use of titanium mesh in laryngotracheal reconstruction: an experimental study on rabbits

LARYNGOLOGY

Use of titanium mesh in laryngotracheal reconstruction:an experimental study on rabbits

Murat Yener • Gul Ozbilen Acar • Harun Cansiz •

Buge Oz • Engin Cigerciogullari • Oktay Seymen

Received: 11 November 2009 / Accepted: 18 December 2009 / Published online: 13 January 2010

� Springer-Verlag 2010

Abstract Titanium mesh may be an alternative material

to be used in laryngotracheal reconstruction. Twenty New

Zealand rabbits were divided into two groups. Group A

underwent laryngotracheoplasty with titanium mesh-buccal

mucosa-muscle complex, and Group B received auricular

cartilage grafts. All animals survived without complica-

tions. The animals were killed at 60 days, and laryngotra-

cheal regions were evaluated. There was no subglottic

collapse at physiologic and supraphysiologic negative air-

way pressures in Group A and mild-moderate collapse in

Group B. Macroscopically the average antero-posterior and

lateral diameters were not statistically different among two

groups. Light microscopic examination revealed no

fibrosis, necrosis or new cartilage formation in both groups.

Inflammation and granulation were more pronounced in

Group A. The lumens in both groups were moderately

obstructed. Reconstruction of the upper airway with tita-

nium mesh may be used in very selected cases where

autologous grafting materials are inadequate and

unsatisfactory.

Keywords Laryngotracheal � Reconstruction � Titanium �Mesh � Graft

Introduction

Management of subglottic laryngeal and upper tracheal

stenosis is a challenge for laryngologists. Many surgical

techniques have been described, including endoluminal

dilations, the use of lasers, hyoid bone grafts, costal car-

tilage grafts, nasal septal and/or auricular cartilage grafts,

endo-luminal stents, end-to-end tracheal anastomosis and

tissue-engineered cartilage grafts or prefabricated flaps.

There is no single method for reconstructing the airway;

each patient generally requires combination of different

techniques. The preferred surgical approach depends on the

severity of the stenosis [1]. For severe stenosis requiring

surgery, the method of treatment is cricotracheal resection

and anastomosis of the patent airway. For mild to moderate

stenosis requiring surgery, the preferred method is laryn-

gotracheal reconstruction, a less extensive procedure in

which the cricoid cartilage is split and expanded with a

graft [2]. To achieve this purpose, many grafts and flaps

have been used such as nasal septal and auricular cartilage

[3, 4], epiglottic cartilage [5], thyroid cartilage [6], costal

cartilage [7], sternocleidomastoid myoperiosteal flap [8]

and hyoid bone [9].

M. Yener

Otorhinolaryngology Department, Faculty of Medicine,

Namık Kemal University, Tekirdag, Turkey

G. O. Acar

Otorhinolaryngology Department,

Goztepe Research and Training Hospital,

Istanbul, Turkey

H. Cansiz

Otorhinolaryngology Department, Cerrahpasa Medical Faculty,

Istanbul University, Istanbul, Turkey

B. Oz � E. Cigerciogullari

Pathology Department, Cerrahpasa Medical Faculty,


O. Seymen

Physiology Department, Cerrahpasa Medical Faculty,


M. Yener (&)

Beylerbeyi Bayiri Sok No. 3, Beylerbeyi, Uskudar,

Istanbul, Turkey

e-mail: [email protected]

123

Eur Arch Otorhinolaryngol (2010) 267:1247–1253

DOI 10.1007/s00405-009-1189-z

However, there are some disadvantages of these autolo-

gous grafts like donor site morbidity, extra operative time

for harvesting and time required for carving the cartilage

into appropriate configuration [10]. These disadvantages

forced the investigators to find alternative materials to

cartilage, but these attempts are mostly experimental and

clinically not available [11–13]. In this experimental study,

we evaluated the effectiveness of a readily available

material, titanium mesh in the reconstruction of subglottic

region and compared the results with auricular cartilage

reconstruction.

Materials and methods

Twenty male white albino New Zealand rabbits aged

between 6 and 10 months and weighted between 1,500 and

1,850 g with otherwise normal airways were used in the

study. The experimental protocol was conducted in

accordance with guidelines published in the Guide for the

Care and Use of Laboratory Animals (DHEW publication

NIH 85-23, revised 1996, Office of Science and Health

Reports, DRR/NIH, Bethesda, MD, USA) and approved by

the Committee on Animal Research of the Istanbul Uni-

versity, Cerrahpasa School of Medicine, Istanbul, Turkey.

