

Patients

Fifteen freshly preserved human cadavers,

nine male and six female, with their age

ranging from 51 to 94 years (mean 76.8

years) were recruited into this study. In all

cadavers a corticocancellous block graft

from the anterior iliac crest and a purely

cancellous transplant from the tibia of the

homolateral side were harvested respec-

tively under standardized conditions.

Surgical procedure and harvesting of thebone grafts

The harvesting procedure at the iliac crest

was performed as follows (Fig. 2): Starting

with a skin incision set at a length of 6 cm

and running in direction of the tension

lines 3–4 cm cranially to the anterior super-

ior iliac spine, the abdominal muscles were

divided by sharp dissection, then the iliac

crest and the inner surface of the iliac ala

were carefully exposed (Fig. 2a). Subse-

quent to completion of the osteotomy

(Fig. 2b) to the desired size being one

quarter to one third of the total iliac length,

a corticocancellous block graft was re-

moved with preservation of the outer cor-

tical layer and further cancellous bone was

collected from the adjacent marrow space

using appropriately sized Volkmann’s

spoons. On balance, the harvesting trauma

was reduced to a justifiable extent by

refraining from a large approach, excessive

dissection of the soft tissue and thus

the maximum possible bone removal

which would be inextricably linked with

long immobilization and comparatively

much discomfort when treating ‘‘real’’

patients.

At the tibia (Fig. 3), the important ana-

tomic landmarks such as the articular cav-

ity, the tibial tuberosity and the medial

tibial margin were first identified and high-

lighted (Fig. 3a). An incision line of about

3.5 cm was drawn from craniomedially to

caudolaterally according to the oblique fi-

bers of the pes anserinus with the proximal

limit 2 cm below the articular cavity. After

the pes anserinus had been exposed by

sharp and blunt dissection, a cortical lid

with a size of 1.8 � 1.5 cm was prepared as

proposed by (Jakse et al. 2001) For that,

first incisions were performed through the

pes anserinus corresponding to the design

of the planned bone lid whose cranial and

caudal sides should run parallel and whose

lateral side should run perpendicular to the

fibers of the pes anserinus (Fig. 3b). Medi-

ally, the pes remained untouched; thus the

cortical lid prepared by using a micro bone

saw and different chisels remained retained

at its medial base (Fig. 3c). Then, the

maximum possible amount of cancellous

bone was gathered with suitable spoon

excavators.

Determination of volume and histomor-phometric analysis

For determination of their respective

volumes the grafts were cautiously cut up

by a bone saw and / or a Luer’s bone

rongeur; the bone pieces were put in a

1 ml calibrated 250 ml measuring cylinder

filled with 50 ml water. The respective

bone volume equaled the measured total

volume minus 50 ml. In order to perform a

histomorphometric evaluation of the bone,

Fig. 1. Position of the cortical lid in the medial

proximal tibia.

Fig. 2. (a) Medial portion of the iliac crest and inner

surface of the iliac ala after blunt dissection of the

iliacus muscle retracted by a large abdominal spa-

tula. (b) Surgical site subsequent to osteotomy of a

monocorticocancellous block from the iliac ala.

Gerressen et al . Tibial versus iliac bone grafts

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 1271 | Clin. Oral Impl. Res. 19, 2008 / 1270–1275

