ORIGINAL ARTICLE
Does Difference in the Storage Method of Bone Flaps After
Decompressive Craniectomy Affect the Incidence of Surgical Site
Infection After Cranioplasty? Comparison Between Subcutaneous
Pocket and Cryopreservation
Joji Inamasu, MD, PhD, Takumi Kuramae, MD, and Masashi Nakatsukasa, MD
Background: After decompressive craniectomy for brain swelling, bone
flaps need to be stored in a sterile fashion until cranioplasty. Temporary
placement in a subcutaneous pocket (SP) and cryopreservation (CP) are the
two commonly used methods for preserving bone flaps. Surgical site infec-
tion (SSI) is a serious complication of cranioplasty, and the storage method
associated with a lower SSI incidence is favored. It is unclear, however,
whether one storage method is superior to the other in terms of SSI
prevention.
Methods: During a 9-year period, 70 patients underwent decompressive
craniectomy and subsequent cranioplasty. Bone flaps from 39 patients were
stored using SP and those from the other 31 were stored using CP. Demo-
graphic data and SSI incidence was compared.
Results: There were no significant demographic differences between the
groups. SSI occurred in seven patients: 2 (5.1%) in the SP group and 5
(16.1%) in the CP group. The difference was not statistically significant (p ⫽
0.23). When each group was further divided into two categories based on
etiology (traumatic brain injury [TBI] versus non-TBI), CP showed a
significantly higher SSI incidence compared with SP (28.6% versus 0%, p ⫽
0.02) in the TBI category. However, the difference in incidence was not
significant in the non-TBI category.
Conclusions: SP and CP may be equally efficacious for storage of bone flaps
of non-TBI etiology; however, SP may be the storage method of choice for
TBI. It remains to be verified in a prospective fashion whether SP is truly the
better method of storing bone flaps in TBI.
Key Words: Bone flap, Cranioplasty, Cryopreservation, Decompressive
craniectomy, Subcutaneous pocket, Surgical site infection, Traumatic brain
injury.
(J Trauma. 2010;68: 183–187)
C ranial defects after decompressive craniectomy (DC)
need to be reconstructed once intractable brain swelling,
for which DC is performed, subsides. Cranial flaps used in
cranioplasty may be either synthetic or autologous.1 Com-
pared with synthetic material, autologous bone is physiologic
Submitted for publication February 25, 2009.
Accepted for publication August 27, 2009.
Copyright © 2010 by Lippincott Williams & Wilkins
From the Department of Neurosurgery, Saiseikai Utsunomiya Hospital,
Utsunomiya, Japan.
Address for reprints: Joji Inamasu, MD, PhD, Department of Neurosurgery,
Saiseikai Utsunomiya Hospital, 911-1 Takebayashi, Utsunomiya 321-0974,
Japanemail; email: ginamasu@aol.com.
DOI: 10.1097/TA.0b013e3181c45384
The Journal of TRAUMA® Injury, Infection, and Critical Care • Volume 68, Number 1, January 2010
and a less expensive option in cranioplasty. The bone flaps
need to be preserved for several weeks to months in a sterile
fashion until cranioplasty, and several storage methods are
available for this purpose. The two most popular methods are
(1) placement in a subcutaneous pocket (SP), most often in
the lower abdominal wall2 but occasionally in the anterolat-
eral thigh3 or even in the scalp4; and (2) cryopreservation
(CP), usually in a deep freezer. The choice of method is
usually based on the surgeon’s preference, and whether one
method is superior to the other has rarely been studied.
Surgical site infection (SSI) is a rare but serious complication
of cranioplasty.1,5,6 To clarify whether differences in the
method used to store bone flaps had an effect on SSI inci-
dence after cranioplasty, we conducted a retrospective study.