The study was done at the ‘Experimental Animal Studies

Laboratory’ of Istanbul University Cerrahpasa School of

Medicine. The rabbits were kept in different cages under

standard light and temperature conditions. The rabbits were

separated into two groups randomly consisting of ten rab-

bits in each group (Group A: titanium mesh and Group B:

auricular cartilage). Titanium mesh of 5 9 10 mm and free

buccal mucosal grafts for the Group A and composite aural

cartilage grafts with the same size for the Group B were

prepared and kept in sterile saline solution at the beginning

of the procedures.

Surgical procedure

Before each surgical procedure the rabbits were anesthe-

tized by ketamine at a dose of 50 mg/kg, and xylasine at a

dose of 10 mg/kg by intramuscular injection. The anterior

neck of each rabbit was shaved and disinfected. To

enhance analgesia, 2 mL of 1% lidocaine hydrochloride

was injected into the subcutaneous area of the anterior

neck. After midline skin incision in the anterior neck, lar-

ynx and trachea were exposed with care taken not to injure

the sternohyoid and sternothyroid muscles. Anterior cricoid

split was performed and a 5 9 10 mm opening was created

in the cricoid and superior tracheal rings. The rabbits in the

study group (n = 10) were reconstructed with titanium

mesh with free buccal mucosal grafts. The titanium mesh

of 5 9 10 mm size was placed on the medial surface of the

sternothyroid muscle and fixed to the muscle with two or

three interrupted 5/0 absorbable sutures with the buccal

mucosa facing the lumen of the subglottis (Fig. 1). Before

the fixation of the mesh over the subglottic region, the

mesh was wrapped between sternothyroid muscle and free

buccal mucosal graft; first fixed to the medial surface of the

sternothyroid muscle and the free buccal mucosa was laid

over the mesh medially, creating a composite material

consisting of muscle, mesh and buccal mucosa from lateral

to medial (Fig. 2). This composite flap was turned over the

opening as a rotatory door flap and fixed to the edges of

the subglottic opening with 5/0 nylon sutures (Fig. 3). The

rabbits in the control group (n = 10), however, were

reconstructed with autologous free aural cartilage grafts

harvested from pinna, which were secured into place with

interrupted 5/0 absorbable sutures. No airway stents were

used, and tracheostomy was not performed. Prophylactic

intramuscular gentamicin (5 mg/kg) injection was admin-

istered to each rabbit postoperatively. All animals recov-

ered from anesthesia and cared in the ‘Experimental

Animal Studies Laboratory’ of Istanbul University Cer-

rahpasa School of Medicine and all survived at the post-

operative period. At postoperative 60th day, the animals

were killed to evaluate the graft stability, collapse and

histologic examination by light microscopy.

Killing

All of the rabbits were killed by intravenous xylasine at a

dose of 20 mg 1 month after the operation, and the tra-

cheal-laryngeal specimens were excised for macroscopic

and microscopic examination.

Measuring collapsing pressures

The portion of the airway, including the reconstructed

segment, was isolated by clamps superiorly and inferiorly

Fig. 1 Intraoperative picture of laryngotracheal region. The mesh

was prepared and fixed to the medial side of the strap muscles

1248 Eur Arch Otorhinolaryngol (2010) 267:1247–1253

123

(Fig. 4) after the killing of each rabbit and a device adapted

from a sphygmomanometer with an 18-gauge needle was

used for inducing negative pressure to the reconstructed

region. The needle was inserted to the reconstructed region

and the degree of laryngotracheal collapse was noted at

physiologic negative airway pressures (-10 mmHg) and at

supraphysiologic negative airway pressures (-50 mmHg)

were noted. The antero-posterior length at the recon-

structed region was measured before the application of

negative pressure, and the same length was re-measured

during negative airway pressures, and the degree of col-

lapse was calculated as percentage.

Macroscopic examination

After killing, the laryngotrachea of each rabbit was dis-

sected and examined macroscopically to note antero-pos-

terior diameter, lateral diameter, granulation (0 none, 1

mild, 2 moderate, 3 severe), inflammation (0 none, 1 mild,

2 moderate, 3 severe) and luminal obstruction (3 patent, 1

moderately obstructed, 1 obstructed).

