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Effect of Platelet-Rich Plasma on

Bone Growth and Osseointegration
in Human Maxillary Sinus Grafts:
Three Bilateral Case Reports

Stuart J. Froum, DDS* The subantral augmentation (sinus

Stephen S. Wallace, DDS** elevation) procedure has been
Dennis P. Tarnow, DDS*** shown to be a predictable method
Sang-Choon Cho, DDS**** for increasing maxillary posterior
bone volume for the successful
placement of load-bearing root-form
implants.1 Initial sinus elevation tech-
Platelet-rich plasma is an autologous product that is derived from whole blood
niques relied on grafts that consisted
through the process of gradient density centrifugation. The proposed value of this
product in dental implantology and in bone augmentation procedures lies in the of 100% autogenous bone har-
ability to incorporate high concentrations of the growth factors PDGF, TGF-
1, vested from either oral (ramus, chin)
TGF-
2, and IGF, as well as fibrin, into the graft mixture. Research has shown an or extraoral (iliac crest) donor sites.2–7
increased bone maturation rate and improved bone density when this product, or It has subsequently been found that
its recombinant growth factors, is added to small bony defects or to larger defects the autogenous bone graft can be
that use autogenous bone as the grafting material. This study tested the efficacy replaced, in whole or in part, by a
of platelet-rich plasma in three bilateral sinus graft cases with grafts of anorganic variety of allografts, xenografts, allo-
bovine bone that contained minimal or no autogenous bone. Histomorphometric plasts, and bone morphogenetic
analysis indicated that the addition of platelet-rich plasma to the grafts did not proteins with a highly predictable
make a significant difference either in vital bone production or in interfacial bone
graft and implant survival rate.8–20
contact on the test implants. (Int J Periodontics Restorative Dent 2002;22:45–53.)
In fact, the addition of autogenous
bone to a composite graft may result
in a higher vital bone percentage at
an earlier time, allowing for earlier
****Clinical Professor, Department of Surgical Services (Periodontics) and implant placement and subsequent
Department of Implant Dentistry, New York University College of Dentistry. loading.20,21
****Associate Clinical Professor, Ashman Department of Implant Dentistry,
The sequence of treatment for
New York University College of Dentistry.
****Professor and Chair, Ashman Department of Implant Dentistry, New York delayed implant placement with a
University College of Dentistry. composite or nonautogenous graft
****Clinical Instructor, Ashman Department of Implant Dentistry, New York begins with a graft maturation
University College of Dentistry.
period of 6 to 12 months. This inter-
****Reprint requests: Dr Stuart Froum, 17 West 54th Street, Suite 1 C/D, val is determined by the clinician
New York, New York 10019. and is based on such factors as

