Int. J. Oral Maxillofac. Surg.

2013; 42: 1054–1059

http://dx.doi.org/10.1016/j.ijom.2013.04.005, available online at http://www.sciencedirect.com

Research Paper
Trauma

Novel bone adhesives: U. Kandalama, A. J. Bouviera,

S. B. Casasa, R. L. Smitha,
A. M. Gallegoa, J. K. Rothrocka,
J. Y. Thompsona, C.-Y.C. Huangb,
a comparison of bond E. J. Stelnickia,c
a
College of Dental Medicine, Nova
Southeastern University, Fort Lauderdale, FL,

strengths in vitro USA; bUniversity of Miami, Miami, FL, USA;

c
Cleft and Craniofacial Center, Joe DiMaggio
Children’s Hospital, Hollywood, FL, USA

U. Kandalam, A. J. Bouvier, S. B. Casas, R. L. Smith, A. M. Gallego, J. K.

Rothrock, J. Y. Thompson, C. -Y. C. Huang, E. J. Stelnicki: Novel bone adhesives:
a comparison of bond strengths in vitro. Int. J. Oral Maxillofac. Surg. 2013; 42:
1054–1059. # 2013 International Association of Oral and Maxillofacial Surgeons.
Published by Elsevier Ltd. All rights reserved.

Abstract. Fracture fixation using adhesive is a promising alternative in craniofacial

surgeries, replacing the plates and screws system. The advantages include the ease
of application and avoidance of drilling holes that may weaken the bone and cause
fractures. In this study the bond strengths of selected adhesives were evaluated and
compared with resorbable plates and screws. Four adhesives, octyl-cyanoacrylate,
N-butyl-cyanoacrylate, a novel methyl-methacrylate, and a novel cyanoacrylate
derivative, were tested for their microtensile and shear bond strengths. The bone
samples were cut into rectangular bars and bonded with selected adhesives for
microtensile testing. For the shear bond test, paired bars were bonded at the overlap,
while two other sets of bars were attached by a Lactosorb plate using either adhesive
or screws. Data were analysed by analysis of variance (ANOVA). The microtensile
bond strengths of N-butyl-cyanoacrylate, novel cyanoacrylate derivative, and novel
methyl-methacrylate derivative were significantly greater than octyl-cyanoacrylate.
When bone sections were fixed with resorbable plates and adhesives, shear bond
Key words: adhesives; cyanoacrylate; plates
strength was significantly greater for N-butyl-cyanoacrylate than plate and screws, and screws; microtensile; shear bond strength.
while the bond strengths of other adhesives were comparable with the plate and
screws. N-Butyl cyanoacrylate was shown to have the greatest potential for fixation Accepted for publication 5 April 2013
of fractured bone in craniofacial surgical applications. Available online 15 May 2013

Recent advancements in craniofacial
surgical procedures have provided a
number of surgical innovations and
new biomaterials for internal fixation
methods. While conventional rigid fixa-
tion with metal plates and screws is ideal
for stable internal fixation,1 the disad-
vantages include extrusion, migration,
palpability, and growth restriction.2–7
The plate fixation system with screws
requires the drilling of holes that may
cause additional trauma and may weaken
the bone, causing further fractures.8,9
Furthermore, the load is mainly trans-
ferred onto the site of the screws, thereby
leading to punctual stress overload and
fixation failures.10
Resorbable fixation systems have been
found to be a good choice for fracture
fixation in recent years.11–13 The limitation
of the resorbable plates with screws system
is that it still requires drilling before screw
fixation. Moreover, during traumatic inju-
ries, fixing the bone fragments is difficult
using plates and screws. Adhesives remain
a promising alternative in cases where
the fixing of bone fragments is difficult
using plates and screws.14,15 The advan-
tages of using adhesive lie in the ease
of application, better biomechanical

