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Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 221e225

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Journal of Cranio-Maxillo-Facial Surgery


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Viability of crushed human auricular and costal cartilage chondrocytes


in cell culture
Fuat Buyuklu a, *, Evren Hizal a, Zerrin Yilmaz b, Feride Iffet Sahin b, Ozcan Cakmak c
a
Baskent University Faculty of Medicine, Department of Otorhinolaryngology, Bahcelievler, 06490 Ankara, Turkey
b
Baskent University Faculty of Medicine, Department of Medical Genetics, Maltepe, 06570 Ankara, Turkey
c
Acibadem University Faculty of Medicine, Department of Otorhinolaryngology, Kadikoy, 34718 Istanbul, Turkey

a r t i c l e i n f o a b s t r a c t

Article history: The amount or quality of available septal cartilage may be inadequate for grafting in some rhinoplasty
Paper received 16 November 2009 patients. In such cases, auricular or costal cartilage may provide an additional source of cartilage. Crushed
Accepted 10 March 2010 septal cartilage has been shown to be useful for dorsal onlay grafts. We aimed to investigate the effect of
different degrees of crushing on the viability of human auricular and costal cartilage. Ten auricular and 10
Keywords: costal cartilage grafts were obtained from 20 patients during secondary rhinoplasty. Each graft was
crushed cartilage
sectioned into five pieces. One of the pieces was left intact and the remaining four were prepared as
graft
slightly, moderately, significantly, and severely crushed. Viability and proliferation rates of chondrocytes
rhinoplasty
auricular
in cell cultures were evaluated. Mean viability rates on day 1 for intact, slightly crushed, moderately
costal cartilage crushed, significantly crushed, and severely crushed auricular cartilages were 70%, 67%, 65%, 58%, and
viability 45%; while those for costal cartilages were 65%, 63%, 59%, 55%, and 53%, respectively. There was no
statistically significant difference between the viability rates of the similarly crushed auricular and costal
cartilage groups on days 1, 2, 3 and 10. The viability of crushed human auricular and costal cartilage grafts
depends on the degree of crushing applied.
Ó 2010 European Association for Cranio-Maxillo-Facial Surgery.

1. Introduction cartilage. However, the amount or quality of available septal carti-


lage may be inadequate, especially in patients with severe defor-
The sophisticated nature of rhinoplasty may lead to unplanned mity (e.g. traumatic or congenital) or in revision rhinoplasty. In
results such as dorsal contour irregularities. These irregularities are such cases, auricular or costal cartilage may provide an additional
most commonly encountered in revision cases or in patients with source of cartilage. Determinative factors to decide the donor site
thin skin, and become more noticeable as the oedema subsides. are based on the quantity and quality of cartilage needed, consent
Camouflage of these irregularities represents one of the most of the patient and experience of the surgeon (Horton and
challenging procedures of rhinoplasty. Various kinds of graft Matthews, 1992; Ag aoglu and Erol, 2000; Cakmak and Ergin,
materials including autografts (cartilage, fascia and dermis), 2002; Cakmak et al., 2005a, 2005b; Cakmak and Buyuklu, 2007).
homografts (irradiated cartilage, preserved acellular dermis) and Crushed autogenous cartilage grafts may be an option for con-
alloplasts (polyester, polyethylene) have been used to achieve cealing the irregularities and to achieve a smoother nasal surface.
better aesthetic results (Guerrerosantos, 1991; Sheen, 1998; However, the literature contains limited and conflicting informa-
Cakmak and Ergin, 2002; Sarukawa et al., 2004; Cakmak et al., tion about the clinical outcome of crushed cartilage grafts (Huizing,
2005a, 2005b; Berghaus and Stelter, 2006; Ozaki et al., 2006; 1974; Breadon et al., 1979; Stoksted and Ladefoged, 1986;
Cakmak and Buyuklu, 2007). Autogenous cartilage is considered to Verwoerd-Verhoef et al., 1991; Hamra, 1993; Bujia, 1994; Guyuron
be ideal for all types of grafting because of its high survival rate, and Friedman, 1994; Rudderman et al., 1994; Yilmaz et al., 2001;
minimal resorption and low immunogenic characteristics. The Cakmak and Ergin, 2002; Cakmak et al., 2005a, 2005b; Cakmak
nasal septum is the first choice of donor site for autogenous and Buyuklu, 2007). The effects of the degree of crushing on
rabbit auricular (Cakmak et al., 2005b) and human nasal septal
(Cakmak et al., 2005a) cartilages, and the clinical outcome of
* Corresponding author. Baskent University Faculty of Medicine, Otorhinolaryn-
gology Department, Bahcelievler, 06490 Ankara, Turkey. Tel.: þ90 312 2238534;
crushed grafts (Cakmak and Buyuklu, 2007) in rhinoplasty were
fax: þ90 312 2157597. assessed before. These studies showed that significant or severe
E-mail address: fuatbuyuklu@yahoo.com (F. Buyuklu). crushing reduced chondrocyte viability and long-term clinical

