Clinical Neurology and Neurosurgery 124 (2014) 8589

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Clinical Neurology and Neurosurgery

journal homepage: www.elsevier.com/locate/clineuro

Cryopreservation versus subcutaneous preservation of autologous

bone aps for Cranioplasty: Comparison of the surgical site infection
and bone resorption rates
Cheng-Hsin Cheng a,b,c , Han-Chung Lee a,c , Chun-Chung Chen c , Der-Yang Cho c ,
Hung-Lin Lin a,c, *
a

Graduate Institute of Clinical Medical Science, China Medical University, Taichung, Taiwan
Department of Neurosurgery, Tainan Municipal An-Nan Hospital, Tainan, Taiwan
c
Department of Neurosurgery, China Medical University Hospital, Taichung, Taiwan
b

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 30 December 2013
Received in revised form 18 June 2014
Accepted 22 June 2014
Available online 1 July 2014

Objective: Decompressive craniectomy is performed to treat malignant brain hypertension. Surgical site
infection (SSI) and bone resorption are common complications following cranioplasty, and the storage
method that minimizes such complication has yet to be identied.
Methods: Over a 10-year period, the details of 290 decompressive craniectomy procedures performed at
our trauma and stroke center were recorded. Bone aps from 110 patients were preserved in
subcutaneous pockets (SPs), and 180 were preserved via cryopreservation (CP).
Results: SSIs occurred in 20 cases (18.2%) in the SP group and 20 cases (11.1%) in the CP group (P = 0.129).
After dividing each group according to the traumatic brain injury (TBI) etiologies, we found that in the SP
group, the SSI rates in the TBI and non-TBI patients were 17.3% and. 20.7% (P = 0.899), respectively, and in
the TBI- and non-TBI CP-group patients, the SSI rates were 11.9% and. 9.7% (P = 0.864), respectively. The
average decrease in bone ap thicknesses were 1.14 mm in the SP group (n = 34) and 1.89 mm in the CP
group (n = 57), and this difference was signicant (P = 0.039).
Conclusions: In this series, the SSI rates were similar in the SP and CP groups. There was no signicant
difference when the patients were grouped by TBI etiology. The incidence of bone ap resorption in the
CP group was higher than that in the SP group. However, identifying of the method that yields superior
results might depend on the individual surgeon's preference and the available equipment.
2014 Elsevier B.V. All rights reserved.

Keywords:
Autologous cranioplasty
Surgical site infection
Cryopreservation
Subcutaneous pocket
Decompressive craniectomy

1. Introduction
The use of decompressive craniectomy (DC) for the treatment of
severe intracranial hypertension following trauma, tumor surgery,
or cerebrovascular accident reemerged in the mid-1990s [13].
When the patient survives the illness, cranioplasty with an
autologous bone graft or another reconstructive material is often
performed to repair the skull defect. Autologous bone aps remain
the among the of the most commonly used materials for delayed
cranioplasty, and their use was rst reported in the 1950s [4].

* Corresponding author at: Department of Neurosurgery, China Medical

University Hospital, 2, Yuh-Der Road, Taichung, Taiwan, Taiwan.
Tel.: +886 4 22052121 ext. 5034; fax: +886 4 22344055.
E-mail addresses: u701018.tw@yahoo.com.tw (C.-H. Cheng),
linhunglin0405@yahoo.com.tw (H.-L. Lin).
http://dx.doi.org/10.1016/j.clineuro.2014.06.029
0303-8467/ 2014 Elsevier B.V. All rights reserved.

Autologous bone aps need to be sterilely preserved for several

weeks or months until the cranioplasty can be performed. Several
storage methods are available for this purpose, and two popular
methods are currently in use. The rst method is preservation in a
subcutaneous pocket (SP). Nakajima et al. reported the method of
the subcutaneous preservation of bone aps in the thigh [5], and
Acikgoz et al. preserved bone aps between the abdominal fat and
the muscle layers [6]. This method requires additional surgical
procedures. The second favored method is cryopreservation (CP) of
the bone ap, typically in a deep freezer. The choice of method is
usually based on the surgeon's preference, and only a few
previously published papers have discussed whether one method
is superior to the other.
To clarify whether differences in the methods used to store
bone aps inuence the incidences of surgical site infection (SSI)
and bone ap resorption following cranioplasty, we retrospectively
reviewed the clinical results obtained from our patients who
underwent DC and delayed cranioplasty within a 10-year period.