0901-5027/0901054 + 06 $36.00/0 # 2013 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

properties, biodegradability, and the ability
to support bone healing.13,16
In order for an adhesive to be consid-
ered as part of an alternative fixation
method, it must fulfill certain criteria:
(1) have sufficient strength to be useful,
(2) be inert, non-toxic, non-carcinogenic,
and non-teratogenic, (3) adhere to moist
surfaces, (4) not interfere with the natural
healing process, (5) have chemical stabi-
lity, (6) be economically feasible, (7) be
bioresorbable, and (8) be as easy to use as
other conventional methods. Out of the
existing adhesives used in biomedical
applications, only a few meet these cri-
teria; these include cyanoacrylates and
methacrylates.
Cyanoacrylates are the most commonly
used group of adhesives for bone fixa-
tion.17 They have been found to have good
biomechanical strength and also work in a
wet environment. Additionally, they have
bacteriostatic and homeostatic proper-
ties.18–20 Studies on butyl- and ethyl-cya-
noacrylate have demonstrated an in vivo
half-life of 24–48 weeks.11,19,21,22 It has
been reported that the use of cyanoacrylate
adhesives does not hinder the vasculariza-
tion of newly formed bone.21,23
Methyl-methacrylate is commonly used
as a bone cement and has been used to fill in
traumatic skull defects for many years.24
Methyl-methacrylate is also a safe implant
material that is used in the craniofacial
region.25,26 Methyl-methacrylate is resorb-
able in the body, with an aqueous aerobic
degradation half-life of 1–4 weeks.27
In a recent in vitro study, the biomecha-
nical strength and biocompatibility of
methyl-methacrylate was assessed and it
was recognized as a promising biomaterial
for bone adhesion and bone regeneration.28
Furthermore, methacrylates do not repre-
sent a barrier for the vasculature during the
fracture fixation process,29 and some of
them show enhanced angiogenesis.30
The present investigation focused on
the use of acrylate-based adhesives for
the bonding of resorbable fixations to
craniofacial bone. The microtensile and
shear bond strength of cyanoacrylate-
and methyl-methacrylate-derived adhe-
sives alone were evaluated. The shear
bond strengths of adhesives and adhesives
in combination with resorbable plates
were evaluated and compared to the bond
strengths of resorbable plates and screws.
Materials and methods
In this study, bond strengths of two types
of novel adhesives, viz. a novel cyanoa-
crylate (NCA) and methyl-methacrylate
(NMMA) derivative, were evaluated and
Bond strengths of novel adhesives 1055
compared with N-butyl-cyanoacrylate
(BCA; provided by Biomet Microfixation,
Jacksonville, FL, USA) and the commer-
cially available adhesive octyl-cyanoacry-
late (OCA; Dermabond1, Ethicon Inc.,
Somerville, NJ, USA) which is currently
used in clinical practice. All of the speci-
mens in this study were randomly allo-
cated for testing.
Human cadaver parietal bone samples
were obtained from the National Disease
Research Interchange, Philadelphia, PA,
USA. Bone samples were stored at
70 8C ( 94 8F) until they were used.
Preparation of adhesives
Among the four adhesives tested, three
were liquid adhesives (derivatives of cya-
noacrylates) and one was a composite
(derivative of methyl-methacrylate). The
composite adhesive was prepared by hand
mixing the liquid monomer with the pow-
der filler. The mixing proportions were as
per the instructions of the manufacturer.
Bone sample preparation for
microtensile test
Bone samples were allowed to thaw for
about 1 h at room temperature and were
then cut into rectangular sections
(2 mm  2 mm  20 mm) using a low-
speed saw (IsoMet; Buehler, Lake Bluff,
IL, USA) with a diamond-rim blade (15 HC
IsoMet Wafering Blade; Buehler). Speci-
men size was determined based on the
available literature.31 The recommended Fig. 1. Example of microtensile bond
size for preparing specimens for microten- strength specimen.
sile testing is 1.6–1.8 mm2. This was deter-
mined as the minimal area that would Group 1—adhesives alone
produce a uniform distribution of stresses. Bone samples were cut into 2 mm 
However, due to the minimum width and 2 mm  20 mm rectangular sections using
thickness of the parietal bone sample pro- a low-speed saw. A lap shear test (ASTM
vided for this study, microtensile bars were D5868) was conducted with minor mod-
cut with a minimal area of 4 mm2. The ifications (Fig. 2A), with the specimen size
rough edges of the bone surface were similar to that for microtensile testing for