histological sections were prepared from

each bone graft by the sawing and grinding

technique according to Donath (Donath &

Breuner 1982), and subsequently were

stained with Giemsa in the customary

manner. Bone density defined as the per-

centage proportion of mineralized tissue

to the entire tissue was estimated using

a computer-based histomorphometric

analysis system comprising a Zeiss light

microscope (model diaplan, Carl Zeiss

MicroImaging GmbH, Gottingen,

Germany) connected with a personal com-

puter via charged coupled device camera,

and the analysis software Leica QWin

(Leica Mikrosysteme Vertriebs GmbH,

Bensheim, Germany). With the camera’s

live image being displayed on the PC

screen, the sections of each graft were first

surveyed at a magnification of � 40 to

obtain an overview about the different

compartments of each slide. While scruti-

nizing the sections at a magnification

of � 160 the area of mineralized tissue

within the measuring frame of

229456.7 mm2 determined by the software

was measured in 50 visual fields. For this

purpose all bony structures within the

frame were outlined with the mouse cursor

whereupon the included area was colored,

calculated and added-up automatically by

the software (Fig. 4). Subsequently, the

sum of all measured areas was put in

proportion to the overall area of the 50

measuring frames and thus, bone density

was determined.

Statistical analysis

In addition to an explorative data analysis,

a t-test for related samples was performed

to statistically compare the measured graft

volumes as well as the ascertained values

for bone density. The influence of gender

on the results was examined by means of

an unpaired t-test. Values of Po0.05 were

considered significant. For assessment of

age-dependence Pearson’s correlation ana-

lysis was done. Statistical computations

were performed using the Statistical Pack-

age for Social Sciences (SPSS), version 14,

under Windows XP.

Results

Graft volume and histomorphometricanalysis

On the whole, both donor sites, the iliac

and the tibial one, provide at least satisfac-

tory amounts of autogenous bone and show

acceptable results in regard to the bone

density of the corresponding transplants

(Table 1).

The mean graft volume presents margin-

ally higher values for the tibial donor site,

however the difference compared with the

iliac graft is not statistically significant

(Fig. 5) and in accordance to the 95%

confidence interval for the difference in

mean values, both donor sites must be

assumed equal regarding the attainable

bone amount (Table 2). This result is

neither dependent on gender nor on age

as it could be revealed by means of an

unpaired t-test and Pearson’s correla-

tion analysis for the differences of the

respective values for both types of trans-

plant. In contrast, the histomorphometri-

cally determined bone density turned out

significantly higher in the iliac graft show-

ing a mean density of 22.3% in comparison

to 16.7% for the tibial transplant (Fig. 6).

This difference in bone density is signifi-

cantly dependent on age (r¼ � 0.556;

Fig. 7), whereas a gender-dependence could

be statistically ruled out (P¼0.09). Conse-

quently, with advanced age the different

bone densities of both grafts lose relevance.

Fig. 3. (a) Left-sided cadaver shank showing the position of the incision line (black arrow) in relation to the

neighbouring anatomic landmarks. (b) Pes anserinus with incision lines placed corresponding to the planned

bone lid after dissection of the overlying soft tissue. (c) Access to the bone marrow of the proximal tibia after

preparation of the medially retained cortical lid.

Gerressen et al . Tibial versus iliac bone grafts

1272 | Clin. Oral Impl. Res. 19, 2008 / 1270–1275 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

Further statistical analyses

If, in a further step, both donor sites are

considered separately from each other, the

iliac crest of the male cadavers provides

markedly higher graft volumes as well as

bone densities when compared with the

female cadavers (Table 3). Overall, the iliac

graft volumes prove to be relatively con-

stant in the observed age interval (r¼0.4),

whereas the bone density suggests a ten-

dency towards age-dependence (Fig. 8). In

contrast to the above findings, the tibial

transplant shows neither age nor gender

dependence in regard to the examined para-

meters (Table 4).

In summary, both donor sites provide

comparably good results regarding the graft

volume whereas the iliac crest is distinctly

superior concerning the bone density of the

corresponding transplants.

Discussion

The primary purpose of this investigation

was to scientifically examine the tibial in

comparison to the iliac donor site regarding

attainable graft amount and histological

bone density. Numerous studies have

discussed the properties of either iliac or

tibial grafts (Kraut & Judy 1993; Lindberg

et al. 1996; Caminiti et al. 1999; Lee

2003; Aboul-Hosn et al. 2006; Tiwana

et al. 2006), but literature is lacking in

examinations with an intraindividual com-

parison of these two donor sites. As second

important issue the characteristics of both

grafts themselves were systematically ana-

lyzed in regard to age-dependence and sex

specifity.