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C.-H. Cheng et al. / Clinical Neurology and Neurosurgery 124 (2014) 8589

2. Materials and methods

Between May 2001 and May 2010, 430 patients underwent
cranioplasty in our trauma and stroke center. Patients with
cranioplasties that utilized bone cement, primary cranioplasties
due to traumatic skull fractures or skull bone tumors, and
craniectomies performed in other hospitals were excluded.
Consequently, 290 patients who underwent DC for malignant
brain hypertension and subsequent cranioplasty with autologous
bone aps were enrolled in this study. The standard procedure for
DC is to create a large frontotemporoparietal hemicraniectomy
(>8  8 cm) and dural opening. This technique was performed for
TBI, malignant infarction and hypoxic encephalopathy. DCs for
aneurysmal subarachnoid hemorrhage were performed with
pterional bone aps that were typically removed for intraoperative
brain swelling. The DCs for intracerebral hemorrhages (ICHs) and
tumors depended on the surgical procedures. Some basic patient
information is presented in Table 1.
For the majority of the study period, the bone aps were
routinely stored in our bone bank at a temperature of 70  C. Of the
study participants, 180 patients were included in this CP group. In
our standard CP procedure, the soft tissue attached to the bone ap
is removed completely, bacterial cultures are performed, the bone
aps are then are immersed in a Betadine solution for at least
30 min and a vancomycin solution (500 mg in 500 ml normal
saline) for another 30 min, wrapped in one layer of sterile glove and
one layer of a sterile plastic bag, and nally covered with two more
layers of sterile cloth. This package is placed into a deep freezer
within 30 min. On the day of the cranioplasty, the bone ap is
removed from the bone bank at the beginning of the operation. The
ap is again soaked in a Betadine solution for 30 min and a
vancomycin solution for 30 min prior to implantation.
From August 2003 to October 2006, our freezer in the bone bank
was not functioning. Therefore, we had to use the SP method to
preserve the bone aps. During this period, 110 bone aps were
stored in SPs. The standard procedure in our institution is to create
an SP in the anterolateral thigh. Soft tissue attached to the bone
ap is removed completely, and a bacterial culture is performed
then. The SP is created in the subcutaneous layer above the
muscular fascia. After carefully ensuring hemostasis, the bone ap
is inserted, and one 10 mm drainage tube is left in place. The thigh
wound was reopened, and the bone aps were retrieved at the
time of the cranioplasty.
SSI was dened as a surgical wound site that exhibited focal
erythema, pus-like discharge or wound rupture. Cases of infection
required an additional surgery for bone graft removal.
The microbiologic results are reported in Tables 4 and 5.

We were also interested in the incidence of bone ap

resorption. After cranioplasty, we compared the thicknesses of
the frontal bones and the bone aps via brain CT. We dened the
standard section of the brain CT using the bilateral frontal horns
and the foramen of Monro. The data were recorded by two
neurosurgeons who were blinded to the storage method. The
difference in the thickness of the bone ap edge compared to that
of the contralateral side (non-operative side) was dened as the
decreased thickness (Fig. 1). The interval for follow-up brain CT
was limited to within 612 months after cranioplasty.
Because most of the patients in our series had experienced
traumatic brain injury (TBI), we also divided each method group
into two subgroups based on etiology (i.e., TBI or non-TBI); the SSI
incidences in each subgroup were determined and are presented in
Table 2. The clinical characteristics of the patients who experienced SSIs are also summarized in Table 2.
Moreover, Inamasu et al. [7] has reviewed the literature related
to the incidence of SSI following cranioplasty. We have included
data from recently published reports in Tables 6 and 7.
Continuous variables are expressed as the mean  the standard
deviation and were compared using Students t test, and
categorical variables were compared using the Fishers exact test.
Differences that produced P values <0.05 were considered
statistically signicant.
3. Results
Basic data
There were fewer patients in the SP group than in the CP group
(110 vs. 180) because our freezer was broken for only 3 years.
During this period, we had to use the SP method to store the skull
aps. After the freezer was xed, the CP method employed.
For the SP group, the interval between DC and cranioplasty
ranged from 11 to 288 days (mean 61.24  60.95 days), and for the
CP group, this interval ranged from 9 to 358 days (mean
59.82  47.71 days). The timing of the cranioplasty was determined
by each neurosurgeon. The difference in this interval between the
groups was not statistically signicant (p = 0.829). These basic data
are summarized in Table 1.