Light microscopic (LM) examination

For each rabbit the trachea was dissected from larynx to

carina and kept in formaldehyde solution. The specimens

were embedded in paraffin, and 5 lm sections were placed

on glass slides. Each slide was stained with Hematoxylin–

Eosine (H&E) to highlight fibrous tissue. The same

pathologist examined all the sections without knowing the

groups. Presence of inflammation (inflammatory cellular

invasion and number) (0 none, 1 mild, 2 moderate, 3

severe), angiogenesis (0 none, 1 mild, 2 moderate, 3

severe), foreign body reaction (0 none, 1 mild, 2 moderate,

3 severe), necrosis (0 none, 1 present), new cartilage for-

mation (0 none, 1 present), fibrosis (0 none, 1 present),

granulation (0 none, 1 mild, 2 moderate, 3 severe) and

lumen obstruction (3 patent, 2 moderately obstructed, 1

obstructed) were noted by using a grid system under light

microscope.

The statistical analysis was performed with student t test

and P \ 0.05 was considered significant.

Results

All of the animals survived during the study period. No

complication like bleeding, infection, subcutaneous

emphysema and immediate dyspnea was noted after the

surgical procedures. The skin sutures were removed 7 days

after the operation. Three animals in group A and one

animal in group B suffered from respiratory distress

beginning at postoperative 10th, 15th, 18th and 12th days,

respectively, but no intervention was taken to relieve the

symptom, and the animals did not suffocate.

Fig. 2 The mesh was wrapped between the strap muscles and buccal

mucosa graft

Fig. 3 The muscle-mesh-buccal mucosa complex was turned into the

tracheal defect like a rotatory door and fixed to close the opening

Fig. 4 Measurement of the collapsing pressures of the reconstructed

region

Eur Arch Otorhinolaryngol (2010) 267:1247–1253 1249

123

Collapsing pressures

In the isolated closed airway system at physiologic nega-

tive airway pressures (-10 mmHg) no collapse was

observed for the group A and about 20% collapse for the

group B. The results were statistically significant

(P \ 0.001). At supra-physiologic negative airway pres-

sures (-50 mmHg), the airway collapse was noted in all

animals, but the anterior wall was stable in the group A,

whereas there was about 50% collapse for the group B. The

results were also statistically significant (P \ 0.001).

Macroscopic findings

The macroscopic findings were summarized in Table 1.

Macroscopically the grafted region healed well without

any major complications (Figs. 5, 6). The average antero-

posterior diameter of the reconstructed region was

0.45 ± 0.08 cm for Group A and 0.37 ± 0.08 cm for

Group B, which was not statistically significant (P =

0.46). The average lateral diameter was 0.28 ± 0.06 cm

for Group A and 0.3 ± 0.06 cm for Group B, which was

not also statistically significant (P = 0.5). Also in the

macroscopic examination granulation, inflammation

and lumen obstruction were investigated. In Group A

moderate granulation (2.6 ± 0.6) was present, whereas the

granulation in Group B was less (1.7 ± 0.48) and was

statistically significant (P = 0.04). The average inflam-

mation score of Group A was 2.2 ± 0.6 and 1.9 ± 0.31 for

Group B, which was not also statistically significant

(P = 0.19). The degree of lumen patency was also evalu-

ated that yielded moderately obstructed lumen in Group A

(1.9 ± 0.6) and moderately obstructed lumen in Group B

(2 ± 0.6). The difference was not also statistically signifi-

cant (P = 0.72).

Microscopic findings

The microscopic findings were summarized in Table 2. In

the light microscopic examination no fibrosis, necrosis or

new cartilage formation was noted in both groups.

Inflammation was more severe in Group A than Group B

(2.2 ± 0.63 vs. 1.3 ± 0.48), and the difference was sta-

tistically significant (P = 0.02). Also granulation was more

pronounced in Group A (1.8 ± 0.63) than Group B

(1.2 ± 0.42), which was also statistically significant

(P = 0.02). Foreign body reaction in Group A was

1.6 ± 0.69 and was 1.3 ± 0.48 in Group B (P = 0.27).

