ORIGINAL ARTICLE

BIOACTIVE GLASS S53P4 IN FRONTAL SINUS OBLITERATION:

A LONG-TERM CLINICAL EXPERIENCE
Matti Peltola, MD, PhD, DDS,1 Kalle Aitasalo, MD, PhD, DDS,1 Jouko Suonpaa, MD, PhD,1
Matti Varpula, MD, PhD,2 Antti Yli-Urpo, DDS, PhD3
1
Department of Otorhinolaryngology, Head and Neck Surgery, Turku University Hospital, FIN-20521
Turku, Finland. E-mail: matti.peltola@tyks.
2
Department of Diagnostic Radiology, Turku University Hospital, Turku, Finland
3
Institute of Dentistry, University of Turku, Turku, Finland

Accepted 23 December 2005

Published online 5 July 2006 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/hed.20436

Abstract: Background. Synthetic, osteoconductive, and anti-

microbial bioactive glass (BAG) has been used in many surgical
applications.
Methods. BAG was used as obliteration material in a series
of osteoplastic frontal sinus operations on 42 patients suffering
from chronic frontal sinusitis, which could not be cured with
other means of treatment.
Results. Accurate obliteration of sinuses was achieved in 39
patients. Uneventful recovery and clinical outcome were seen in
92% of the patients. Histopathologic samples harvested at 1, 5,
and 10 years after obliteration revealed a healing process pro-
gressing from the brous tissue phase to bone formation with
scattered brous tissue and bony obliteration maintaining BAG
granule remnants. Fourier-transform infrared (FTIR) studies
showed bone produced by BAG to be similar to natural frontal
bone. Micorobiologic cultures obtained with histologic samples
revealed no growth of bacteria.
Conclusions. BAG appears to be a reliable frontal sinus
obliteration material, providing favorable conditions for total
bony sinus obliteration. V C 2006 Wiley Periodicals, Inc. Head
Neck 28: 834841, 2006
Keywords: BAG; frontal sinus obliteration; long-term
Correspondence to: M. Peltola
V
C 2006 Wiley Periodicals, Inc.
Most conditions of the frontal sinus requiring
surgery can be treated successfully by endonasal
or nasofrontal duct reconstruction procedures.17
However, in certain difcult cases, optimal expo-
sure of the entire frontal sinus is essential. Indica-
tions of frontal sinus obliteration include those
problematic conditions that are not resolvable
with functional endoscopic sinus surgery tech-
niques, because of irreversibly damaged natural
drainage.7,8
Since its description in the literature,9,10 the
osteoplastic ap with fat obliteration has become
the standard operation for chronic frontal sinus
disease.1115 According to Hardy and Montgom-
ery,13 the overall complication rate in frontal
sinus obliteration with fat is 18%, including ab-
dominal donor site morbidity, wound complica-
tions, postoperative infections, fat necrosis, and
recurring chronic sinusitis. However, a complica-
tion rate of 25% in frontal sinus obliteration
using traditional obliteration methods has also
been presented.16 An exceptionally high failure
rate in frontal sinus obliteration with muscle,
including re-aeration and sinus infections, has
been described.17

834 Bioactive Glass S53P4 in Frontal Sinus Obliteration HEAD & NECKDOI 10.1002/hed September 2006
Synthetic Obliteration Materials. The benets of
synthetic materials are the avoidance of donor-
site morbidity and scars, prolongation of opera-
tion time, and complexity of surgical technique.18
In addition, with allogenic transplants, there is,
in principle, a risk of biohazard infections, for
example, human immunodeciency virus (HIV)
and hepatic viruses.19,20 Synthetic materials use
in this setting include the following:
Methyl methacrylate: This acrylic resin is one
of the most widely used alloplastic materials
in head and neck surgery. However, the mate-
rial produces a signicant exothermic reaction
when liquid monomer and powder polymer
are combined. In addition, foreign-body reac-
tion with acrylate has been noted.21
Hydroxyapatite: This material has been inves-
tigated in frontal sinus obliteration,22 but the
long-term clinical outcomes are unknown.