Table 1
Basic patient data and infection rates.

Sex (M:F)
Age (yr)
Initial diagnosis
TBI
Malignant infarction
Spontaneous ICH
Subarachnoid hemorrhage
Tumor edema
Hypoxic encephalopathy
Surgical site infection
Duration of bony preservation (days)

SP group

CP group

(n = 110)

(n = 180)

P value

79:31
48.97  17.87

118:62
50.45  18.80

0.328
0.509
0.112

81 (73.6%)
18 (16.4%)
5 (4.5%)
4 (3.6%)
0 (0.0%)
2 (1.8%)
20 (18.2%)
61.24  60.95

118 (65.6%)
33 (18.3%)
11 (6.1%)
13 (7.2%)
5 (2.8%)
0 (0.0%)
20 (11.1%)
59.82  47.71

0.129
0.829

x2 test, Yates correction x2 test, students t-test.

CP, cryopreservation; ICH, intracerebral hemorrhage; SP, subcutaneous pocket;
TBI, traumatic brain injury.

Fig. 1. Measurement of bony resorption. (A) Obtain standard postoperative brain CT

cut using foramen of Monroe and bilateral anterior horns. (B) Switch to bone
window. (C) Divide the image with a line drawing and determine the difference in
thickness between the cranioplasty edge and the contralateral bone.

C.-H. Cheng et al. / Clinical Neurology and Neurosurgery 124 (2014) 8589
Table 2
Comparison of surgical site infection incidence by etiology and storage method.
TBI
SP group
Thigh infection
Epidural abscess
Total SSI
CP group
Infection

Non-TBI

87

Table 3
Comparison of bony resorption in two groups.

P value
Decreased thickness (mm)

SP group (n = 34)

CP group (n = 57)

P value

1.14  1.20

1.89  2.20

0.039*

6/81
8/76
14/81

(7.4%)
(10.5%)
(17.3%)

2/29
4/27
6/29

(6.9%)
(14.8%)
(20.7%)

1.000
0.508
0.899

By students t-test.
SP, subcutaneous pocket; CP, cryopreservation.

14/118

(11.9%)

6/62

(9.7%)

0.846

Literature review

YSP, subcutaneous pocket; CP, cryopreservation; TBI, traumatic brain injury.

Yates correction x2 test.

Incidence of SSI
The total SSI incidence of all 290 patients was 13.8%. Twenty
cases of infection occurred in the SP (18.2%). In the CP group,
infection occurred in 20 patients (11.1%). The difference between
these groups was not statistically signicant (p = 0.129). Detailed
data for each infection case are summarized in Tables 4 and 5.
In the SP group, there were two infection sources i.e., the thigh
wound and the cranioplasty site. Therefore, we separated the
patients into two subgroups for discussion purposes (Table 4).
Among these patients, 5 cultures were negative. Of the 8 patients
who developed an SSI in the thigh wound, 2 were infected with
Staphylococcus aureus (S. aureus) and one with Escherichia coli (E.
coli). In contrast, there were 12 SSIs in the cranioplasty wounds.
The most common pathogen (7 cases) was methicillin-resistant
Staphylococcus aureus (MRSA), and SA was isolated from the other
5 patients. Moreover, there were 5 cases in which the removal of
the skull bone from the thigh was required due to wound rupture,
and 3 cases developed purulent discharges from the thigh wounds.
In all but 1 patient, the skull ap was removed from the infected
thigh. In that 1 case, we debrided the wound, and the retrieved
skull ap was preserved in the other thigh. Cranioplasty was
performed two months later without infection in this case. In the
cranioplasty wound infection group, 10 epidural abscesses (EDA),
and 2 ruptured wounds occurred. The mean interval from the DC
to the thigh SSI was 23.75 days. Among the 12 infected
cranioplasties, the mean interval from the DC to the cranioplasty
was 35.58 days, and the mean duration from cranioplasty to SSI
was 59.83 days.
In the CP group, 20 cases of infection were recorded (Table 5).
The most common pathogen (8 cases) was MRSA. There were 15
patients who developed EDA. The other 5 cases were infected due
to ruptured wounds. The mean duration from DC to cranioplasty in
this group was 59.05 days, and the mean interval from cranioplasty
to SSI was 38.40 days.
Subgroup analyses
Detailed comparisons of the various subgroups (by TBI etiology,
SSI, SP and CP) are presented in Table 2.
The incidence of bone resorption
We also calculated the incidence of bone ap resorption. For
this calculation, we excluded the infected cases, and limited the
follow-up interval to between six and twelve months. Thus, 91
cases were included in this study of bone resorption. There were
34 patients in the SP group. The mean follow-up interval to brain
CT was 228 days (range from 6 to 12 months). The CP group
included 57 patients. The mean follow-up interval was 250 days.
The bony resorption data are shown in Table 3.