rounded using 320 grit abrasive paper (Car- comparison between the two groups. A
biMet; Buehler) in order to obtain samples custom-made fixture (Fig. 2B) was used
suitable for bond strength testing. The rec- for shear bond testing. The rectangular
tangular bars were sectioned perpendicular bone pieces were overlapped (10 mm)
to the long axis and made into equal halves onto each other and the adhesive was
and glued together with the selected adhe- applied in the region of contact (Fig. 2B).
sives (Fig. 1). A sample size of 10 speci-
mens per group was selected for the
microtensile test. Octyl-cyanoacrylate
Group 2—resorbable plates with adhesive
was chosen as the control as it is currently
used in clinical applications. Lactosorb resorbable plates (Biomet Micro-
fixation) measuring 6 mm  22.8 mm were
used. The bone sample size was determined
Bone sample preparation for shear bond
based on the size of the plates. Bone sam-
strength
ples measuring 6 mm  6.5 mm  40 mm
Samples were assigned to three different were prepared using the low-speed saw.
groups, as outlined below. Resorbable plates were cross-hatched with
1056 Kandalam et al.
Fig. 2. (A) Schematic figure of lap shear test. (B) Set-up for shear bond test.
a scalpel to obtain a rough surface in order
to increase the retention of the adhesive
onto the plate. The bone sections were
secured together with the plate and adhesive
(Fig. 3A).
Group 3—resorbable plates and screws
Bone samples measuring 6 mm 
6 mm  40 mm were prepared according
to the size of plates and screws
(Ø1.5 mm  3 mm; Biomet Microfixa-
tion). The fixation was performed using
Lactosorb plates with holes, fixed to the
Fig. 3. Example of resorbable plate shear specimens. (A) Resorbable plate and adhesive. (B)
Resorbable plate and screw.
outer cortex of each bone segment with the
Lactosorb screws (bone samples were
secured with the plates fixed with a total
of four screws, i.e., two screws on each
segment) (Fig. 3B). Screws were placed
after drilling a pilot hole slightly smaller
than the screw diameter.
For all of the experiments, the setting
time of the samples with adhesives was
kept to between 10 and 20 min and at
37 8C (98.6 8F) under humid conditions.
Cured bone sections were secured in
a linear configuration onto a universal
testing machine (Model 8831; Instron,
Canton, MA, USA) using a cyanoacrylate
ester (Rocket Heavy and Accelerator;
Dental Ventures of America Inc., Corona,
CA, USA). Load was applied to the fixture
with a crosshead speed of 1 mm/min until
failure. The maximum tensile and shear
bond strengths were recorded on a com-
puter attached to the machine and repre-
sented in a graph. Bond strength was
calculated in megapascals (MPa) from
the division of the maximum force (in
Newtons) by the known area of adhesive
applications. A sample size of five speci-
mens per group was selected for all three
shear testing groups.
Sample preparation for failure analysis
After the specimens were tested for micro-
tensile bond strength, they were removed
from the testing apparatus and the sites of
failure were observed under a stereo zoom
microscope (SMZ 140; VWR Interna-
tional, West Chester, PA, USA) to identify
the mode of failure. Bone samples were
air-dried overnight and mounted with the
fracture surface facing up on aluminium
stubs using a carbon tape. They were then
gold sputter coated and observed using a
scanning electron microscope (Quanta
200; FEI, Hillsboro, OR, USA). The mode
of failure was determined as being adhe-
sive (failure at the bonding surface, i.e.,
between bone and adhesive), cohesive
failure (failure in the material itself, i.e.,
failure within the adhesive or failure
within the bone), or mixed mode failure.
Data analysis
Data were analysed with a one-way ana-
lysis of variance (ANOVA) using Graph-
Pad PRISM (GraphPad Software, Inc., La
Jolla, CA, USA). Dunnett’s post hoc test
and Tukey’s multiple comparison test
were performed for inter-group compari-
sons. The criterion for statistical signifi-
cance was P < 0.05.
Results
The bond strengths are presented in MPa.
The force of failure reflects the bond
strengths of adhesives. The microtensile
bond strengths (Fig. 4) of BCA (2.18 
0.70 MPa), NCA (2.43  0.72 MPa), and
NMMA (2.92  0.73 MPa) were found to
be significantly stronger (P < 0.05) than
OCA (1.08  0.22 MPa). However, there
was no significant difference in the bond
strengths among these three adhesives
(P > 0.05). Scanning electron microscopy
results confirmed that all microtensile bond