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height of remaining crestal bone, risk of disease transmission associ- the study was explained to each
quality of the remaining crestal ated with use of this technology. patient, and each signed an in-
bone, percentage of autogenous The proposed value of PRP in bone formed consent form that was
bone in the composite graft, and grafting lies in the ability to incor- approved by both the University
surface texture of the implant(s) porate high concentrations of the Committee on Activities Involving
being placed. As early loading pro- growth factors PDGF, TGF-
1, TGF- Human Subjects and the New York
tocols generally do not apply to
2, and IGF, as well as fibrin, into State Department of Health Blood
grafted bone, an osseointegration the graft mixture. Resources Program.
period of approximately 6 months is Marx et al22 used this technol- On the day of surgery, a flip of a
allowed prior to second-stage ogy in treating large mandibular coin determined the experimental
surgery (if applicable) and loading. continuity defects. The increased side (PRP) and the control side (non-
Consequently, with staged implant bone maturation rate and bone den- PRP). All six sinuses in this pilot study
placement, the patient must wait sity in these defects warranted a con- were grafted with anorganic bovine
between 12 and 18 months to trolled clinical, histologic, and histo- bone (0.25 to 1 mm cancellous
receive the implant restoration. morphometric study to evaluate the BioOss, Osteohealth). All sinus grafts
Grafts of 100% autogenous bone healing response in sinus augmen- were performed with a lateral win-
may require only 4 to 6 months for tation surgery using autologous dow approach, modified from the
maturation, reducing the waiting platelet gel (thrombin-activated PRP) technique presented by Wood and
period to 10 to 12 months. with composite grafts containing Moore.4 The step-by-step surgical
The incorporation of platelet- minimal or no autogenous bone. technique and histomorphometric
rich plasma (PRP) activated with evaluation protocols have been
bovine thrombin (autologous described in a previous article.20 PRP
platelet gel) in a sinus graft has been Method and materials was obtained from a blood draw of
proposed as a method of creating 350 to 450 mL processed with a
dense, vital bone in a shorter inter- Three patients were selected from Sequestra 1000 gradient density cell
val. If effective, this could reduce those who presented for maxillary separator (Medtronics). This yielded
the interval from composite grafting posterior implant therapy at the New approximately 30 mL of PRP for clin-
to implant loading to one resem- York University Department of ical use. The remaining blood frac-
bling that applicable to 100% auto- Implant Dentistry. All were diag- tion was autotransfused through the
genous bone grafting (10 to 12 nosed as requiring bilateral sinus closed system to minimize blood
months). augmentation procedures prior to volume loss. The BioOss graft mate-
PRP is derived from whole the placement of the implants. All rial was hydrated with the PRP
blood by sequestering and con- patients were advised of alternative (experimental side only) in a dap-
centrating the platelets via gradient treatment plans and selected the pen dish. Bovine thrombin was
density centrifugation. Improved plan requiring maxillary sinus eleva- added just prior to placement of the
technology has allowed the blood tion. All patients with absolute con- graft, resulting in the formation of an
draw required for production of the traindications for this procedure, autologous platelet gel containing
final product to be reduced from such as uncontrolled diabetes, long- the particulate graft material.
450 mL to a much more manage- term steroid usage, and blood dis- Membranes were placed over all six
able 50 mL. This negates the need orders, were excluded. All patients lateral windows, as this has been
for autotransfusion of the unused were informed of the requirements shown to result in improved vital
fraction to maintain patient fluid for participation in the study, and all bone counts.23
volume. As the growth factor had the option of withdrawing from In case 3, miniature test implants
source is autologous, there is no the study at any time. The nature of of 2.0 mm in diameter and 10 mm in

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Fig 1 (left) Panoramic view of test

implants in place in grafted sinuses in case
3. Test sinus is on right, control is on left.

Fig 2 (below) Clinical view of test (PRP)

sinus graft completed and test implants in
place in case 3.

length (3i/Implant Innovations) were percentage connective tissue, per- Case 2

placed through the crestal bone into centage residual graft material, and
the sinus grafts. Figures 1 and 2 percentage of bone at the implant- The patient was a 35-year-old
show the test implants in place in bone interface. woman who was a light smoker
case 3. Placement of the permanent (three to five cigarettes per day) with
implants was performed at 7 an unremarkable medical history.
months, 7.5 months, and 11 months, Case 1 Bilateral sinus grafts were placed
respectively, for cases 1, 2, and 3. At using 95%+ BioOss and < 5% auto-
the time of implant placement, The patient was a 43-year-old non- genous bone harvested from the
trephine cores of 3 mm in diameter smoking woman with an unremark- tuberosity. PRP activated with bovine
and 10 mm in length were harvested able medical history. Bilateral sinus thrombin was added to the graft
through the site of the former lateral grafts were placed using 100% material for the left sinus prior to
window. The three test implants BioOss. PRP activated with bovine graft placement. BioGide mem-
were removed with a special guide thrombin was used to hydrate the branes were placed over both lateral
and trephine at the same time. The graft on the experimental side prior windows and stabilized in position
cores were fixed and sent to the to graft placement. A bioabsorbable with titanium tacks. Cores were
Hard Tissue Research Laboratory at BioGide membrane (Osteohealth) taken at the time of implant place-
the University of Oklahoma College was placed over both lateral win- ment, which occurred 7.5 months
of Dentistry for blinded histologic dows and stabilized in position with after sinus grafting.
and histomorphometric evaluation. titanium tacks. Cores were taken at
The test implants were evaluated the time of implant placement,
for total volume of calcified which occurred 7 months after sinus
material, percentage of vital bone, grafting.