1010-5182/$ e see front matter Ó 2010 European Association for Cranio-Maxillo-Facial Surgery.
doi:10.1016/j.jcms.2010.03.013

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222 F. Buyuklu et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 221e225

predictability of the crushed cartilage grafts (Cakmak and Ergin, directly on the 7th costal cartilage in the men, it was placed under
2002; Cakmak et al., 2005a, 2005b). However, the effect of the breast crease in the women in order to hide the scar. After the
different degrees of crushing on the viability of human auricular skin incision was completed, the fascia over the external oblique
and costal cartilage chondrocytes has not been investigated. We muscle was opened and the fibres of this muscle were bluntly
present the first study that investigates the effect of different elevated to expose the underlying costal cartilage. The perichon-
degrees of crushing on the viability of human auricular and costal drium over the outer surface of the costal cartilage was incised and
cartilage chondrocytes. a circumferential subperichondrial elevation was performed. When
the elevation was complete the desired section of costal cartilage
2. Materials and methods was excised. The donor site was filled with water to check for
a pleural tear and then closed with 4-0 vicryl (Vicryl suture;
Ten auricular and 10 costal cartilages were obtained from 20 Johnson & Johnson Gateway LLC, Piscataway, New Jersey) and 5-
patients who underwent secondary septorhinoplasty in the 0 prolene (Prolene suture, Johnson & Johnson Gateway LLC, Pis-
Department of Otorhinolaryngology at Baskent University Hospital, cataway, New Jersey) sutures. A light dressing was applied on the
Ankara, Turkey. In each patient, the required amount of cartilage wound. No drains were required.
was used as graft and the remaining part of the cartilage was Both auricular and costal cartilages were immediately sectioned
prepared and used for the study. The study protocol was approved into five 3  3 mm pieces. One of the pieces was left intact (1) and
by the Clinical Research Ethical Committee of Baskent University the remaining four pieces were prepared, using a Cottle cartilage
and written informed consent was obtained from all patients. crusher (model 523900; Karl StorzGmbH&Co, Tuttlingen,
Auricular cartilage was harvested via preauricular approach. Germany), as follows: slightly crushed (2), moderately crushed (3),
An incision was made just inside the antihelical fold and was significantly crushed (4), and severely crushed (5) (Fig. 1). As
therefore hidden by a shadow. The incision passed through the defined in our group’s previous experimental (Cakmak et al., 2005a,
anterior and posterior perichondrial layers and adequate amount 2005b) and clinical (Cakmak and Buyuklu, 2007) studies, the
of cartilage was then harvested. The incision was closed using degree of crushing was based on the appearance of the cartilage, as
a running 6-0 Polyglytone 6211 (CaprosynTM, Tyco Healthcare follows: slightly crushed, to soften the surface without reducing the
ECE, 154 Fareham Road, PO13 0AS). Finally, two or three trans- elastic strength of the cartilage; moderately crushed, to soften the
cutaneous sutures were placed on the conchal bowl to ensure surface and reduce the elastic strength of the cartilage; significantly
reapproximation of the skin flap. A small bacitracin soaked gauze crushed, to apply a force enough to cause the cartilage bend with
pack was lightly placed on the conchal bowl and removed on the gravity; and severely crushed, to destroy the integrity of the
day after surgery. cartilage totally. Each piece of cartilage was placed in a separate
Costal cartilage was harvested from the 7th rib because of its tube containing 5 mL of sterile transfer medium and was imme-
long cartilaginous curvature. While the skin incision was placed diately transported to the genetics laboratory.