Glass ionomer cement: This material has also
been used in frontal sinus reconstruction.23
Since severe complications using glass ionomer
cement next to the dura mater have been found,
this material has been taken off the market.7
Proplast or Polytef: This Teon uorocarbon
polymer has vitreous carbon bers. It is ex-
tremely porous to body uids.24 The material
can cause a mild foreign-body reaction. The
results in a clinical follow-up study lasting to
5 years and in radiologic studies, showed signs
of probable connective tissue inltration.21,24
Bioactive Glass. A bioactive material is one that
elicits a specic biologic response at the interface
of the material, resulting in the formation of a
bond between tissues and the material.25 Bioac-
tive glasses and ceramics are synthetic materials
based on a SiO2Na2OCaOP2O5Al3O2MgO obstruction (17 patients), orbital swelling (16
K2O structure. These materials have been shown
to be biocompatible and nontoxic.26,27
Bioactive glass S53P4 (BAG) of the composi-
tion SiO2 53.0; CaO 20.0; Na2O 23.0; P2O5 4.0 wt%
has been used in clinical frontal sinus oblitera-
tion.28 In the experimental research of the disso-
lution on ions from clinical frontal sinus oblitera-
tion, the amount of BAG used showed BAG to be a
stable material.29 In addition, a reliable clinical
follow-up and evaluation of the outcome of the
obliteration with BAG can be performed indirectly
with CT and with the region of interest (ROI)
method.30 Comparison and evaluation of the dif-
ferences between the synthetic materials in an ex-
Bioactive Glass S53P4 in Frontal Sinus Obliteration
perimental frontal sinus and skull bone defect
obliteration were carried out.31,32 The control
materials were hydroxyapatite and bioactive
glass 1393. In these studies, BAG produced more
new bone than the control materials during the
observation periods of 1, 3, 6, and 12 months. In
addition, in the Fourier transform infrared spec-
troscopy (FTIR) studies, the bone produced by
BAG and bioactive glass 1393 was of the same
type as natural frontal bone, whereas the bone
produced with hydroxyapatite differs from natu-
ral bone. The bone formation in monkey mandibu-
lar cortical bone defects was higher with bioactive
glass than with synthetic hydroxyapatite, or with
tricalcium phosphate.33,34
The combined effects of BAG, hydroxyapatite,
and the oral microorganisms were experimentally
studied.35 All microbes lost their viability when
placed in contact with BAG. On the surface of hy-
droxyapatite, stronger adhesion and colonization
of bacteria were found. Furthermore, the effects of
BAG on Haemophilus inuenzae and Streptococ-
cus pneumoniae were studied.36 BAG did not favor
the adhesion of either H. inuenzae or S. pneumo-
niae on the surface of BAG particles.
PATIENTS AND METHODS
Patients. Forty-two consecutive patients, 20 wom-
en and 22 men, suffering from chronic suppura-
tive frontal sinusitis and treated surgically by
osteoplastic frontal sinus obliteration, were en-
rolled in the study. Informed consent was obtained
from all patients. The mean age of the patients
was 53.9 (range, 2079 years). The duration of
symptoms varied from 3 months to 12 years. All
patients reported chronic frontal pain as their
chief complaint. Other symptoms included nasal
patients), and diplopia (2 patients). One patient
had a stula in the frontal skin as a sign of frontal
sinus pyocele. Three patients reported paresthe-
sia on the frontal region as a complication of previ-
ous operations. Ten patients had nasal polyposis,
and 7 had frontal sinus mucocele. Acetylsalicylic
acid intolerance was diagnosed in 5, and nasal
allergy in 9, while 13 patients had asthma and 4
had diabetes. Table 1 presents the previous sinus
operations of 42 patients. Five patients had a his-
tory of some type of osteoplastic operation, 1 had
undergone earlier attempts at Lynch frontal
sinusotomy, and 1 had undergone Killian frontal
sinusotomy. Frontal sinus trephines were per-
HEAD & NECKDOI 10.1002/hed September 2006 835

Table 1. Previous operations in 42 patients undergoing
osteoplastic frontal sinus obliteration with bioactive glass.