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Case 3 Figures 5 and 6 depict representative components as an adjunct to intra-

histologic samples of the implant- oral bone grafting, implant place-
The patient was a 69-year-old non- bone interface of the test implants. ment, and/or grafting of the maxil-
smoking man with a history of hyper- lary sinus.
tension. Bilateral sinus grafts were Lynch et al27 reported on the
placed using 100% BioOss. PRP acti- Discussion effects of combined recombinant
vated with bovine thrombin was PDGF-IGF on bone formation
added to the graft material for the There has been some confusion in around roughened titanium implants
right sinus prior to graft placement. the literature regarding the nomen- in the dog model. Direct application
Nonabsorbable expanded polyte- clature of the blood product to the implants stimulated the regen-
trafluoroethylene (e-PTFE) mem- described in this article. It has been eration of bone in periimplant sites
branes (Gore-Tex Augmentation referred to as PRP, platelet concen- in the early phase of healing. Both
Material oval-9, 3i/WL Gore) were trate, and autologous platelet gel. the implant-bone contact and fill of
trimmed and placed over both lateral The definition of these blood prod- the periimplant spaces were
windows and stabilized with titanium ucts or fractions can be found in the improved. An immediate extrac-
tacks. Two test implants were placed technical manual of the American tion–implant placement dog study28
in the right (test) and one in the left Association of Blood Banks.24 These observed a twofold increase in
(control) sinus at the time of sinus definitions may not be applicable to implant-bone contact and in areas of
grafting. The sites chosen for these the technique that we are clinically bone adjacent to the implant sur-
implants were determined to be describing, as the plasma volume in face when using a recombinant
future final implant positions by use which the sequestered platelets are PDGF and IGF-I gel beneath an e-
of computed tomographic scanning ultimately suspended is left to the PTFE membrane. Tayapongsak et
and SimPlant (Columbia Scientific) discretion of the clinician. The al29 showed a 50% decrease in time
analysis with radiographic and surgi- authors have opted for the use of the for remodeling and graft incorpora-
cal templates. Cores were taken from term PRP in this article, as it is the tion with the addition of autologous
the lateral window area and the test nomenclature most often encoun- fibrin adhesive to particulate can-
implants were removed with sur- tered in the literature. In the litera- cellous bone and marrow grafts in
rounding bone cores at the time of ture review, however, we have left major mandibular reconstruction
implant placement, which occurred the original authors’ nomenclature surgery.
11 months after sinus grafting. unchanged. Marx et al 22 reported on a
Numerous references in the group of 88 cancellous cellular mar-
periodontal literature relate to the row bone graft reconstructions of 5
Results effectiveness and mode of action of cm or greater mandibular continuity
PDGF, TGF-
, IGF, and fibrin in peri- defects; 44 received grafts with PRP
Table 1 presents the vital bone con- odontal regeneration. These are added, with 44 additional cases
tent of the three bilateral sinus grafts. readily available and are beyond the serving as a control. The grafts with
The two test implants placed in the scope of this article. Ross et al25 and PRP added showed a radiographic
PRP sinus had slightly higher per- Westermark26 have published com- maturation rate that was 1.62 to
centages of implant-bone contact prehensive reviews of the biology of 2.16 times that of the grafts without
(37.6% and 38.8%) than the test PDGF. A limited number of refer- PRP. Histomorphometry demon-
implants placed in the contralateral ences, however, are found in the strated a greater bone density in
non-PRP sinus (33.8%). Figures 3 and dental literature relating to the use of the PRP-added sites (74.0% ± 11%)
4 show representative histologic PRP, platelet concentrate, autolo- than in the sites where PRP was not
samples of bone cores from case 3. gous platelet gel, or its recombinant added (55.1% ± 8%). Additionally,

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Table 1 Histomorphometric analysis of vital bone in grafted

sinuses
Time % vital bone % vital bone
Case (mo) Graft PRP (test) non-PRP (control)
1 7 100% BioOss 15 13
2 7.5 95%+ BioOss 21 19
< 5% autogenous bone
3 11 100% BioOss 34 32
Mean 23.3 21.3

Fig 3 (left) Non-demineralized section

from test (PRP) bone core (Stevenel’s
blue–van Gieson’s picric fuchsin stain; orig-
inal magnification  25).