PATIENTS AND METHODS
Between January 1999 and December 2007, a total of
70 patients underwent DC for malignant brain swelling and
subsequent cranioplasty with autologous bone flaps in our
institution, which is a tertiary referral center for trauma. Bone
flaps for 39 patients were stored using SP. A transverse skin
incision was made in the lower abdomen, and a pocket was
created in the subcutaneous fat layer to accommodate the
bone flaps. The abdominal wound was reopened and bone
flaps were retrieved at the time of cranioplasty. Bone flaps for
the remaining 31 patients (CP group) were stored in a deep
freezer, at a temperature of ⫺70C°. In the CP group, bone
flaps were immersed in betadine solution immediately after
harvest, wrapped with sterile gauze, and placed into a deep
freezer. Neither autoclave7 nor ethylene oxide8 sterilization of
bone flaps was used. Bone flaps were thawed at room tem-
perature immediately before cranioplasty.
The choice of the two storage methods was neither
controlled nor randomized. Rather, it depended primarily on
the decision of the attending neurosurgeon who performed
the DC. SP and CP were exclusively used by two and one
surgeons, respectively. No synthetic materials were used to
fill the gap between the bone flaps and skull. In all patients,
the dura mater was reconstructed with Dura Substitute (W. L.
Gore & Associates, Flagstaff, AZ), and bone flaps were fixed
to the skull with titanium plates. None of the patients had a
violation of paranasal sinuses during DC. Autologous cranio-
plasty has never been used for patients with a penetrating
183
Inamasu et al. The Journal of TRAUMA® Injury, Infection, and Critical Care • Volume 68, Number 1, January 2010

traumatic brain injury (TBI) in our institution. Piperacillin, 4
g/d, was administered routinely for 5 to 7 days as a postop-
erative systemic antibiotic. Medical records were meticu-
lously reviewed, and SSI incidence was compared between
the two groups. We were also interested in determining
whether difference in the etiology of brain lesions for which
DC was performed affected SSI after cranioplasty. Therefore,
each group was further divided depending on whether the
etiology was a TBI or not, and subgroup comparison of the
SSI incidence was made. Clinical characteristics of patients
who sustained an SSI were also summarized. Finally, perti-
nent literature documenting SSI incidence after cranioplasty
was reviewed. Subgroup comparison of the data obtained
from literature was conducted whenever possible. Statistical
analyses were performed using SPSS 13.0 for Windows.
Continuous variables, expressed as mean ⫾ standard devia-
tion, were compared using the Student t test, categorical
variables using Fisher exact test, and p ⬍ 0.05 was consid-
ered statistically significant.
RESULTS
Demographics
Among patients in the SP group (n ⫽ 39), DC was
performed for closed TBI in 19, aneurysmal subarachnoid
hemorrhage in 13, spontaneous intracerebral hematoma
(ICH) in 5, and cerebral infarction in 2 patients. Among
patients in the CP group (n ⫽ 31), DC was performed for
closed TBI in 14, for aneurysmal subarachnoid hemorrhage
in 7, for spontaneous ICH in 9, and for cerebral infarction in
1 patient. The difference in the frequency of TBI in the SP
group (48.7%) compared with the CP group (45.2%) was not
statistically significant (p ⫽ 0.77). The male-to-female ratio
was 20:19 in the SP group and 17:14 in the CP group. The
difference was not statistically significant (p ⫽ 0.77). The
mean age at the time of cranioplasty was 48.4 ⫾ 16.3 years
in the SP group and 43.1 ⫾ 17.4 years in the CP group. The
difference was not statistically significant (p ⫽ 0.21). In the
SP group, the interval between DC and cranioplasty ranged
from 18 to 150 days (mean, 37.5 ⫾ 20.7 days), and in the CP
group, the interval ranged from 24 to 100 days (mean, 40.4 ⫾
24.6 days). The difference was not statistically significant
(p ⫽ 0.60). The mean follow-up period after cranioplasty was
52.4 ⫾ 34.7 months in the SP group and 46.5 ⫾ 35.3 months
in the CP group. The difference was not statistically signifi-
cant (p ⫽ 0.67). These data are summarized in Table 1.