Fig. 4. Microtensile bond strength of selected adhesives; OCA, octyl-cyanoacrylate, BCA, N-
butyl-cyanoacrylate, NCA, novel cyanoacrylate, NMMA, novel methyl-methacrylate
(*P < 0.05 as compared octyl-cyanoacrylate).
failures were mixed mode failures, as
shown in Fig. 5.
Shear bond strength testing results in
the adhesive group alone (Fig. 6) demon-
strated no significant difference (P >
0.05) between the bond strength of BCA
(1.97  0.22 MPa) and NCA (1.92 
0.30 MPa). While there was a more than
50% decrease in bond strength of NMMA
(1.09  0.47 MPa) compared to BCA and
NCA (P < 0.05), there was no significant
difference observed with reference to
OCA (1.08  0.14 MPa) (P > 0.05) when
applied directly to bone (Fig. 6). On the
other hand, shear bond strengths of all
adhesives were significantly greater than
that for the plate and screws group
(P < 0.05) when they were applied
directly to the bone sections (adhesives
alone group). When the adhesive was
applied along with the plate, only BCA
exhibited a significantly greater shear
bond strength (P < 0.05) when compared
to the plate and screws group (Fig. 7).
Shear bond strength testing plate failure
was observed in only one sample for group
2 (resorbable plates and adhesives), viz. in
BCA. There was no plate failure in group 3
(resorbable plates and screws group). All
samples in group 3 failed from pull-out of
screws from bone.
Fig. 5. Scanning electron microscope images showing mixed mode failure in a bone sample. (A) Presence of bone surface demonstrating adhesive
failure. (B) Presence of adhesive pull-out from the bone surface showing adhesive failure, presence of adhesive on the bone shows cohesive failure.
(Overall failure indicates that it was a mixed mode failure.)
Bond strengths of novel adhesives
Discussion
The use of adhesives is one of the appeal-
ing alternatives for internal fixation of
bones in craniofacial surgeries that can
replace pinning or screwing.29,32 A good
adhesive for consideration in clinical
applications should meet certain criteria,
such as an appropriate adhesive strength,
adequate time of action, and long-term
biocompatibility without interference with
the physiological healing process.29
Growing interest in adhesive fixation has
led to the production of substances with
adequate adhesive strength and adhesive
properties for use in clinical applica-
tions.33
The microtensile bond strengths of
NCA and NMMA adhesives were found
to be comparable to that of BCA
(P > 0.05). The microtensile bond
strengths of all of the adhesives showed
high levels of standard deviation. This
may be attributed to the fact that the bone
is a biological material with variation in
chemical and biomechanical properties
among individuals.34
Observed shear bond strengths of the
bone sections secured with resorbable
plates and adhesives were shown to be
comparable to that of plates and screws,
1057
expect for BCA, which was significantly
greater than all other adhesives. The long
lateral chain of OCA compared to BCA,
may be responsible for the observed
decrease in the adhesive properties of
octyl-cyanoacrylate.21
Our results showed that the shear bond
strengths of bones secured with adhesive
alone were greater than the bond strength
observed with resorbable plate and adhe-
sive. One possible reason for the decrease
in shear strength for the resorbable plate
and adhesive group is the composition of
the plate. Lactosorb resorbable plates,
which are 82% poly-L-lactide and 18%
polyglycolic acid,35 prevent ionization
and polymerization of cyanoacrylate
adhesives.17 This would contribute to
the observed reduction in the retention
of the adhesives to the resorbable plates.
Another reason could be that the surface of
the plates does not provide significant
mechanical adhesion when compared to
the surface of bone.
In this study we used an in vitro model
with human parietal bone samples. The
results presented here may not be identical
to prevailing conditions in vivo or may not
directly translate or address the clinical
scenario. However, the methodology
adopted here could easily be applied to
the shear stress in specific craniofacial
regions. For example, in a clinical situa-
tion such as sagittal split osteotomy of the
mandible for advancement or setbacks, the
shear forces may still occur. Nevertheless,
when bone has to be bonded in traumatic
injuries, overlapping shear forces occur,
albeit in a different direction. Our study
was focused on investigating the shear
bond strength in simulated experimental
conditions. Furthermore, when the plates
are bonded with glues or screws, and
pulled apart (as described in the Materials
and Methods under ‘‘experimental group
1058 Kandalam et al.
Fig. 6. Comparison of shear bond strength of adhesive alone (group 1) and resorbable plates and