No. of operations
No. of in one
Surgical procedure patients patient, range
Frontal trephine 16 16
Osteoplastic operation 5 13
with obliteration
External frontoethmoidectomy 9 13
Endoscopic frontal sinusotomy 4 12
Endonasal ethmoidectomy 16 15
Caldwell-Luc operation 9 12
Septoplasty 3 1
Frontobasal fracture 1 1
No previous operations 3 erative controls only in the case of clinical need. In
formed in 16 patients. The decision to operate was
based on history and ndings from frontal sinus
CT scans. Because of the previously described reli-
able outcome with BAG in frontal sinus oblitera-
tion in 10 patients followed up for 5 years,28 and
the limited number of patients, BAG was used
without clinical control material in this long-term
study.
Operation. The osteoplastic operations were per-
formed through a bicoronal (35 patients) or eye-
brow (7 patients) incision. The upper orice of the
nasofrontal duct was obliterated using a dense 3-
layer-containing occlusion plug (pericranial peri-
osteum-lyoplant-pericranial periosteum) and -
brin glue. BAG granules, 0.50.8 and 0.81.0 mm
in size (Vivoxid Ltd, Turku, Finland), were mois-
tened with saline, and frontal sinuses were oblit-
erated accurately with BAG granules. The
detailed description from the operative technique
has been published previously.28 In 11 patients,
frontal trephine holes in the anterior frontal bone
approximately 5 mm in diameter, were not com-
pletely healed. The largest frontal bone defect,
approximately 2.5 cm2 in size, was found in a
patient who had undergone 3 obliterations before
the nal BAG obliteration. The frontal bone
defects were revised and lled with BAG at the
same time as the sinus obliterations were per-
formed. The patients were given intravenous cefu-
roxim for 5 postoperative days.
Follow-up Examinations. Patients were closely
followed up by the surgeons (KA, JS, MP). The
protocol for clinical evaluation of the frontal sinus
obliteration patients was the same for all the
patients. Two of the 42 patients attended only
836 Bioactive Glass S53P4 in Frontal Sinus Obliteration
1-month and 3-month controls in Turku Univer-
sity Hospital. One patient was taken ill with
amyotrophic lateral sclerosis. His clinical data
were available up for 24 months and showed an
uneventful clinical frontal sinus obliteration. One
patient died of pulmonary carcinoma 8 years after
obliteration.
The results of the clinical examinations and
patient symptoms were recorded at 1 week, 1, 3,
and 6 months, and thereafter annually. CT scans
were obtained at each observation point. Routine
hematologic tests, including C-reactive protein
(CRP) and creatinine, were carried out at postop-
clinical examinations, a progressive healing pro-
cess with diminishing postoperative clinical symp-
toms and normally progressing skin wound heal-
ing were the criteria for acceptance. In CT studies,
the acceptable outcome was accurate frontal sinus
obliteration without loss of volume. In histologic
studies, special attention was paid to new bone
formation and resorption of BAG.
In region of interest (ROI) evaluation, the sta-
bility and preservation of BAG obliteration were
estimated by the variation in Hounseld units
(HU). The cortical calvarial bone was used as a ref-
erence in the clinical ROI evaluation. The clinical
level of cortical calvarial bone mean HU varies
from 1590 to 1670.30 The criteria used to evalu-
ate the outcome of frontal sinus obliteration in ROI
evaluation were set at the known level of bone tis-
sue and bioactive glass on the Hounseld scale. On
that scale, the mean values of compact bone vary
from 300 HU to 1100 HU.37 The initial mean
HU in the clinical frontal sinus obliteration with
BAG granules in an experimental and clinical fron-
tal sinus obliteration model varies from 1350 to
1250 HU, with HU decreasing during the follow-
up to 900 HU at 48 months.38,30
To date, our mean follow-up time is 6.1 years
(range, 3 months to 13.1 years). Twenty-four
patients were followed up for more than 5 years,
and the number of patients whose follow-up lasted
more than 10 years was 12. CT studies were per-
formed in all patients and ROI evaluation in 30
patients for up to 7 years. Two patients had dis-
comfort after the obliteration in the frontal area.