Incidence of SSI
SSI occurred in seven patients: 2 (5.1%) in the SP
group and 5 (16.1%) in the CP group (Table 1). The differ-
ence was not statistically significant (p ⫽ 0.23). Their demo-
graphic data are summarized in Table 2. Four of the five
patients who developed an SSI in the CP group were TBI
victims, whereas both patients who developed an SSI in the
SP group had sustained an ICH. Among these seven patients,
six showed purulent discharge from the scalp wound, and the
other patient had an SSI in the abdominal wound. Staphylo-
coccus aureus was isolated from all seven patients. Five of
the six patients with a scalp wound infection developed a
concomitant epidural abscess. All five patients who devel-
oped an epidural abscess required debridement surgery, bone
flap removal, and delayed cranioplasty with allograft. The
other patient with a scalp wound infection developed dehis-
cence of the infected wound that was limited to the superficial
scalp. This infection was treated conservatively, without flap
removal. Intravenous vancomycin was administered to all
patients. In the patient with an abdominal SSI, the bone flap
was discarded; this patient later underwent cranioplasty using
an allograft. Most patients who developed an SSI did so
within 3 weeks of cranioplasty; delayed SSI occurred in only
two patients.

TABLE 1. Demographics and Incidence of Surgical Site Infection of 70 Patients Who Underwent Cranioplasty
Group n M:F Age (yr) Etiology SSI Interval (d) Follow-Up (m)
SP 39 20 :19 48.4 ⫾ 16.3 TBI (19), SAH (13), ICH (5), CI (2) 2 (5.1%) 37.5 ⫾ 20.7 52.4 ⫾ 34.7
CP 31 17 :14 43.1 ⫾ 17.4 TBI (14), SAH (7), ICH (9), CI (1) 5 (16.1%) 40.4 ⫾ 24.6 46.5 ⫾ 35.3
p 0.77 0.21 0.77 0.23 0.60 0.67
CI, cerebral infarction; ICH, intracerebral hemorrhage; SAH, subarachnoid hemorrhage; TBI, traumatic brain injury.

TABLE 2. Summary of Seven Patients Who Developed a Surgical Site Infection After Cranioplasty
Interval (d) Interval (d)
Group Age, yr Gender Etiology Infection Site Pathogen (DC to CPL) (CPL to SSI) Treatment Required
CP 27 Male TBI Scalp, EDA Staphylococcus aureus 60 10 Debridement, flap removal
CP 41 Male TBI Scalp, EDA S. aureus 27 8 Debridement, flap removal
CP 16 Male TBI Sup. scalp S. aureus 120 13 IV Vancomycin only
CP 2 Female TBI Scalp, EDA S. aureus 14 20 Debridement, flap removal
CP 37 Male ICH Scalp, EDA S. aureus 15 8 Debridement, flap removal
SP 27 Male ICH Abdomen S. aureus 27 37 Debridement, flap removal
SP 53 Female ICH Scalp, EDA S. aureus 24 7 Debridement, flap removal
CPL, cranioplasty; DC, decompressive craniectomy; EDA, epidural abscess; SSI, surgical site infection.

184 © 2010 Lippincott Williams & Wilkins

The Journal of TRAUMA® Injury, Infection, and Critical Care • Volume 68, Number 1, January 2010 Surgical Site Infection After Cranioplasty

Subgroup Analysis
Each group was further divided into two categories ac-
cording to etiology (TBI versus non-TBI), and SSI incidence
was compared for each category. Among patients with a TBI
etiology, SP showed a significantly lower SSI incidence com-
pared with CP (0% versus 28.6%, p ⫽ 0.02). Among those with
a non-TBI etiology, there was no significant difference in SSI
incidence between CP and SP (10.0% versus 5.9%, p ⫽ 0.88).
The results are summarized in Table 3. Next, we examined
whether SSI incidence among patients with TBI or non-TBI
etiologies differed within the same preservation method. In the
SP group, SSI incidence was 0% in TBI versus 10.0% in
non-TBI (p ⫽ 0.49). In the CP group, SSI incidence was 28.6%
in TBI versus 5.9% in non-TBI (p ⫽ 0.15). Statistical difference
was present in neither. These results are summarized in Table 4
(TBI) and Table 5 (non-TBI).