screws (group 3); OCA, octyl-cyanoacrylate, BCA, N-butyl-cyanoacrylate, NCA, novel cya-
noacrylate, NMMA, novel methyl-methacrylate (*P < 0.05 as compared to resorbable plates
and screws).
3’’) they experience shear stress. Our
results demonstrate that the bonding
strengths of bones fixed with plates and
screws can also be achieved using glues
and thus may help surgeons to reduce the
time of surgery.
Specimens used for the microtensile
bond strength study were prepared with
a minimal surface area that would provide
a more uniform distribution of the stress to
the material.31,36 Most clinical failures
result primarily from the tensile forces
rather than shear forces.37 Hence, micro-
tensile properties of the adhesives may
provide better capacity for discrimination
than the shear bond strengths.37 Based on
this, it was thought that NMMA, which
had greater bond strength in microtensile
bond strength testing, may be one of the
potentially strong adhesives to be consid-
ered. However, the results of the shear test
with adhesive alone and adhesives with a
plate indicated BCA to have a signifi-
cantly greater bond strength than all of
the other adhesives.
The reason for the variations in
strengths of the NMMA might be the
method of preparation of the adhesive.
Unlike other adhesives, the preparation
of the novel methyl-methacrylate involved
many steps, including manual mixing of
Fig. 7. Comparison of shear bond strength of adhesive with plates (group 2) and resorbable
plates and screws (group 3); OCA, octyl-cyanoacrylate, BCA, N-butyl-cyanoacrylate, NCA,
novel cyanoacrylate, NMMA, novel methyl-methacrylate (*P < 0.05 as compared to resorbable
plates and screws).
two components: a liquid monomer and
solid powder filler. This might have
resulted in a product that was non-homo-
geneous and subject to batch-to-batch var-
iations.
In an in vitro model, Gosain et al.12
demonstrated that resorbable plates fixed
with adhesives were as strong as titanium
plates fixed with screws in regards to their
compression properties. On the other
hand, the distraction of bone segments
fixed with adhesives directly or secured
using resorbable plates displayed weaker
bond strength. The results of that study
indicated that adhesives are better used if
the forces of relapse are primarily com-
pressive. Gosain et al.12 reported that all of
the failures occurred at the plate–bone
interface in the group where plates held
the respective bone segments together
with adhesive. In our studies, this obser-
vation was true, with the exception of one
plate failure in one of the samples (BCA).
Previous results of in vivo studies with
BCA have indicated that adhesives might
be a viable option in place of the plates and
screws system.11,19,38 Studies on animal
models using BCA adhesives reported that
there was no significant difference in the
maximum torque needed to produce fail-
ure between the plated or adhesively fixed
bone fragments at any anatomic locations
tested.11,38 A comparative study to test the
healing strength and bone density of bones
fixed with metal plates and screws and
BCA revealed that there was no significant
difference in bone density or histological
analysis between the two groups.39
In conclusion, bond strengths of cya-
noacrylate and methyl-methacrylate adhe-
sives, to resorbable plates, were evaluated
for use as an alternative fixation system
for cranial bone. We identified N-butyl-
cyanoacrylate as having superior bond
strength to the resorbable plates, when
compared to other adhesives and the con-
ventional system of plates and screws. The
bond strengths of resorbable plates bonded
to bone using adhesive compared to that
of resorbable plates fixed with screws
were comparable. With comparable bond
strengths, using plates and glues is less
time-consuming and offers a viable alter-
native to the use of plates and screws,
especially in the management of traumatic
injury to the bones of the craniofacial
regions in situations where plate and screw
fixation is not possible. Further character-
ization of adhesives should include in vivo
degradation studies, in vivo defect-fixa-
tion animal studies, biocompatibility stu-
dies, and time-set kinetic analyses.
Funding
This work was supported by Biomet
Microfixation (Jacksonville, FL, USA).
Competing interests
There are no conflicts of interest.
Ethical approval
Not required.
Acknowledgement. The authors are grate-
ful to Dr Vijay Palaniswamy and Dr.
Eustrogio Lopez for their thoughtful sug-
gestions in the preparation of this manu-
script.
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Address:
Umadevi Kandalam
Department of Pediatric Dentistry
Nova Southeastern University
3200 South University Drive
Ft. Lauderdale
FL
USA
Tel: +1 954 262 7386;
Fax: +1 954 262 1782
E-mail: kandalam@nova.edu