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29 Osteobiologics
281
process is slow and the resorption of the graft is
increased. On the other hand, corticocancellous
grafts do not have an immediate mechanical benefi t, but due to the large contact area, they are easily integrated and can promote bone remodeling.
One of the main health concerns with allografts is
the transmission of diseases. Mroz reported that
between 1994 and 2007, 96.5 % of musculoskeletal allografts were recalled due to contamination
and recipient infection [ 10 ]. Furthermore, a study
done by Jurgensmeier found frequent inconsistencies in tissue banks, with 39 % accepting samples from elderly donors (≤80 years of age) and
only 50 % of banks excluding grafts from osteoporotic patients [
11 ]. Those discrepancies in graft
collection have a signifi cant impact on the
mechanical properties of the graft and can contribute to fusion failure. However, the use of
allografts in surgeries avoids complications associated with ICBG harvest. Allografts are manufactured in various forms as strips, chips, or
demineralized bone matrix.
29.3.1 Demineralized Bone Matrix
Demineralized bone matrix (DBM) is a human,
demineralized, cell-free allograft bone graft.
During the extraction process, antigenic markers
are removed, making DBM less immunogenic.
The bone type used for DBM production is crucial, as tubular and cortical bones are more osteoinductive than fl at bones [ 12 ]. The demineralized
matrix consists of collagen (93 %), glycoproteins
(3 %), debris, and calcium phosphate. The collagen matrix provides osteoconductivity to DBM;
it is mainly composed of collagen I and a small
fraction of collagen IV and X. Growth factors
contribute to the osteoinductivity of DBM and
include bone sialoprotein, osteopontin, and
TGF-β superfamily [
a central role in cell differentiation toward osteoblasts. However, aging leads to decreased
amounts of BMPs in DBM matrix. Conversely,
tumor growth factor beta (TGF-β) and insulin
growth factor 1 (IGF-1) are not affected by aging
and thus have an important role in bone osteoinduction and interaction with major BMPs [ 14 ].
13 ]. BMP2 and BMP7 play
After bone demineralization, DBM is produced
in powder form. Studies have shown that the particle size of DBM determines its osteoinductive
properties by affecting host interaction and the
release of growth factors. A size range between
420 and 840 μm was found to be the most osteoinductive [
15 ]. DBM is mixed with various carri-
ers at a ratio of 15 % DBM and 85 % carrier for
easier delivery, precise surgical localization, and
containment. The type of the carrier defi nes the
fi nal form of the DBM graft such as chips, putty,
gel-fi lled syringes, and powder. Common carriers
are calcium sulfate, glycerol, gelatin, and hyaluronic acid. DBM graft potentials have been
evaluated in a large number of animal studies and
clinical trials. Morone and co-workers have
found that in a rabbit fusion model, a DBM gel
(Grafton) alone or in combination with ICBG
produced similar fusion rates compared to ICBG
16 ]. Studies have shown that the Grafton
alone [
DBM in form of putty or fl ex led to higher fusion
rates, even achieving 100 % when mixed with a
small percentage of autologous bone. Both putty
and fl ex are fi brous in structure, promote better
osteoconductivity, and are similar to the native
tissue. In our study we found that both the Grafton
putty and the Osteofi l paste led to fusion, whereas
Dynograft did not promote fusion [ 17 ].
Furthermore, Osteofi l induced fusion at earlier
time points (4 weeks) and had the highest overall
fusion rate (Fig. 29.1 ).
In spine orthopedics DBM is commonly used
as bone fi ller or graft extender. Because the DBM
is biodegradable, the scaffold can be used as a
slow-release delivery vehicle for growth factors,
antibiotics, cells (with/without gene modifi cations), and other active components. DBM has
been used as an exogenous delivery system in
numerous studies. In our study DBM was combined with an adenoviral Nel-like molecule 1
(NELL-1), BMP2, or BMP7. NELL-1, one of the
key proteins in osteoblastic differentiation,
caused the formation of a well-defi ned tissue
mass similar to cortical bone and a continuous
connection of newly formed bone and transverse
processes [ 18 ]. We observed signifi cantly higher
fusion rates in the NELL-1 group compared to
other studies that used BMP (Fig.