Fig 4 (right) Non-demineralized section

from control (non-PRP) bone core
(Stevenel’s blue–van Gieson’s picric fuchsin
stain; original magnification  25).

Fig 5 (left) Test implant from control

(non-PRP) sinus from case 3. The superior
portion of the implant is in crestal bone.
The apical portion is in the sinus graft
(Stevenel’s blue–van Gieson’s picric fuchsin
stain; original magnification  2).

Fig 6 (right) Test implant from the test

(PRP) sinus from case 3, which demonstrat-
ed an overall 38.8% bone contact at the
interface (Stevenel’s blue–van Gieson’s picric
fuchsin stain; original magnification  10).

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the harvested cancellous marrow abdomini muscles of athymic nude The sinus model may be con-
was shown to have receptor sites rats. More specifically related to the sidered to be a relatively large-
for PDGF and TGF-
. These were present article, Terheyden33 com- volume graft. Uchida et al36 showed
predominantly centered around pared rhOP-1 and PRP in bilateral that a sinus graft for multiple 15-mm
blood vessels (endosteal osteoblasts) sinus grafts that used 100% anor- implants is likely to require 5.5 mL of
but were also found in lesser num- ganic bovine bone as a grafting graft material. When using a bone
bers in the marrow (marrow stem material. The PRP was not effective graft substitute that contains neither
cells and osteoprogenitor cells). in producing bone regeneration, vital cells nor bone morphogenetic
Anitua30 used PRP in the prepa- whereas in the contralateral sinus proteins, bone formation must orig-
ration of future implant sites. Extrac- the rhOP-1 was effective. inate from the bony walls (endosteal
tion sockets in 20 patients were The literature appears to indi- osteoblasts and circulating stem
either treated with PRP or left un- cate that PRP may be effective in the cells). This healing pattern was pro-
treated as controls. The sockets with relatively small periodontal defect posed by Boyne and James2 and
PRP added exhibited greater buc- and in larger bone defects when later demonstrated in monkeys37
colingual/palatal bone width, they are grafted with autologous and humans.8
greater bone density, and faster soft bone. When autologous bone is not The most effective way to eval-
tissue coverage than the controls. present in the graft, and the graft is uate the effects of PRP on the for-
Kassolis et al31 recently pub- of large volume, PRP may not pro- mation of bone in a sinus graft is to
lished the results from 14 sinus grafts duce the desired stimulatory study the effect in bilateral sinus
and three maxillary ridge augmen- response because vital bone cells grafts, with the addition of PRP
tations using PRP with freeze-dried are needed for this stimulation to being the only controlled variable.
bone allografts (LifeNet). The grafts occur. This is the first study to be per-
were mixed at a ratio of 0.5 g:2 mL Several authors 22,34–35 (and formed in this manner. We chose to
PRP prior to insertion into the sinus. Russo and Garg, unpublished data) use a nonvital bone substitute as a
The grafts were then covered with a have explained the mode of action graft material for two reasons. First,
PRP “membrane.” Histologic sec- of platelet growth factors. In review, reports using autogenous bone in
tions revealed numerous areas of platelet degranulation and release the nonsinus model have shown PRP
osteoid and bone formation around of growth factors occurs within 3 to to have a positive effect on bone
the freeze-dried bone allograft par- 5 days, and the growth factor activ- formation. Second, we felt it impor-
ticles, with no evidence of inflam- ity may end in as soon as 7 to 10 tant to determine if PRP would have
matory cell infiltrate. Histomorpho- days. The PDGF that is released dur- a similar positive effect on a nonin-
metry was not performed, and there ing degranulation is chemotactic for ductive, nonvital graft material.
were no controls; therefore, quanti- macrophages, which then make The above-outlined wound-
tative measurements could not be their own contribution to the healing mechanisms, coupled with
made. wound-healing cascade. The com- the relatively large graft size, could
While the reports using auto- bined roles of PDGF, TGF-
, and explain the minimal difference in vital
genous bone with PRP are promis- IGF are chemotaxis and mitogene- bone between test and control
ing, other reports indicate that PRP sis of stem cells and osteoblasts, sinuses in our study. With the excep-
may not be effective when used angiogenesis for capillary ingrowth, tion of case 2, which had minimal
with bone substitutes. Wironen et bone matrix formation, and colla- autogenous bone in the graft, there
al32 have shown that PRP is not gen synthesis. Fibrin maintains the were no cells (endosteal osteoblasts
osteoinductive when added to regenerative space and provides a or stem cells) present in the body of
demineralized bone matrix placed matrix for cell migration and prolif- the graft. Endothelial migration
in pouches created in the recti eration. (revascularization) and migration of