What is important we wanted to exam-

ine the possible bone graft amounts under

practically relevant and realistic condi-

tions. Of course it would have been theo-

retically possible to choose a larger

approach at the iliac crest and to harvest a

maximum sized bone block. However,

most of the patients undergoing a bone

transplantation in the maxillofacial region

attach importance to rapid mobilization, a

short hospital stay and tolerable pain.

Major complications as fractures in the

harvesting area, a permanent sensory dis-

turbance or remaining gait problems should

be avoided. Therefore we decided on the

described harvesting method which we, in

our experience, can also expect of our ‘real’

patients.

In general, there is a relatively low but

significant morbidity associated with the

iliac crest donor site. Younger & Chapman

(1989) reported a rate of major complica-

tions of 9.2%, whereas minor complica-

tions were observed in 20.7% of the

examined cases. Sensibility impairment of

the lateral femoral cutaneous nerve (LFCN)

Table 1. Survey of the measured graft properties

Patient no. Age/years Gender Graft volume/ml Bone density/%

Iliac crest Tibia Iliac crest Tibia

1 94 Female 8 5 14.85 20.142 67 Male 6.8 11 40.51 24.593 88 Male 14 12.5 16.24 19.474 53 Male 9 15 38.44 17.555 78 Male 13 9 27.83 17.996 69 Female 7 6.5 15.08 11.437 88 Male 8 13 9.4 7.868 75 Male 8 9 37.41 30.199 89 Female 7 8 6.54 14.49

10 93 Male 14 14 10.75 15.5411 71 Male 11 11 36.19 16.4412 76 Male 9.5 10 31.38 17.2613 84 Female 10 16 11.25 9.0414 51 Female 6 9.5 8.71 12.4715 76 Female 6 9.5 30 16.44

15.0

Comparison of the graft volumes

12.5

10.0

7.5

5.0

Iliac crest Tibia

Fig. 5. Boxplot presentation for comparison of the

determined graft volumes (in millilitres).

Fig. 4. Screenshot of the working window of the employed Leica QWin software during determination of the

bone area: after the trabecula have been outlined by the mouse cursor in their entire circumference, they are

dyed green and their area is ascertained automatically by the software.

Gerressen et al . Tibial versus iliac bone grafts

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 1273 | Clin. Oral Impl. Res. 19, 2008 / 1270–1275

is described in o1% of the patients (Men-

dicino et al. 1996). In an own retrospective

study of 319 patients with non-vascular-

ized grafts from the iliac crest (unpublished

observations), we were able to reveal, that

sensory disturbances in the dermatom of

LFCN as well as postoperative pain are

significantly dependent on the bone

amount harvested. Therefore a less inva-

sive harvesting procedure should reduce the

discomfort to the patient. However, the

proximal tibia as donor site excels by its

comparatively even lower morbidity. The

overall complication rates reported for this

procedure range from 1.3% to approxi-

mately 4% (O’Keeffe et al. 1991; Lee

2003). Major complications as fracture of

the proximal tibia are extremely rare (Thor

et al. 2006).

When considering the bone amounts, it

is notable that in particular for the tibial

donor site, the graft volumes turn out lower

as reported in the literature. These values

vary between 20 and 40 ml for tibial grafts

and between 7 and 40 ml for transplants

from anterior iliac crest (Kraut & Judy

1993; Foitzik & Vietor 1996; Herford

et al. 2003; Aboul-Hosn et al. 2006;