29.2 ).
282
Z. Buser et al.
Osteofil paste Grafton putty Dynograft
Fig. 29.1 L4–5 posterolateral fusion at 6 weeks in athymic rat using various DBMs: Osteofi l paste, Grafton putty, and
Dynograft (Reproduced from Wang et al. [
Clinical trials for cervical and lumbar fusion
have shown that DBM can act as a bone graft
leading to fusion and that there are no differences
in the complication rates or duration of surgery
when compared to ICBG. For example, Sassard
and co-workers reported similar fusion rates in
patients with autologous bone graft and Grafton
putty vs. autologous graft only, with no signifi cant differences in bone mineralization [
However, DBM’s disadvantage is a large variability due to donor demographics, type of bone,
carrier, amount of growth factors, and the extraction procedure.
17 ] )
phosphate (β-TCP) are mainly used for spine surgeries due to their prolonged rate of resorption,
up to a year for hydroxyapatite and several
months for β-TCP. Furthermore, the structure and
pore size of hydroxyapatite and β-TCP are very
similar to cancellous bone. Once implanted,
β-TCP is populated with a fi brovascular stroma
that is soon replaced with osteogenic cells, leading to bone formation. Several clinical studies
19 ].
have found that both ceramic grafts induced similar fusion rates compared to patients who received
ICBG [ 20 , 21 ]. One of the most commonly used
hydroxyapatites is Pro Osteon Coralline
Hydroxyapatite (Interpore Cross International,
Irvine, CA). It is derived from a sea coral and
29.4 Ceramics
mainly consists of calcium carbonate. Another
graft mixture is Collagraft (NeuColl, Inc., Palo
Ceramics are osteoconductive grafts defi cient in
growth factors and cells. They are easily obtainable in large amounts, are disease-free, and are
with a pore size that is suitable for cell and blood
vessel ingrowth. Hydroxyapatite and β-tricalcium
Alto, CA), consisting of collagen and a mixture
of hydroxyapatite and β-TCP closely resembling
the natural bone structure. Silicate-substituted
calcium phosphate and calcium sulfate have been
used in the recent years as synthetic graft extend-
29 Osteobiologics
283
a
Nell-1
bc
de f
Lac Z
Fig. 29.2 Lumbar X-rays ( a , d ) and micro-CT scans ( b ,
c , e, and f ) of Nell-1 and LacZ (control) 6-week fusion
samples. The red arrows identify the radiopaque tissue
masses on both sides of spine at L4 and L5 segments. The
ers, showing variable fusion rates. The general
disadvantage of ceramic grafts is its brittleness
and inability to sustain heavy loads. Due to the
low mechanical stability, ceramics are usually
combined with fi xation instruments. Because
ceramics lack osteogenic and osteoinductive
properties, they are often combined with materials containing growth factors and cells.
29.5 Bone Morphogenetic Proteins
Bone morphogenetic proteins (BMPs) are part of
the TGF-β superfamily of growth factors involved
in bone and cartilage formation by stimulating
stem cell differentiation. Through their control of
cell proliferation, differentiation, and tissue
architecture, BMPs play an important role in
medial edge ( green arrows ) of each mass displayed the
highest density similar to cortical bone (Reproduced from
Lu et al. [
18 ] )
pathological conditions such as bone ossifi cation
and cancer. Depending on the signaling pathway
and tissue, both down- and upregulation of BMP
can lead to cancer progression. BMPs can be iso-
lated from donor bone or produced from recom-
binant DNA. Because of their powder form,
BMPs require the use of a carrier. The successful
use of BMPs depends on the structural and
mechanical properties of the carrier, which
enable proper delivery and maintenance of the
concentration. Commonly used carriers in spine
fusions are ceramics, absorbable collagen I
sponges (ACS), allografts, and polylactic acid.