Inamasu et al. [7] reviewed several articles documenting the

incidences of SSIs following autologous cranioplasties. All of these
articles were reports of retrospective studies, and only one
involved a comparison of the incidence of SSI between SP and
CP groups [7]. A list of the previously published data is shown in
Tables 6 and 7.
4. Discussion
SP and CP are the two methods that are most commonly used
to store autologous bone aps [8]. However, the SP method is
forbidden by law in some countries. It remains unclear whether
one method is superior to the other because, to our knowledge,
prospective randomized trials evaluating the efcacies and
safeties of the two methods have not been conducted. The most
common complication of cranioplasty is infection of the bone ap
and surrounding tissues, and the incidence of this complication
has been reported to be as high as 33% [1,913]. Thus, storage
methods with lower SSI incidences might be favored by surgeons
Tables 4 and 5.
The current retrospective study revealed that the overall SSI
incidence in the CP group was lower than that of the SP group
(11.11% vs. 18.18%, respectively). However, this difference was not
signicant (P = 0.129). Interestingly, analyses of the SP group data
according to the location of the SSI revealed that the incidence of
thigh SSI was 7.27% and that of cranioplasty was 11.65%. Compared
of the cranioplasty SSIs between only the CP and SP groups
revealed similar rates (11.11% vs. 11.65%, respectively). In our
opinion, the additional surgical wound in the thigh or abdomen
and the additional surgical time required for the SP group might
have been one of the reasons for the higher overall infection rate. A

Table 4
Summary of 20 SP SSIs.

Sex (M:F)
Age (yr)
Etiology
Traumatic brain injury
Malignant infarction
Subarachnoid hemorrhage
Infection type
Local abscess
Ruptured wound
EDA
Pathogen
Negative culture
Staphylococcus aureus
MRSA
Escherichia coli
Mean (SD) interval (days)
DC to SSI
DC to CPL
CPL to SSI

Thigh infection
(n = 8)

Cranioplasty infection
(n = 12)

8:0
48.00  21.93

11:1
46.67  15.35

6 (75%)
2 (25%)
0 (0%)

9 (75.0%)
2 (16.7%)
1 (8.3%)

3 (37.5%)
5 (62.5%)
0 (0%)

0 (0%)
2 (16.7%)
10 (83.3%)

5
2
0
1

0
5
7
0

(62.5%)
(25.0%)
(0%)
(12.5%)

(0%)
(41.7%)
(58.3%)
(0%)

23.75  14.93
35.58  19.74
59.83  76.81

CPL, cranioplasty; DC, decompressed craniectomy; EDA, epidural abscess; SSI,

surgical site infection; SP, subcutaneous pocket; SD, standard deviation; MRSA,
methicillin-resistant S. aureus.