We noted none to mild angioneogenesis in both groups that

was not also statistically significant (0.5 ± 0.52 for Group

A, 0.4 ± 0.51 for Group B; P = 0.67). In the evaluation of

lumen patency, we noted moderately obstructed lumen in

Group A (2.1 ± 0.66) and moderately obstructed lumen in

Group B (1.8 ± 0.63). The difference was not statistically

significant (P = 0.5).

Table 1 Summary of

macroscopic findings

The value in bold represents

P \ 0.05

Group Ant-post diameter Lateral diameter Granulation Inflammation Lumen obstruction

A 0.45 ± 0.08 0.28 ± 0.06 2.6 ± 0.6 2.2 ± 0.6 1.9 ± 0.6

B 0.37 ± 0.08 0.3 ± 0.06 1.7 ± 0.48 1.9 ± 0.31 2 ± 0.6

P value 0.46 0.5 0.04 0.19 0.72

Fig. 5 Postoperative 60th day view of the reconstructed region. Note

that the reconstructed region with titanium mesh healed well without

necrosis

Fig. 6 Postmortem view of the laryngotracheal region. Note that the

reconstructed region was healed without any major complications


123

Discussion

There are still controversies in the treatment of subglottic

stenosis and remains a dilemma in field of laryngology.

Many authors with different success rates have offered

many grafts or flaps for expansion of the upper airway.

Autologous grafts are generally the most preferred mate-

rials in the laryngotracheal reconstruction, but pose some

potential problems like donor-site morbidity, variable graft

resorption and prolonged operating time [13, 14]. Also,

there is a risk of graft necrosis that was the main purpose of

studies demonstrating the use of vascularized grafts. Such

grafts were successfully used in reconstruction, which had

benefits of resistance to infection, chondritis and sub-

sequent re-stenosis [15]. The authors of this manuscript

successfully used autologous composite nasal septal graft,

muscle-pedicle hyoid bone flaps in subglottic and tracheal

reconstruction, but we believe that some alloplastic mate-

rials should be introduced to the field of laryngology in

order to overcome disadvantages of autologous grafts like

resorption, risk of infection or necrosis [16, 17].

There are various articles that specify the benefits of

various implants, but each material has some disadvantages

like rejection and extrusion [13]. The ideal implant to be

used in upper airway reconstruction should allow epithe-

lization, resist infection, cause minimal scarring, be rigid

and also flexible, and allow for single stage repair without

stenting [13, 18]. To achieve these purposes Klein et al.

[13] used polyglycolic acid/poly-L-lactic acid copolymer in

laryngotracheal reconstruction of rabbits and noted that the

material was safe, maintaining adequate strength and

patency. Mitskavich et al. [19] used microplates in a por-

cine model with subglottic stenosis. They produced sub-

glottic stenosis and reconstructed the stenotic region with

anterior cricoid split and micro plate distraction and sta-

bilization. They suggested that this rigid fixation was a

viable alternative to traditional methods without stenting or

risks of a donor site. Casiano et al. [14] used titanium plates

in tracheoplasty with strap muscle flap in nine patients and

decanulated seven of the subjects. Hashem et al. [12] used

med-pore implant in laryngotracheoplasty in an animal

model and achieved successful results in tracheal recon-

struction. Stein was the first author who used titanium

screen implant with rotary door flap. They implanted the

screen into the sternohyoid muscle and closed the laryn-

gofissure by 180� rotation of the flap. They also used

porous polyethylene, hydroxylapatite cement with rotary

door flap and concluded that such support materials did not

improve stability, increased the difficulty to flap harvest,

caused dehiscence and migration and raised mortality rate,

but the best results were achieved with titanium screen

[20]. Our study is somehow different from the study of

Stein et al. in the usage of the titanium mesh. In their study,

Stein implanted the titanium screen into the muscle,

whereas we wrapped the mesh with muscle and buccal

mucosa. We secured the buccal mucosa onto the medial

surface of the sternothyroid muscle and achieved the via-

bility of the mucosal graft demonstrated by mild angio-

neogenesis and no necrosis or fibrosis microscopically. In a

more recent study, Janssen et al. [21] used porous titanium

to investigate if its support for revascularization of a

mucosal graft in tracheal reconstruction. They concluded

that porous titanium was an inert biomaterial that provided

support and allowed easy revascularization of a mucosal

graft. This study also supports our findings.