Even though ACS is the most commonly used
carrier, it lacks mechanical strength. A study
done by Minamide showed that ACS with BMP2
performed poorly and that the combination of
ceramics and collagen I with BMP2 provided
284
Z. Buser et al.
high fusion rates and tensile strength [ 22 ]. There
is a large body of clinical studies on BMP2 and
BMP7 and their effectiveness in spine fusions. In
2002 BMP2 was approved by the Food and Drug
Administration (FDA) for anterior lumbar interbody fusion (ALIF). Because of high fusion rates
(98 %), BMP2 use was extended to posterior
lumbar interbody fusion (PLIF), transforaminal
lumbar interbody fusion (TLIF), and cervical
fusion. Since then there has been a debate about
the positive effects and complications related to
the “off-label” use of BMP2 [ 23 – 26 ]. In our
study we found that the initial fusion mass was
larger, and the time to solid fusion was shorter in
patients with low pseudarthrosis risk in both
rhBMP2 and ICBG groups [
found higher fusion rates in the rhBMP2 group
compared to ICBG.
BMP7 (OP-1) has been used under a humanitarian device exception for the posterolateral
lumbar approach in patients where an autologous
bone harvest is not possible or when the bone
quality would not lead to fusion. Vaccaro and colleagues found that among 12 patients who
received OP-1, 20 % showed clinical improvement, 50 % had a solid fusion, and no complications were observed [ 28 ]. The use of recombinant
DNA technology for the delivery of BMPs and
stem cell differentiation shows promise. In our
study we used human adipose stem cells expressing BMP2 and BMP7 from a lentiviral vector.
The cells were loaded onto the collagen carrier
and placed at the decorticated L4–5 transverse
processes. Animals that received cells with
BMP2, BMP7, or BMP2+BMP7 had a solid
fusion by 8 weeks [ 29 ]. We found that the group
expressing both BMP2 and BMP7 had a signifi cantly greater area of bone formation compared
to stem cells expressing BMP2 or BMP7 alone
29.3 ).
(Fig.
27 ]. Furthermore, we
The main disadvantages are harvest site morbidity, naturally low numbers of stem cells, and
donor quality. The bone marrow of young,
healthy patients contains one mesenchymal stem
cell (MSC) on every 50,000 nucleated cells, and
those numbers decrease with age. In addition,
aspiration of more than 2 cc of bone marrow per
site will lead to a reduction of stem cell numbers.
Once aspirated, BMA can be processed for stem
cell isolation, and the cells can be expanded
in vitro for several passages without losing their
differentiation potential. Several animal studies
have confi rmed the benefi ts of expanded MSCs
during spine fusion, which in some cases was
superior to whole bone marrow [
spective cohort study, we found differences in
single- and multilevel fusion rates when BMP2,
BMA, or autograft was used [ 31 ]. BMA led to
the same fusion rates for single level (100 %), but
was inferior for multilevel fusions when compared to BMP2 and autograft (63 % vs. 100 %,
respectively). This leads to the conclusion that
BMA is suitable for single-level procedures and
is cost advantageous compared to BMPs. Even
though MSCs can provide a great alternative to
autologous bone, there are several logistical
issues with their use in a clinical setting, such as
in vitro expansion, potential contamination, and
revision surgery for implantation.
30 ]. In a retro-
29.7 Platelet Gels
Platelet gels contain platelets, platelet-derived
growth factor (PDGF), and transforming growth
factor (TGF-β) and can be combined with an
auto- or allograft. Even though animal studies
presented encouraging data, several clinical
studies have found that platelet gels led to lower
fusion and higher nonunion rates.
29.6 Bone Marrow Aspirate (BMA)
Bone marrow aspirate has osteoinductive and
osteogenic properties. Since it lacks mechanical
stability, BMA is always combined with a carrier,
usually collagen I sponges or DBM (Fig. 29.4 ).