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cells from the bony sinus walls is Aside from any effect that PRP vary from three to eight times the
unlikely to happen in an interval that might have on wound healing, the platelet concentration in the
would render the released growth handling properties of the particu- patient’s blood. Additionally, the
factors effective (7 to 10 days). late graft material were dramatically operator may alter the final concen-
Therefore, the stimulating effect of improved by the addition of the tration by increasing or decreasing
these growth factors may only occur thrombin-activated PRP. The resul- the volume into which the platelet
close to the bony walls. Each of the tant fibrin formation consolidated button is suspended. It then
three cases in this pilot study showed the graft, allowing it to be cut into becomes obvious that the final
only a 2% increase in vital bone on conveniently sized blocks that could platelet concentration will depend
the test (PRP) side, which is not clin- be easily carried to and inserted into upon three factors: (1) the total num-
ically or statistically significant. It the lateral window. These soft blocks ber of platelets in the original sam-
would appear that the differences in could then be moved to any desired ple; (2) the recovery rate of the sys-
vital bone formation between the location, such as the narrow and tem used; and (3) the final volume of
three cases relate to maturation time often hard-to-reach anterior region, plasma into which the platelets are
of the graft and not to any effect of where they could be molded into suspended. For purposes of factor-
the PRP. The effect of time on the for- position. Additionally, graft place- ing in the actual platelet concentra-
mation of vital bone in sinus grafts ment can be accomplished without tion used in our future cases, we pro-
was demonstrated in prior articles the inadvertent spillage of graft pose to obtain platelet counts from
from the authors’ sinus graft material into the buccal flap area. the initial blood sample and also
study.20,38 Tayapongsak et al29 reported similar from the harvested PRP. A standard-
Our findings of similar vital bone handling qualities when adding ized technique should be devised
formation in the test (PRP) and con- autologous fibrin adhesive activated that includes dilution of the concen-
trol (non-PRP) sinuses are paralleled with bovine thrombin to cancellous trated platelets, resuspension, and
by the results seen in the cores con- bone and marrow grafts. multiple sampling to ensure an accu-
taining the test implants that were Marx et al22 showed a mean rate platelet count.
placed bilaterally in case 3. The two increase in platelet concentration of
test implants placed in the PRP sinus 338% using an Electro Medics 500
had slightly higher percentages of (Medtronics) gradient density cell
implant-bone contact (37.6% and separator with a 400- to 450-mL
38.8%) than the test implant placed whole blood sample. Other cen-
in the contralateral non-PRP sinus trifuge units, which require a whole
(33.8%). Considering that the native blood sample approximating 50 mL,
crestal bone above both sinuses was are the Platelet Concentrate
approximately 5 mm, the above val- Collection System (3i/Implant
ues represent an accurate reflection Innovations) and the SmartPReP
of the healing response of the graft (Harvest Technologies). Both of the
materials. As all three test implants above small-draw units report higher
were well-integrated, it seems that platelet concentrations than the
the difference in implant-bone con- large-draw Medtronics unit.
tact was not significant to implant It is of interest to note that the
success. Of course, these values manufacturers of platelet sequestra-
should be viewed in light of the 11- tion and concentration systems give
month implant and graft healing varying values for the final platelet
period. concentration achieved. This may

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Conclusions References 11. Misch CE, Dietsh F. Bone grafting mate-

rials in implant dentistry. Implant Dent
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1. Academy of Osseointegration. Sinus
The following conclusions may be
Graft Consensus Conference, Wellesley, 12. Small SA, Zinner ID, Panno FV. Augment-
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20. Froum SJ, Tarnow DP, Wallace SS, Cho S- 28. Becker W, Lynch SE, Lekholm U, et al. A 36. Uchida Y, Goto M, Katsuki T, Soejima Y.
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Volume 22, Number 1, 2002