Titanium mesh was used in this study in the recon-

struction of the anterior wall of the rabbits and compared

the results to a well-known and widely accepted material;

auricular cartilage grafts, as the material is biocompatible

with sufficient tensile and fatigue strength [22]. Also,

absence of chemical foreign effect and presence of soft

tissue and bone adherence make titanium favorable in

terms of tissue susceptibility to infection [20, 23]. The

stability of the titanium was demonstrated by induction of

supraphysiologic negative pressure to the reconstructed

area, and we did not note any collapse in titanium but some

degree of collapse in auricular cartilage. These results are

compatible to the results of some previous manuscripts [13,

20]. We believe that titanium mesh with its high strength

and durability may be used in patients with subglottic

stenosis, in whom malacia is a major problem. It is early to

give clinical recommendations, and we believe the material

must be tested in very selected cases with insufficient

autologous grafting materials.

The measurements of the subglottic dimensions in this

study yielded a larger antero-posterior diameter than the

Table 2 Summary of microscopic findings

Group Inflammation Neo-vascularisation Foreign body

reaction

Necrosis New cartilage

formation

Fibrosis Granulation Lumen

obstruction

A 2.2 ± 0.63 0.5 ± 0.52 1.6 ± 0.69 0 0 0 1.8 ± 0.63 2.1 ± 0.66

B 1.3 ± 0.48 0.4 ± 0.51 1.3 ± 0.48 0 0 0 1.2 ± 0.42 1.8 ± 0.63

P value 0.02 0.67 0.27 0.02 0.5

The values in bold represent P \ 0.05


123

lateral diameter composing an oval shape with longer AP

axis. This diameter was also longer in Group A. This

finding is in accordance with the findings of Klein and

Silver [13, 24]. This was proposed to form from the oblong

growth of broken cricoid ring caused by unopposed bio-

mechanical stresses [13] or may be due to anterior dis-

placement as a result of anterior drawing effect of the mesh

and muscle complex.

The presence of mild to moderate foreign body reaction

and no extrusion of the mesh note the biocompatibility of

the material, but the degree of inflammation and granula-

tion were more pronounced in the titanium mesh group.

Clinically we detected difficulty in breathing and stridor in

three animals with titanium mesh and one animal with

auricular cartilage after tenth day, but all the animals sur-

vived to the end of the experiment. In a study of Gaafar

et al. [25] titanium mesh was used to augment the anterior

wall of the patients with stenosis. They detected severe

granulation in some of their patients. This was true for the

animals in Group A in our experiment. After harvesting the

trachea and larynx, we noted moderately obstructed lumen

in both groups, Group A being more obstructed, which was

not statistically significant. The more pronounced

obstruction in Group A was due to granulation and edema

especially in the animals with clinical stridor. In their

microscopic examination, we detected that the edges of the

mesh was naked; the mucosal graft was alive but shrunken

in size. This severe complication may cause problems like

pronounced granulation, edema and obstruction in the

long-term prognosis of the cases. As the material is not

flexible but rigid, and the trachea and larynx is dynamic

that moves with inspiration, expiration and swallowing, we

believe that the rigid edges of the implant irritated the

implanted region causing more granulation and inflamma-

tion. Application of the material with larger skin grafts may

avoid this reaction. The presence of granulation and

inflammation in these cases might be problematic and

might restrict the use of titanium mesh, but more clinical

and experimental trials are needed.

Conclusion

These are early postsurgical results and long-term studies

need to be conducted before use in humans could be con-

sidered. Clinical investigations in very selected frustrating

cases, where autologous grafting materials were inadequate

and unsatisfactory, must be performed. The material

achieves stable and airtight airways under physiologic and

supraphysiologic conditions. Although there are some

limitations of this study such as small number of the

experiment animals, need to extrapolate from the animal

model and use in clinical practice and lack of subglottic

stenosis in this model, we believe that titanium mesh can

be reliably used in cases where more rigid stability is

necessary like tracheo-laryngomalacia.

Acknowledgments The authors of this paper declare that they have

no conflict of interest. There is no financial and material support for

this research. There are no financial interests the authors may have in

companies or other entities that have an interest in the information in

the contribution.

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use of titanium mesh in laryngotracheal reconstruction: an experimental study on rabbits

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