29.8 Summary
The risk and benefi t profi le of any technique used
to deliver an interbody placement is unique. The
lateral transpsoas approach has evolved to allow
surgeons to avoid potential complications
29 Osteobiologics
285
Fig. 29.3 Radiographs of L4–5 fusion. ( a ) Cells only, ( b ) cells with GFP, ( c ) cells expressing BMP2, ( d ) cells express-
ing BMP7, and ( e ) cells expressing BMP2/BMP7 (Reproduced from Kaito et al. [
associated with the traditional fusion. Several
grafting materials have been widely used and
represent viable ICBG substitutes. However, one
must be cautious when choosing the graft material and keep in mind that most of the grafts do
not require FDA approval and therefore lack preclinical studies. Further research in bone biology
will improve the engineering of scaffolds to provide a mechanically stable, porous matrix, which
enhances cell proliferation.
29 ] )
286
Z. Buser et al.
BMA – collagen sponge
Collagen sponge
Fig. 29.4 Bone marrow aspirate graft
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Indirect Decompression
Yu-Po Lee and Vinko Zlomislic
3 0
30.1 Lumbar Stenosis
Lumbar spinal stenosis (LSS) is the most common indication for lumbar spinal surgery in the
elderly population [ 1 – 4 ]. A combination of disc
protrusion, facet joint hypertrophy, and buckling
of the ligamentum fl avum contributes to narrowing of the spinal canal and the neuroforamen
[ 1 – 4 ]. Symptoms include loss of sensation,
weakness, and pain, which may radiate down the
leg to the feet [ 1 – 4 ]. Additional symptoms in the
legs may be fatigue, heaviness, paresthesias, as
well as bowel or bladder symptoms [ 1 – 4 ].
Symptoms are most commonly bilateral and
symmetric, but they may be unilateral. Patients
may also complain of back pain [ 5 ]. Back pain
may be secondary to disc degeneration or facet
arthropathy. However, compression of the sinuvertebral nerve may result in back pain [ 6 ].
Symptoms typically worsen with standing or
walking and improve with sitting. These symptoms have been referred to as pseudoclaudication
in the past due to the similarities in these symptoms to vascular claudication. Now, this constellation of symptoms is often referred to as
Y.-P. Lee , MD (*) • V. Zlomislic , MD
Department of Orthopaedic Surgery , University
of California , 200 West Arbor Drive , San Diego , CA
92103-8894 , USA
yupo90025@yahoo.com
e-mail:
neurogenic claudication [ 1 – 4 ]. Symptoms are
typically exacerbated with standing or walking
because the spine is extended during these activities. Extension of the spine causes further narrowing of the spinal canal and greater compression
on the nerve roots [ 1 – 4 ]. This is due to buckling
of the ligamentum fl avum and narrowing of the
neuroforamen. Patients often report improvement
of their symptoms with fl exion of their spine or
sitting. Flexion increases the canal diameter via
ligamentotaxis of the ligamentum fl avum, and
this relieves pressure on the nerve roots [ 1 – 4 ].
Patients may report that they can walk further
while leaning forward on a shopping cart. They
may also report that they can walk more easily
uphill or that riding a bicycle is their preferred
form of exercise because they are able to lean forward. This helps to distinguish neurogenic claudication from vascular claudication because
walking uphill or riding a bicycle results in pain
from ischemia when the patient has vascular
claudication.
When nonoperative pain management fails to
alleviate symptomatic low back pain, surgical
intervention may be considered. Procedures such
as laminotomy or laminectomy and facetectomy
may be considered in those patients who have
failed attempts at nonoperative care. Surgery in
these cases has been shown to be very successful.
In a study by Atlas et al., 148 patients with lumbar spinal stenosis were followed prospective for
10 years [
7 ]. They found that low back pain
© Springer International Publishing Switzerland 2017
M.Y. Wang et al. (eds.), Lateral Access Minimally Invasive Spine Surgery,
DOI 10.1007/978-3-319-28320-3_30
289
290
Y.-P. Lee and V. Zlomislic
relief, predominant symptom improvement, and
satisfaction were similar in patients initially
treated surgically or nonsurgically. However, leg
pain relief and greater back-related functional
status continued to favor those initially receiving
surgical treatment. In another study by Weinstein
et al., the authors followed 654 patients in a randomized clinical trial comparing operative versus
nonoperative care for patients with lumbar stenosis [ 8 ]. Patients with symptomatic spinal stenosis
treated surgically compared to those treated nonoperatively maintain substantially greater
improvement in pain and function through
4 years. Hence, surgical intervention is appropriate and benefi cial in patients with lumbar spinal
stenosis who have failed attempts at conservative
care.