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C.-H. Cheng et al. / Clinical Neurology and Neurosurgery 124 (2014) 8589

Table 5
Summary of 20 CP SSIs.
N (%) or mean  SD
Sex (M:F)
Age (yr)
Etiology
Traumatic brain injury
Malignant infarction
Spontaneous intracerebral hemorrhage
Subarachnoid hemorrhage
Infection type
EDA
Ruptured wound
Pathogen
Staphylococcus aureus
MRSA
Serratia marcescens
Escherichia coli
Klebsiella pneumoniae
Pseudomonas aeruginosa
Propionibacterium acnes
Not available
Interval (days)
DC to CPL
CPL to SSI

12:8
47.55  20.25
14 (70%)
4 (20%)
1 (5%)
1 (5%)
15 (75%)
5 (25%)
2
8
2
1
1
1
1
4

(10%)
(40%)
(10%)
(5%)
(5%)
(5%)
(5%)
(20%)

59.05  54.35
38.40  34.08

CPL, cranioplasty; DC, decompressed craniectomy; EDA, epidural abscess; SSI,

surgical site infection; CP, cryopreservation; SD, standard deviation; MRSA,
methicillin-resistant S. aureus.

multivariate analysis of the SSI rates might be superior for

identifying the roles played by other factors, such as age, comorbidities, hospital stay duration, and CSF leakage.
Among TBI cases, the reported incidences of SSI range from 0%
to as high as 38.5% (Tables 6 and 7). However, the groups studied
in these reports were small (ranging from 7 to 37 patients). In our
series, there were a total of 199 TBI cases. In previous reports, the
incidence of SSI in non-TBI groups has ranged from 0% to 14.3%
and tended to be lower than those of TBI groups. A comparison of
the SSI rates of the TBI and non-TBI groups is shown in Table 2.
Our data demonstrate that, in the SP group, the SSI rate in cases of
TBI was 17.3% and that of the non-TBI cases was 20.7%. In the CP
group, the SSI rate in the cases of TBI was 11.9% and that in the
non-TBI cases was 9.7%. Comparing of the etiologic subgroups in
our study revealed a higher incidence of TBI cases in our database
(68.6%) compared to previous reports. There was no signicant
difference in SSI incidence by TBI etiology in the SP or CP
subgroups. In 2006, Matsuno [22] analyzed the factors that
inuence bone graft infection after delayed cranioplasty. This
author concluded there were no statistically signicant differences in the bone graft infection rates between the following four
categories of pre-existing disease: cerebrovascular disease, head
trauma, infectious disease, and brain tumor. The same result was
observed in our study i.e., the rate of SSI was not inuenced by
etiology (i.e., TBI vs. non-TBI).
Osawa et al. reported follow-up results of 27 cases of
cranioplasty with autologous bone grafts that were stored in a

deep-freezer and autoclaved prior to use [14]. In 1 case , the bone

ap had to be removed due to an EDA, and the infection rate was
calculated to be 3.7%. Experiments revealed deep-freezing and
autoclaving had only minimal effects on bone structure, although
the osteocytes were swollen and destroyed. The experiments of
these authors revealed that bacteria survived the long-term
freezing and maintained considerable growth capacity. Therefore,
these authors stated that sterilization prior to use is essential for
autologous bone ap. Compared to the rate reported in that study
(3.7%), the SSI rate of autologous bone grafts in our series (11.1%)
was higher. Indeed, recent studies have reported rates of infection
lower than that reported here (Table 7). Although we were unable
to determine the precise reason for this higher infection rate
observed in our study, the use of different surgical techniques and
differences in the surgeons degrees of experience might have been
important inuences.
We noticed that the SSI incidence (20.69%) was mildly elevated
among the patients in the SP group with non-TBI etiologies. We
have discussed this phenomenon and reviewed the database. We
found that 4 SSIs were counted due to 2 cases of bilateral
cranioplasty in the non-TBI SP subgroup. This bias might have been
one of the biases that led to the higher infection rate. Moreover, the
small number of cases (n = 29) may have caused statistical errors.
Our use of the SP storage method resulted from our possession
of a non-functioning freezer for three years. Therefore, during this
time, the decisions regarding storage method were not inuenced
by subjective factors. However, differences in decisions regarding
the indications for DC and the interval between DC and
cranioplasty, both of which may vary substantially by surgeon,
might have affected the SSI incidence. Differences of in underlying
diseases (such as diabetes, hypertension, and anemia), age, sex,
and general condition were not analyzed, and thus their inuences
on SSI incidence remain uncertain.
These limitations and unanswered questions may ultimately be
addressed through large randomized controlled trials. This study
was a preliminary study and raised some questions that highlight
the need for a prospective randomized study. Not only does the
rate of ap infection require further study, but the rates of bone
fusion and bone resorption, which are concerns during delayed
follow-ups of these patients, also require further study.
The reported incidences of bone ap resorption vary from 3%
to 12% [15,16]. However, to our knowledge, there are no existing
reports that have compared the SP and CP procedures in terms of
the incidence of bone ap resorption. Our data showed that the
degree of bone ap resorption was higher in the CP group
(Table 3). Storing the bone ap in the freezer might cause bone
cell death. We hypothesize that dead bone aps might cause
foreign body reactions following cranioplasty. Active osteoclasts
might destroy the dead bone, which would cause bone resorption
and a decrease in ap thickness. In contrast, the SP storage
method might keep the bone cells alive. Future studies are
warranted to elucidate the precise mechanisms of bone resorption that occur in these settings.