The discomfort was related to the miniplates used
for xation of the osteoplastic ap and, thus, they
were removed. One patient had severe basal cell
carcinoma in the frontal skin area and a residual
basal cell carcinoma operation was performed. In
addition, 2 patients underwent reobliteration be-
cause of mucocele formation. Histologic and micro-
HEAD & NECKDOI 10.1002/hed September 2006
 Table 2. Symptoms at follow-up after osteoplastic frontal sinus obliteration with bioactive glass in 42 patients.
Symptoms in frontal region
Chronic frontal pain
Supraorbital nerve pain
Paresthesia in supraorbital region
No. of subjects not satised with the treatment
biologic samples were harvested from above-men-
tioned 5 patients. These samples were harvested
from different patients at 6, 12, 60, 104, and 120
months after the primary BAG obliteration,
respectively.
The study plan was reviewed and approved by
the Joint Commission on Ethics of Turku Univer-
sity and Turku University Hospital.
Statistical Analysis. The variation of HU in ROI
evaluation was analyzed using a random coef-
cients regression model. Statistical analyses,
tables and graphs were performed with SAS1 ver-
sion 8.2 for Windows (SAS Institute, Cary, NC).
RESULTS
All patients obtained relief from their intense
frontal pain and had a satisfactory cosmetic result
at 12 months postoperatively. At 3 months, 10
patients reported discomfort comparable to neu-
ralgia over the innervation area of the supraorbi-
tal nerve, but the symptoms diminished with
time. Chronic frontal pain was recorded at
3 months in 7 patients, but it diminished during
the follow-up. Paresthesia in the supraorbital
region was observed in 6 patients. Dissatisfaction
of the treatment was not observed. In 1 patient,
wound healing was delayed up to 12 months post-
operatively because of recurrent basal cell carci-
noma. After wound revision, healing progressed
normally. Postoperative neuralgia and paresthe-
sia, persistent in 2 patients at 36 months, were
probably caused by damage to the supraorbital
and supratrochlear nerves, due to the eyebrow
incision used in earlier operations (Table 2).
Histology. In the obliterated frontal sinuses, the
dense brous tissue revealed by histopathologic
studies, between the BAG granules and the reac-
tion layers formed on the BAG granule surface at
6 and 12 months as described earlier.28 Two
patients had frontal pain and swelling in the left
frontal sinus area at 104 and 120 months after
obliteration. CT scans showed a mucocele forma-
tion laterally in the left frontal sinus. Reoblitera-
Bioactive Glass S53P4 in Frontal Sinus Obliteration
3 mo 6 mo 12 mo 36 mo
7 5 1 0
10 6 3 1
6 4 2 1
0 0 0 0
tion with BAG was performed. Clinically, in the
operation eld, new bone formation was seen
between BAG granule remnants in the obliterated
frontal sinuses. The suspicion of mucocele was
conrmed in the operations and in histopathologic
studies. The histologic studies revealed more new
bone formation with less scattered brous tissue
formation between the BAG granules in frontal
sinuses at 104 and 120 months versus at 60
months (Figure 1). Two patients had an enlarged
ethmoidal mucocele in contact with the BAG obli-
terated frontal sinus bottom area. In above men-
tioned 2 patients, a Lothrop-type operation was
performed at 20 and at 117 months when ethmoi-
dal mucoceles were removed. Frontal sinus oblit-
erations with BAG were visualized from below,
and dense obliterations were seen. BAG oblitera-
tion completely occluded the frontal sinuses. His-
tologic studies revealed BAG granule remnants
and lamellar bone formation. No inammatory
changes or foreign-body reactions were seen.
Scanning electron microscope back-scatter
mode studies showed new bone formation with
BAG granule remnants covered by a calcium
FIGURE 1. Histologic 20-lm-thick section from bioactive glass
(BAG) obliteration at 120 months after operation. Lamellar new
bone formation with minor scattered brous tissue between glass
granule remnants (Masson Goldner stain; original magnication
310; scale bar 0.1 mm). [Color gure can be viewed in the
online issue, which is available at www.interscience.wiley.com.]