However, complications may occur during
lumbar laminectomy. Nerve root injury, postoperative radiculitis, and incidental durotomies are
just a few of the complications associate with
direct lumbar decompression [
complications have also been noted with minimally invasive decompressions [ 12 , 13 ].
9 – 11 ]. Similar
30.2 Lateral Interbody Fusion
Minimally invasive spine surgery has gained
increasing popularity over the past few years.
Advantages of minimally invasive spine surgery
include less tissue trauma during the surgical
approach, less postoperative pain, improved cosmesis, shortened recovery time, and quicker
return to normal daily living for the patient compared to traditional open approaches of lumbar
interbody fusion [
fusion (LIF) accesses the spine via a more lateral
position through the retroperitoneal fat and psoas
muscle. This allows for a less invasive access to
the spine while still affording direct visualization
of the disc. This procedure allows the surgeon to
correct coronal plane deformity and to restore the
disc height. Also, this technique has the ability to
correct spondylolithesis as well. The process of
correcting these deformities often will indirectly
decompress the central canal, the lateral recess,
and neuroforamen [ 18 – 23 ].
14 – 17 ]. Lateral interbody
The interbody cage provides an indirect
decompression by restoring disc height, which
reduces spinal deformities through ligamentotaxis since the anterior and posterior ligamentous
structures are left intact. Reduction of the spinal
deformities has been shown to increase the
foraminal and central canal area (Figs. 30.1 , 30.2 ,
and 30.3 ) [ 18 – 23 ]. Both the indirect decompres-
sion and percutaneous pedicle screws are
accepted minimally invasive surgical (MIS) techniques that require little soft tissue dissection and
minimal blood loss.
30.3 Evidence for Indirect
Decompression
The earliest evidence for indirect decompression
came from the development of interspinous
spacers. Interspinous spacers were developed to
treat lumbar spinal stenosis. Distraction of the
intervertebral segment stretches the ligamentum
fl avum and increases the central canal. Also, distraction of the disc space increases the diameter
of the neuroforamen. This effectively relieves
pressure on the traversing and exiting nerve roots
to relieve patients of their neurogenic claudication and radiculopathy symptoms. In 2004,
Zuckerman et al. published the results of their
prospective study on the X-STOP [ 24 ]. They
randomized 191 patients in a prospective study
comparing the X-STOP versus nonoperative
care. At 6 months, the success rates were 52 and
9 %, respectively, and at 1 year, 59 and 12 %. The
authors determined that the X-STOP was a signifi cant improvement over nonoperative therapies at 1 year with a success rate comparable to
published reports for decompressive laminectomy, but with considerably lower morbidity. In
another study by Siddiqui et al., MRI studies
were performed on patients before and after sur-
25 ]. Signifi cant increase in the dimensions
gery [
of the neural foramen and canal area were demonstrated after surgery. The problem with the
interspinous spacers is they would erode through
the spinous processes over time, and patients
would have recurrent symptoms as the distraction was lost [ 26 , 27 ]. Hence, interspinous spac-
30 Indirect Decompression
a
b
291
cd
Fig. 30.1 ( a ) Preoperative sagittal MRI showing L4–5
spondylolisthesis with stenosis at L3–4, L4–5. ( b )
Preoperative axial MRI of L3–4 level. Note the lateral
recess and foraminal stenosis on the left side. ( c )
ers demonstrated the ability to decompress the
spinal canal via indirect decompression, but the
concern was that the effect may not be long
lasting.
Preoperative axial MRI of L4–5 level. Note the central
and lateral recess and foraminal stenosis bilaterally. ( d )
Preoperative parasagittal view of the neuroforamen
With lateral interbody fusion, indirect decompression would be achieved by placement of the
interbody spacer, and the benefi t would be
maintained via the pedicle screws and ultimately