Fig. 1. Five pieces of grafts prepared from auricular (above) and costal (below) cartilages (from left to right): intact, slightly crushed, moderately crushed, significantly crushed, and
severely crushed.

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In the genetics laboratory, each cartilage sample was processed a significant difference, the Wilcoxon Signed Rank Test was used to
as described in our previous cell culture study (Cakmak et al., identify where the differences occurred. The viability rates of the
2005a); each cartilage sample was first washed with RPMI 1640 auricular and costal cartilage chondrocytes were compared with
medium (with 25 mM HEPES and L-glutamine; Biological Indus- the ManneWhitney U test. A value of P < .05 was accepted as
tries Ltd, Kibbutz Beit Haemek, Israel) and then mechanically statistically significant. No correction was made for multiple
minced using a sterile lancet. A volume of 1.5 mL of RPMI 1640 testing.
medium containing 2 mg/mL of type II collagenase (Gibco, Invi-
trogen Corp, Karlsruhe, Germany) was added to each tube, and the 3. Results
specimens were left overnight at 37  C. The next day, each colla-
genase-treated cell suspension was placed in a sterile tube con- The study comprised the data of 10 patients (7 women, 3 men;
taining 3 mL of RPMI 1640 medium and centrifuged at 1200 rpm for mean age, 27.2 years; range 20e48 years) who required auricular
10 minutes. After the supernatant was discarded, the pellet was cartilage grafting, and 10 patients (6 men, 4 women; mean age, 30.2
homogenized with 3 mL of RPMI 1640 medium, and the same years; age, 29e45 years) who required costal cartilage grafting,
centrifuge process was repeated. The supernatant was again dis- between October 2006 and November 2008. The mean chon-
carded. Culture medium (DMEM Nutrient Mix F12; Gibco) drocyte viability rates of the auricular and costal cartilages on days
containing 10% foetal calf serum (Biochrom GA, Berlin, Germany), 1, 2, 3 and 10 are given in Tables 1 and 2 and Figs. 2 and 3.
2% L-glutamine (200 mM; Biochrom GA), and 1% pen- The results of the Wilcoxon Signed Rank Test for cartilage group
icillinestreptomycin (10 000 U/mL of penicillin and 10 mg/mL of comparisons are given below.
streptomycin) was added to reach a volume of 8 mL, and the cells
were homogenized. The homogenized cell suspension was divided
into equal volumes in 4 culture flasks, and cell cultures were set up. 3.1. Auricular cartilage group
The flasks were stored at 37  C in 5% carbon dioxide in an incubator
(Heracell; Kendro Laboratory Products, Hanau, Germany) that The results for the auricular cartilage group showed that at all
provided a moist environment. For the cultures that were incu- time points assessed the mean chondrocyte viability rates
bated for 10 days, the cells were fed fresh medium on day 7. decreased as the level of crushing increased.
Cultures were assessed at 1, 2, 3, and 10 days. On each assessment
day, the medium in each flask was transferred to a tube using 3.2. Day 1
a glass Pasteur pipette. The cells were detached from the surface of
the flask by applying a trypsineEDTA solution (0.05% trypsin and The viability rates for the significantly and severely crushed
EDTA at a 1:5000 ratio, Biological Industries Ltd.) and were added auricular cartilage groups were significantly lower than the corre-
to the same tube. The tube was centrifuged at 1000 rpm for 10 min. sponding rates for all the other groups. However, the difference
The supernatant was discarded, 10 pL of trypan blue (Gibco) was between the intact and slightly crushed cartilage groups and the
added to the pellet, and the mixture was homogenized. This difference between the slightly and moderately crushed groups
mixture was incubated at room temperature for 2 min, and living were not statistically significant (Fig. 2).
cells (those that excreted trypan blue) and dead cells were counted
under a light microscope (Nikon E600; Nikon Corp, Tokyo, Japan). 3.3. Day 2
Statistical analysis was performed using the software package
SPSS for Windows version 15.0 (SPSS Inc, Chicago, Ill). A mean The mean chondrocyte viability rate for the intact cartilage
chondrocyte viability rate was calculated for each group of (intact, group was significantly higher than the corresponding rates for all
slightly, moderately, significantly, or severely crushed cartilage) at the other groups. Similar to day 1, the viability rates for the
each time point studied. The statistical analysis was performed significantly and severely crushed auricular cartilage groups were
using nonparametric tests because of the small number of significantly lower than the corresponding rates for all the other
sampling. The Friedman test was used to assess the differences in groups. However, the difference between the slightly and moder-
the viability rates of chondrocytes at each evaluation time point ately crushed groups, and the difference between the significantly
(days 1, 2, 3, and 10) (Tables 1 and 2). If this step revealed and severely crushed cartilage groups were not statistically signif-
icant (Fig. 2).
Table 1
Chondrocyte viability rates for the auricular cartilage. 3.4. Day 3
Day Intact Slightly Moderately Significantly Severely
crushed crushed crushed crushed Similar to day 2, the mean chondrocyte viability rate for the
1 69.8  17.5 66.6  14.9 64.6  14.6 57.5  11.1 44.8  19.6 intact cartilage group was significantly higher than the corre-
2 75.7  12.7 70.5  14.4 66.7  13.7 57.1  14.6 49.9  18.5 sponding rates for all the other groups. However, the difference
3 75.5  14.4 67.5  16.3 64.5  11.4 61  14.2 48.5  18.4 between the slightly and moderately crushed groups, and the
10 70.5  15.5 67.5  16.2 63  15.5 59.5  17.4 60  12.9
difference between the moderately and significantly crushed
cartilage groups were not statistically significant (Fig. 2).