Literature Review
Fifteen peer-reviewed articles documenting SSI inci-
dence after autologous cranioplasty were retrieved from lit-
TABLE 3. Subgroup Comparison of Surgical Site Infection
Incidence Based on the Etiology
Category SP vs. CP (n) SSI:SP vs. CP
TBI 19 vs. 14 0 (0%) vs. 4 (28.6%)
Non-TBI 20 vs. 17 2 (10.0%) vs. 1 (5.9%)
erature. All were retrospective studies and none involved
comparison of SSI incidence between SP and CP. The 15
studies were categorized into two arms: SP and CP. The SP
arm comprised five studies, with overall SSI incidence rang-
ing from 0% to 5.7% (Table 4).9 –13 The CP arm comprised 10
studies, with overall SSI incidence ranging from 0% to 25.9%
(Table 5).1,5–7,14 –19 In 7 of the 10 CP studies, statistical
comparison of SSI incidence based on the etiology was
feasible.1,5–7,14,17,19 SSI incidence was higher for patients with
a TBI etiology in most of them (Table 5). However, the
difference was statistically significant in only one study.6
DISCUSSION
DC is an effective treatment for alleviating malignant
brain swelling refractory to medical management. After the
acute brain swelling subsides, cranioplasty is almost invari-
ably necessary for protection of the underlying brain and also
for cosmesis. Cranial flaps used in cranioplasty may be either
synthetic or autologous.1 Compared with synthetic materials,
autologous bone flap is physiologic and less expensive. It has
two other potential advantages: the fusion between the skull
and bone flap may occur, and theoretically, adverse reactions
to foreign materials will not develop. Although several meth-
ods to store bone flaps harvested during DC have been
p reported, purported advantages associated with the choice of
0.02 method are anecdotal and there have been no guidelines or
0.88 recommendations on the subject. SP and CP are the two
methods most commonly used to store bone flaps.2 It is

TABLE 4. Reported Incidence of Surgical Site Infection After Cranioplasty With Subcutaneous Pocket (SP Arm)
TBI: SSI Incidence SSI Incidence SSI Incidence TBI vs.
Author n Non-TBI (Overall) (TBI) (Non-TBI) Non-TBI p
Häuptli et al.10 43 N/A 1/43 (2.3%) N/A N/A N/A
Flannery and McConnell9 20 17:3 1/20 (5.0%) N/A N/A N/A
Tybor et al.13 36 N/A 1/36 (2.8%) N/A N/A N/A
Movassaghi et al.12 53 12:41 3/53 (5.7%) N/A N/A N/A
Ichinose et al.11 12 3:9 0/12 (0%) 0/3 (0%) 0/9 (0%) N/A
Present study 39 19:20 2/39 (5.1%) 0/19 (0%) 2/20 (10.0%) 0.49
N/A, not available.

TABLE 5. Reported Incidence of Surgical Site Infection After Cranioplasty With Cryopreservation (CP Arm)
TBI SSI Incidence SSI Incidence SSI Incidence TBI vs.
Author n Non-TBI (Overall) (TBI) (Non-TBI) Non-TBI p
Prolo et al.18 53 37:16 2/53 (3.8%) N/A N/A N/A
Crotti and Mangiagalli15 15 N/A 2/15 (13.3%) N/A N/A N/A
Osawa et al.7 27 7:20 1/27 (3.7%) 0/7 (0%) 1/20 (5.0%) 0.58
Asano et al.14 110 24:86 5/110 (4.5%) 2/24 (8.3%) 3/86 (3.5%) 0.65
Shimizu et al.19 39 15:24 1/39 (2.6%) 1/15 (6.7%) 0/24 (0%) 0.38
Nagayama et al.6 195 28:167 8/195 (4.1%) 4/28 (14.3%) 4/167 (2.4%) 0.02
Iwama et al.17 49 15:34 1/49 (2.0%) 1/15 (6.7%) 0/34 (0%) 0.30
Matsuno et al.1 54 26:28 14/54 (25.9%) 10/26 (38.5%) 4/28 (14.3%) 0.06
Grossman et al.16 12 N/A 0/12 (0%) N/A N/A N/A
Cheng et al.5 52 33:19 7/52 (13.5%) 5/33 (15.2%) 2/19 (10.5%) 0.64
Present study 31 14:17 5/31 (16.1%) 4/14 (28.6%) 1/17 (5.9%) 0.15
N/A, not available.