Table 6
Previously-reported cranioplasty infection rates after SP preservation.
Author

TBI:non-TBI

SSI incidence (TBI)

SSI incidence (non-TBI)

SSI incidence (total)

p value
(TBI vs. non-TBI)

Current study
Movassaghi et al. [14]
Huptli et al. [17]
Inamasu et al. [7]
Tybor et al. [18]
Flannery and McConnell [19]

110
53
43
39
36
20

81:29
12:41
N/A
19:20
N/A
17:3

14/81 (17.28%)
N/A
N/A
0/19 (0%)
N/A
N/A

6/29 (20.69%)
N/A
N/A
2/20 (10.0%)
N/A
N/A

20/110 (18.18%)
3/53 (5.7%)
1/43 (2.3%)
2/39 (5.1%)
1/36 (2.8%)
1/20 (5.0%)

0.899
N/A
N/A
0.49
N/A
N/A

N/A, not available; TBI, traumatic brain injury.

C.-H. Cheng et al. / Clinical Neurology and Neurosurgery 124 (2014) 8589

89

Table 7
Previously-reported cranioplasty infection rates after CP.
Author

TBI:non-TBI

SSI incidence (TBI)

SSI incidence (non-TBI)

SSI incidence (total)

p value
(TBI vs. Non-TBI)

Nagayama et al. [20]

Current study
Asano et al. [21]
Matsuno et al. [22]
Prolo et al. [23]
Cheng et al. [11]
Iwama et al. [24]
Shimizu et al. [25]
Inamasu et al. [7]
Osawa et al. [26]
Ima et al. [27]
Kim et al. [28]

195
180
110
54
53
52
49
39
31
27
131
85

28:167
118:62
24:86
26:28
37:16
33:19
15:34
15:24
14:17
7:20
61:70
42:43

4/28 (14.3%)
20/118 (11.86%)
2/24 (8.3%)
10/26 (38.5%)
N/A
5/33 (15.2%)
1/15 (6.7%)
1/15 (6.7%)
4/14 (28.6%)
0/7 (0%)
8/61 (13.1%)
4/42 (9.5%)

4/167 (2.4%)
6/62 (9.67%)
3/86 (3.5%)
4/28 (14.3%)
N/A
2/19 (10.5%)
0/34 (0%)
0/24 (0%)
1/17 (5.9%)
1/20 (5.0%)
6/70 (8.6%)
2/43 (4.7%)

8/195 (4.1%)
20/180 (11.1%)
5/110 (4.5%)
14/54 (25.9%)
2/53 (3.8%)
7/52 (13.5%)
1/49 (2.0%)
1/39 (2.6%)
5/31 (16.1%)
1/27 (3.7%)
14/131 (10.7%)
6/85 (7%)

0.02
0.846
0.65
0.06
N/A
0.64
0.30
0.38
0.15
0.58
N/A
N/A

N/A, not available; TBI, traumatic brain injury.

5. Conclusions
SP and CP might both be effective and safe methods for the
storage of bone aps for cranioplasty, regardless of whether the
etiology is TBI or non-TBI. The results of the current retrospective
review of the experiences of single institution with two autologous
cranioplasty ap storage methods indicate that a large randomized
prospective study is warranted to identify the superior method.
Additionally, the rates of ap infection, bone fusion and bone
resorption following delayed cranioplasty all require further study.
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