HEAD & NECKDOI 10.1002/hed September 2006 837

FIGURE 2. Scanning electron microscope back-scatter mode
picture of bioactive glass at 104 months after frontal sinus obliter-
ation with bioactive glass. White areas in middle of new bone for-
mation are calcium phosphate (original magnication 315; scale
bar 2.0 mm)
phosphate layer at 104 months (Figure 2). Fourier
transform infra-red spectroscopy studies showed
the natural anterior frontal bone to be very simi-
lar to the bone produced by BAG in the frontal
sinus obliteration (Figure 3).
Microbiologic cultures from the BAG oblitera-
tions showed no growth of bacteria. The blood
chemistry of the operated subjects revealed no
unexpected values in basic blood analysis or in
CRP or serum creatinine levels.
FIGURE 3. Fourier transform infrared (FTIR) spectroscopy of
the sample at 104 months postoperatively and of natural human
frontal bone. Lower line, natural frontal bone; upper line, bone for-
mation in bioactive glass (BAG)-obliterated frontal sinuses. In FTIR
spectra, l, carbonate groups; n, phosphate groups; ~, organic
material.
838 Bioactive Glass S53P4 in Frontal Sinus Obliteration
Computed Tomography. A radiologic evaluation
with CT at the observation point of 1 week, 6
months, 12 months, and thereafter annually was
made in 42 patients. In the CT scans, the BAG
obliterations were found to be stable and there
was no loss of volume (Figure 4). Two patients
complained of deterioration of frontal symptoms,
and CT scans were taken. Incomplete frontal
sinus obliterations were found in 3 patients. One
patient had insufcient frontal sinus obliteration
due to insufcient closure of the nasofrontal duct,
and the other 2 had mucocele formation. These
deviating ndings were seen, respectively, at 34,
104, and 120 months postoperatively. After reob-
literation, accurate frontal sinus obliterations
without any deviating ndings were seen. An
uneventful outcome was observed in the CT scans
of the patients whose frontal bone defects were
obliterated at the same time as they underwent
frontal sinus obliteration.
Region of Interest. The ROI evaluation (Figure
4) was performed in 30 patients from the middle of
the BAG obliteration in 9 separate CT image
regions. The mean density of BAG obliteration
and reference bone with standard deviations in
FIGURE 4. Obliterated frontal sinus with bioactive glass (BAG)
on a 3-mm-thick CT scan at 12 months after operation. Three
separate regions (13) in the middle of BAG obliteration were
analyzed by region of interest (ROI) technique, and the position
of scanned areas was standardized at each scanning session.
The separate regions of equal area and location of the calvarial
bone (4) were used for reference throughout follow-up. Scan-
ning parameters of 120 kV and 100 mA/s were used.
HEAD & NECKDOI 10.1002/hed September 2006

FIGURE 5. Region of interest (ROI) evaluation from bioactive
glass (BAG) obliteration CT scans. Columns show mean den-
sity in Hounseld units (HU) with standard deviation.
the ROI evaluation are given in Figure 5. The
number of patients at each observation point, and
the average decrease between 1 week and later ob-
servation points, are given in Table 3. The
decrease in HU was seen between 1 week and 24
months, after which the HU level seemed to
decrease up to 48 months. Thereafter, the HU
level was stable beginning to increase slightly up
to approximately 1000 HU. Only minor variation
in HU was observed in ROI evaluation after 12
months. The variation in HU showed reliable
preservation of BAG obliteration in frontal
sinuses. The variation (1.5% to 3%) in the HU of
standard calvarial bone was very similar to that
described earlier.30
DISCUSSION
In frontal sinuses, the infection usually originates
from the ostiomeatal unit inside the ethmoids, in
prolonged or recurrent infections, and, thus, most
conditions of frontal sinuses requiring surgery
can be successfully resolved with endoscopic sur-
gery. Furthermore, transnasal endoscopic meth-
ods have certain advantages over the conven-
tional external approach, advantages such as
avoidance of facial scars, preservation of the bony
Table 3. Number of patients at each observation point in ROI evaluation among 30 patients. Mean decrease in HU between 1 week
and later observation points in ROI analysis.