© 2010 Lippincott Williams & Wilkins 185

Inamasu et al. The Journal of TRAUMA® Injury, Infection, and Critical Care • Volume 68, Number 1, January 2010
unclear, however, whether one method is superior to the
other, as prospective randomized trials to evaluate the effi-
cacy and safety of the two methods have never been con-
ducted. SSI is one of the most serious complications of
cranioplasty,1,5,6 and a storage method with a lower SSI
incidence may be favored by surgeons.
This retrospective study showed that there was no
significant difference in the overall SSI incidence between SP
and CP (5.1% versus 16.1%). The results, which are similar
to those reported in the previous meta-analysis,2 are not
unexpected and may be proof that both storage methods are
efficacious and have stood the test of time. The reported SSI
incidence in the SP arm of the literature review ranged from
0% to 5.7%,9 –13 which is similar to the figure of 5.1%
obtained in our retrospective study. On the other hand, the
reported SSI incidence in the CP arm of the literature review
varied more widely, ranging from 0% to 25.9%,1,5–7,14 –19 and
our figure of 16.1% seems like an average. Interestingly,
when a subgroup comparison was made within the TBI
etiology, the CP subgroup showed a significantly higher SSI
incidence compared with the SP subgroup. In contrast, there
was no significant difference in SSI incidence between SP
and CP subgroups, when the etiology was non-TBI. These
results suggest that SP and CP may be equally effective as
storage methods for bone flaps of non-TBI etiology, whereas
SP may be the storage method of choice for TBI etiology.
This is the first study in literature to document SSI incidence
stratified by etiology and storage methods.
Why SSI incidence was particularly elevated among
patients in the CP group with a TBI etiology remains to be
explained. The reported incidence of postcranioplasty SSI
among that population ranged from 0% to as high as
38.5%.1,5,6,14,16,17,19 In contrast, SSI incidence among patients
in the CP group with a non-TBI etiology ranged from 0% to
14.3%,1,5,6,14,16,17,19 which tend to be lower compared with
that of the TBI etiology. The difference may be partly
attributable to the fact that DC for TBI is inherently very
vulnerable to postoperative infection. In a recent study on
severe, closed TBI, 4 in 18 (22.2%) TBI patients who had
undergone a DC developed a cerebrospinal fluid infection
before a scheduled cranioplasty.20 Even so, the figure we
obtained (i.e. the SSI incidence of 28.6% in CP with a TBI
etiology) may be unacceptably high. In retrospect, the way
bone flaps were handled before storage in a deep freezer
might not have been optimal: autoclave7 or ethylene oxide8
sterilization, which is advocated by several authors to de-
crease the incidence of infection, had never been used in our
institution. Immersion into antibiotic solution might also have
been effective to some degree. The interval between DC and
cranioplasty, which may be an independent risk factor for
development of SSI, might have been too short in this study,
as an interval of ⬎2 to 3 months has been recommended in
literature.5 These factors, in combination, might have led to
the high SSI incidence among patients in the CP group with
a TBI etiology. In contrast, fewer published data are available
regarding the SSI incidence in SP with a TBI etiology (Table
4); therefore, it does not make much sense to compare the
current figure of 0% in this subgroup with that reported in
186
literature. Although the SP method may be capable of nour-
ishing osteocytes in the bone flaps21 and purifying a bone flap
that had previously been infected,22 it is not clear whether the
lower SSI incidence for SP with a TBI etiology may be
explained by immunologic defense mechanisms provided by
the host. Although bacterial proliferation in bone flaps may
be prevented to some extent in either group by different
protective mechanisms, no comparative studies have been
conducted to evaluate the sterility of either preservation
method (e.g., bacterial count or culture).
This study has several limitations. The decision about
the storage method to be used during DC was made by the
attending surgeon-on-call. Thus, the differences in the indi-
cations for DC as well as in the interval between DC and
cranioplasty, both of which may vary substantially by sur-
geon, might have affected SSI incidence, although demo-
graphics were similar between the two groups. The relatively
small number of patients in each subgroup might also have
resulted in a type I error. Moreover, the incidence of solid
fusion between the skull and bone flaps or that of abnormal
resorption of flaps, neither of which were evaluated in this
study because of insufficient follow-up imaging studies,
should also be evaluated in a comparative fashion, and which
of the two storage methods is superior in this aspect also
needs to be ascertained. These limitations and unanswered
questions may ultimately be addressed with randomized con-
trolled trials. In autologous cranioplasty, an randomized con-
trolled trial may be conducted without much difficulty,
because of the relatively low medical cost required in either
method. In ethical terms, however, we have some concerns
about using CP for TBI, and currently, CP is used exclusively
for non-TBI etiology in our institution.