Table 2 3.5. Day 10


Chondrocyte viability rates for the costal cartilage.

Day Intact Slightly Moderately Significantly Severely The mean chondrocyte viability rates for the intact and slightly
crushed crushed crushed crushed crushed cartilage groups were significantly higher than the corre-
1 64.5  17.4 63  18.7 58.8  15.3 55.2  14.7 52.5  12.7 sponding rates for all the other groups. However, the difference
2 68.4  16,8 64  14.7 63  13.8 57.5  15.1 54.5  13.2 between the mean chondrocyte viability rates of moderately,
3 70.8  15.8 69  14.7 66.5  14.5 62  13.6 58  12.3
10 72.6  17.8 71  14.5 69.5  14.8 65.5  14.6 61.5  13.9
significantly and severely crushed groups was not significant
(Fig. 2).

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224 F. Buyuklu et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 221e225

severe deformities, however, requires larger amounts of cartilage


for the graft. The quality and/or quantity of the septal cartilage may
be insufficient especially in patients who have a history of trauma,
congenital anomaly or previous septal surgery. In these patients,
autogenous auricular or costal cartilage has been used as a safe and
cosmetically acceptable graft alternative (Peer, 1941; Gunter et al.,
1997; Sheen, 1998; Cakmak and Ergin, 2002; Murrell, 2004). The
quantity and quality of the cartilage needed, the requirements of
the patient and the surgeon’s skills determine the choice of donor
site. Some factors such as warping of the costal cartilage, subop-
timal geometric structure of the auricular cartilage, and an unpre-
dictable resorption pattern for both may limit the use of auricular
and costal cartilage grafts.
The durability of autogenous costal and auricular cartilage grafts
has been studied both experimentally and clinically. Peer (1941)
implanted autogenous costal cartilage beneath the chest and
Fig. 2. Comparison of the mean viability rates of the auricular cartilage groups at
nasal skin of human volunteers. Grafts harvested up to 6 years after
different time points.
implantation were reported to have a histologically normal
appearance. Gunter et al. (1997) reported a series of 28 patients in
who autogenous rib cartilage was used as columellar struts and/or
dorsal nasal grafts. Satisfactory aesthetic results were achieved in
all but one patient, in whom a dorsal nasal graft required removal
due to postoperative infection and partial graft resorption. Cakmak
and Ergin (2002) have used autogenous costal cartilage grafts for
structural and nonstructural purposes in 20 rhinoplasties and
reported no graft resorption or extrusion with a follow-up ranging
up to 32 months. Sheen (1998) has shared his clinical experience
with costal cartilage and advocated the use of crushed or morsel-
ised longitudinal strips of costal cartilage autografts for dorsal
reconstruction when septal cartilage was not available. In a clinical
study, Endo et al. (1991) used auricular cartilage layers as dorsal
grafts and reported occasional graft resorption in 1263 patients that
had been followed-up for a mean of 8 months. Although they did
not mention the amount of resorption, Becker et al. (2003) advo-
cated the use of auricular cartilage in revision rhinoplasty, based on
their clinical experience. Murrell (2004) has reviewed 101 patients
Fig. 3. Comparison of the mean viability rates of the costal cartilage groups at different