Tiwana et al. 2006). In the study in hand,

the transplants from the proximal tibia

show on average 10.6 ml (range 5–16 ml,

Table 1) bone amount, a markedly smaller

volume. In the iliac crest, for which a mean

graft volume of 9.15 ml (range 6–14 ml)

was measured, the difference to reported

values is less obvious. A possible reason for

the comparatively small volumes in our

collective could be older age of the cadavers

(76.8 years), but on the other hand neither

the graft volumes for the tibial (r¼ � 0.06)

nor for the iliac grafts (r¼0.402) exhibit

age dependence in the examined age inter-

val. Furthermore, our applied measuring

method consisting of volume displacement

of water could play an important role,

since, in contrast to the simple determina-

tion of volume by a syringe or a measuring

jug (Lindberg et al. 1996), the hollow

spaces between the bone pieces do not

affect the measured volume. Nonetheless,

bone amount obtained from each donor site

is sufficient to perform sinus lifting, one of

the most important indications for harvest-

ing autogenous bone grafts, at least unilat-

erally (Lee 2003).

Due to the significantly higher bone

density and bone volume comparable to

the tibial transplants, grafts from the iliac

crest may have a better osteogenetic poten-

tial as they provide a higher amount of

osteoinductive and osteoconductive mate-

rial in the recipient site. However, the bone

density difference disappears with age, so

that especially in older patients both graft

types should lead to comparably acceptable

treatment results.

An influence of gender was only found

out for the iliac graft. The acquired data

indicate that in men larger grafts with

60.00

35.00

30.00

25.00

20.00

15.00

10.00

5.00

80.00 100.00

Age

His

tolo

gica

l bon

e de

nsity

Fig. 8. Points cluster for illustration of the relation

between bone density and patients’ age in iliac crest

transplants (r¼ �0.463).

Table 2. Statistical comparison between both donor sites

Donorsite

Meanvalue

Standarddeviation

t-Test

P-value 95 %confidence interval

Graft volume Iliac crest 9.15 ml 2.7 0.095 [3.18; 0.289]Tibia 10.6 ml 3.1

Bone density Iliac crest 22.3 % 12.5 0.042 [0.23; 10.92]Tibia 16.7 % 5.7

45

40

35

30

25

20

15

10

5

Iliac crest Tibia

Comparison of the bone density

o8

Fig. 6. Comparative presentation of bone density (in

percent) arisen for the iliac and for the tibial grafts.

25.00

20.0015.0010.005.00

0.00

–5.00

–10.00

Diff

eren

ces

in b

one

dens

itybe

twee

n ili

ac a

nd ti

bial

gra

fts

60.00 80.00 100.00

Age

Fig. 7. Relationship between the bone density differ-

ence and patients’ age revealing a significant correla-

tion (r¼ � 0.556).

Table 3. Dependence on gender in the iliac graft

Gender Meanvalue

Standarddeviation

t-test

P-value 95 % confidence interval

Graft volume Male 10.4 ml 2.7 0.029 [0.36; 5.71]Female 7.3 ml 1.5

Bone density Male 27.6 % 12.3 0.04 [0.69; 25.64]Female 14.4 % 8.3

Table 4. Dependence on gender in the tibial graft

Gender Meanvalue

Standarddeviation

t-test

P-value 95 % confidence interval

Graft volume Male 11.6 ml 2.1 0.123 [� 0.78; 5.83]Female 9.1 ml 3.8

Bone density Male 18.54 % 6.2 0.135 [� 1.62; 10.71]Female 14.0 % 3.9

Gerressen et al . Tibial versus iliac bone grafts

1274 | Clin. Oral Impl. Res. 19, 2008 / 1270–1275 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

higher bone density can be harvested.

Thus, hormonal as well as constitutional

factors seem to be more relevant to the iliac

crest than to the tibia.

In conclusion, for indications not

requiring cortical bone transplants

cancellous grafts from proximal tibia

represent a real alternative to the widely

spread iliac bone graft, particularly in

elderly patients and irrespective of

gender.

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c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 1275 | Clin. Oral Impl. Res. 19, 2008 / 1270–1275