CONCLUSION
SP and CP may be equally effective and safe methods
of storing bone flaps for cranioplasty when the etiology is
non-TBI; however, SP may be the storage method of choice
for a TBI etiology because of its lower SSI incidence. It
remains to be resolved whether SP is truly the better method
of storing bone flaps for TBI. In addition, the defense mech-
anism against bacterial overgrowth when free bone flaps are
stored with SP needs to be studied.
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influencing bone graft infection after delayed cranioplasty. Acta Neuro-
chir (Wien). 2006;148:535–540.
2. Zingale A, Albanese V. Cryopreservation of autogeneous bone flap in
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preservation of free skull bone flap taken out in decompressive craniec-
tomy—a follow-up study. No Shinkei Geka. 1977;5:1329 –1333.
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affecting graft infection after cranioplasty. J Clin Neurosci. 2008;15:
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Br J Neurosurg. 2001;15:518 –520.
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EDITORIAL COMMENT
The retrospective study of Inamasu and colleagues is one of
those experiential nuggets so passé in our evidenced-based
world. Yes, passé and even ridiculed, but of immense prac-
tical value to the practicing surgeon: what are the arguably
simplest and safest strategies under the circumstances? As
decompressive craniectomy has become increasingly ac-
cepted for malignant brain swelling, what should be done
with the bone flap is a practical question. Statistics aside, the
authors have shown that the old strategy of the subcutaneous
pocket remains legitimate, based on not a small experience,
especially in the trauma case. The here-to-fore reported
cranioplasty infection rate is alarmingly high, especially in
© 2010 Lippincott Williams & Wilkins
Surgical Site Infection After Cranioplasty
traumatic brain injury and by comparison the author’s negligible
rate is compelling, not withstanding the report’s admitted short-
comings. The security of modern “extrabody” preservation,
however refined, is another consideration favoring the subcu-
taneous pocket; the misplaced or occultly contaminated flap
just doesn’t happen when it is kept in its “owner.”
Richard L. Saunders, MD
Professor Emeritus
Dartmouth Medical School
Hanover, New Hampshire
EDITORIAL COMMENT
This report is a retrospective review of a single-institution
experience with autologous cranioplasty flap storage. The
authors stored bone flaps by direct implantation into the
abdominal subcutaneous tissues (subcutaneous pocket [SP])
or soaked the bone flap and wrapped it in gauze and froze the
flap at ⫺70°C (cryoprotection [CP]). In either case, the flap
was removed at cranioplasty from its storage site and was
implanted without any further sterilization procedures. The
study was rather limited by the small sample size of 70
patients over 8 years. Overall, the demographics were similar.
The only pathology-storage means to have significance was
traumatic brain injury and CP (28.6%) as compared with
traumatic brain injury SP (0%). Overall, the flap infection rate
was 10%, which is somewhat higher than previous reports;
the difference between SP (5.1%) and CP (16.1%) was not
significant.
This is an interesting report that seems to suggest that
there may be differences in flap infections after autologous
cranioplasty, based on the flap-storage method. The obvious
initial criticism is that the CP group did not undergo any
further sterilization, which may explain the differences. The
other is that this being a small study prevents strong valida-
tion of its conclusions because of an inadequate sample.
However, I think this is the kind of preliminary study that
raises enough questions to support a prospective random-
ized study. These include, as the authors point out, not
only the rate of flap infection but also the rates of bone
fusion and bone resorption, which are concerns during
delayed follow-up of these patients.
Overall, this is an interesting study that begins to
suggest that subcutaneous implantation may be safer from a
bone-flap-infection standpoint, particularly in the traumatic
cohort, as compared with CP.
Adnan H. Siddiqui, MD, PhD
Departments of Neurosurgery and Radiology
Toshiba Stroke Research Center
School of Medicine and Biomedical Sciences
University at Buffalo
State University of New York
Buffalo, New York
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