in whom auricular cartilage grafts had been used and reported no
time points.
graft resorption or extrusion after a follow up of up to 72 months.
Gruber et al. (2003) used auricular cartilage for grafting the nasal
3.6. Costal cartilage group dorsum and advocated not crushing or bruising the grafts in order
to avoid warping and irregularities and to prevent a possible
Similar to the auricular cartilage group, the results revealed in negative effect on resorption rates.
general that at all time points assessed the mean chondrocyte In an animal model Tjelmeland and Stal (2000) compared the
viability rates decreased as the level of the crushing applied resorption of auricular and costal cartilage. These authors reported
increased. The viability rates for the significantly and severely that the auricular cartilage resorbed more than the costal cartilage
crushed costal cartilage groups were significantly lower than the and carving had no effect on the amount of resorption. Lattyak et al.
corresponding rates for all the other groups. When examined in (2003) investigated and compared the biological characteristics of
detail, however, the difference between the intact and slightly cartilage autografts that had been taken from different donor sites
crushed cartilage groups, the difference between the slightly and in rabbits, and reported that the septal cartilage showed a higher
moderately crushed groups, and the difference between the resorption rate when compared with the auricular and costal
significantly and severely crushed cartilage groups were not cartilages. These authors’ results suggested that cartilage obtained
statistically significant. The difference between the intact and from different sources might undergo different degrees of resorp-
moderately crushed cartilage groups was statistically significant on tion. However, the biological properties of human cartilage prob-
day 1 (Fig. 3). ably differ from those of the animal cartilage, and confirmation of
There was no statistically significant difference between the this result in humans is needed. More recently, we investigated the
viability rates of the chondrocytes in similarly crushed auricular effect of different degrees of crushing on the viability of cultured
and costal cartilage groups, on days 1, 2, 3 and 10 (ManneWhitney human nasal septum chondrocytes (Cakmak et al., 2005a). In that
U test, P > .05) study, the mean viability rates for the intact human septal cartilage
group on days 1, 2, 3, and 10 were 96%, 93%, 93%, and 93%,
respectively. Since the cartilage autografts from different donor
4. Discussion sites might have different biological characteristics, one can assume
that the effects of crushing on the viability of these materials and
Autogenous nasal septal cartilage is the first graft of choice thus the clinical outcome may be different as well. We have been
when available for structural grafting or to camouflage mild to using both intact and crushed forms of the auricular and costal
moderate dorsal irregularities in rhinoplasty. Correction of more cartilages, as well as septal cartilage, in our clinical practice, with

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F. Buyuklu et al. / Journal of Cranio-Maxillo-Facial Surgery 39 (2011) 221e225 225

satisfactory aesthetic results (Cakmak and Ergin, 2002; Cakmak and References
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aog
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