Mean HU variation in % 8.2
No. of patients 30 24
Observation point 1 wk 6 mo
Abbreviations: ROI, region of interest; HU, Hounseld units.
Bioactive Glass S53P4 in Frontal Sinus Obliteration
superstructures of the frontal sinus infundibu-
lum, and preservation of a greater amount of mu-
cosa.39 Despite many advances in frontal sinus
surgery,40 there are still problematic cases in
which the osteoplastic procedure with obliteration
is needed.7,8
In the present study, the long-term complica-
tions were 2 mucoceles (4.8%) and 1 obliteration
that was reoperated (2.4%) due to insufcient
nasofrontal duct occlusion. The total complication
rate was 7.2%. The indications for reobliterations
were not related to the properties of BAG, but to
the inadequate operative technique. The overall
complication rate was lower than previously
described.13,16 According to Montgomery and van
Orman,41 the osteoblastic theory of osteogenesis
does not explain the frontal sinus bone formation,
because the frontal sinuses are rendered free of
periosteum and endosteum in obliterative frontal
sinus surgery, and, thus, the osteogenesis prob-
ably occurs as a result of metaplasia of connective
tissue. The present clinical long-term follow-up
study reveals the histologic healing process in
BAG-obliterated frontal sinuses. The healing
process progressed from the connective tissue
phase to bony obliteration with BAG obliteration
maintaining granule remnants. The dissolution of
ions from the amounts of BAG used in clinical
frontal sinus obliteration has been shown to be so
small that BAG seems to be a stable material for
permanent clinical frontal sinus obliteration.29,30
Reliable estimation of the density of the BAG
obliteration can be made with the ROI method.29
The decrease in HU is probably partly attributa-
ble to the replacement of saline and hemoglobin
containing bloody uid with tissue uid without
hemoglobin between the BAG granules at obliter-
ation. In addition, the dissolution of silicon and
phosphorous from BAG granules adds to the
decrease of HU in ROI evaluation. As the healing
process progressed, connective tissue was seen
between the BAG granules and, furthermore, -
brous tissue was replaced by lamellar new bone
formation, which was seen as a slight increase of
HU in ROI analysis. In experimental studies,
10.8 10.5 10.5 12.5 8.2 7.1 5.6
23 20 18 14 9 8 8
12 mo 24 mo 36 mo 48 mo 60 mo 72 mo 84 mo
HEAD & NECKDOI 10.1002/hed September 2006 839
BAG produces more new bone than hydroxyapa-
tite,3234 and the bone produced by BAG is very
similar to natural frontal bone.32 In this clinical
study, the FTIR studies showed bone produced by
BAG to be very similar to natural human frontal
bone. The properties of BAG are important factors
in obliteration material, that is, in chronic
infected frontal sinuses, with a relative risk of
reinfection. The faster healing process and the
occlusion of the sinuses decrease the risk of
relapse.
An ideal material for successful obliteration of
the frontal sinus should have the following prop-
erties.7 It should be available at any time and in
any amount. It should be easy to handle. There
should be no donor site morbidity. It should not
cause a foreign-body reaction or be toxic. Any
transmission of infectious diseases must be
excluded. The material should not have any effect
at follow-up examinations, particularly on CT and
MRI. The obliteration material should be econom-
ical, namely, it should entail no additional cost or
prolong the operation time. BAG fullls the major
part of the above mentioned ideal properties of
frontal sinus obliteration material.
Promising results have been described with
the use of BAG in chronically infected nasal sep-
tum perforation reconstruction.42 The interac-
tions between the bacteria related to chronic fron-
tal sinusitis43 and BAG have not been studied but,
in principle, the experimentally shown antibacte-
rial properties of BAG35,36 can promote the clini-
cal outcome of obliterated sinuses after chronic
infection. Probably the antibacterial properties of
BAG can provide extraordinarily favorable condi-
tions for an uneventful healing process in a
chronically infected environment. This is a new
aspect of frontal sinus obliteration. However, the
antibacterial property of BAG needs more
research, and we need to know more to be able to
draw nal conclusions about its clinical benet.
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