A Novel Technique Combining Platelet Gel, Skin Graft, and
Fibrin Glue for Healing Recalcitrant Lower Extremity Ulcers
TIM MO CHEN, MD, JUI-CHE TSAI, PHD,y
AND
THIERRY BURNOUF, PHDz
BACKGROUND There is no ideal procedure for the treatment of chronic skin ulcers. The use of platelet
gel (PG) in this indication is raising interest.
OBJECTIVE To evaluate the safety and efficacy of a new procedure combining allogeneic single-donor
PG and fibrin glue (FG) to enhance skin graft take for treating recalcitrant ulcers.
MATERIALS & METHODS Fifteen patients with 17 ulcers of various etiologies were enrolled. Skin ulcers
were débrided, and the wounds covered with moist saline dressing. Three to 14 days later, the wound
bed was sprayed with PG, a thin split-thickness skin graft with multiple slits was put on the wound bed,
and FG was sprayed on the skin graft. A short leg polypropylene splint was used to immobilize the skin
graft.
RESULTS Most skin grafts took well. The interval between skin graft and complete wound healing
ranged from 3 weeks to 2 months. No recurrence of ulcers was noted during the 3- to 18-month follow-up
period. No adverse reactions were observed.
CONCLUSIONS The procedure provides advantages in skin grafting for recalcitrant ulcers because PG
functions as a delivery system of powerful mitogenic and chemostatic factors and FG as a hemostatic
tissue sealant that avoids the use of staples or sutures.
The authors have indicated no significant interest with commercial supporters.
P
latelet-rich plasma (PRP) or platelet releasates
have been proposed as surgical adjuncts for the
treatment of wound healing,1–4 including recalcitrant, severe leg ulcers,5–9 while reducing infections
and length of hospital stay.10 In most applications,
PRP is mixed with thrombin before clinical application as a means of generating a platelet gel (PG)
biomaterial that is applied to tissues. The scientific
rationale for the clinical use of PG is that thrombinactivated platelets release numerous growth factors
(GFs) from their a-granules that can modulate cell
proliferation and differentiation and accelerate soft
tissue repair in vivo.6,11 Those include at least seven
locally acting GFs: three isomers of platelet-derived
growth factor (PDGF-AA, PDGF-AB, and PDGFBB), two isomers of transforming growth factor-b
(TGF-b1 and TGF-b2), vascular endothelial growth
factor (VEGF), and epithelial growth factor (EGF).
In an experimental model of laser-induced burns,
autologous PG was also shown to favorably influence wound healing by stimulating an intense
inflammatory process, leading to highly significant
increases in the production of extracellular matrices
and granulation tissue. PG may accelerate vascular
ingrowth, increase fibroblastic proliferation, and
accelerate collagen production. Such a highly
vascularized bed may promote the success of skin
grafting in patients with deep partial-thickness and
full-thickness burns.12 Clinical studies using recombinant human (Rh) PDGF-BB (becaplermin) support
the benefit of GFs in these indications. Rh-PDGF-BB
was licensed more than 10 years ago for the treatment of neurotrophic diabetic ulcers.13,14 Randomized, prospective, multicenter trials demonstrated
that once-daily topical application of Rh-PDGF-BB
at a dose of 100 mg/g, in conjunction with good ulcer
Division of Plastic Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center,
Taipei, Taiwan; yDepartment of Biomedical Engineering, I-SHOU University, Kaohsiung County, Taiwan;
z
Human Protein Process Sciences, Lille, France
& 2010 by the American Society for Dermatologic Surgery, Inc. Published by Wiley Periodicals, Inc. ISSN: 1076-0512 Dermatol Surg 2010;36:453–460 DOI: 10.1111/j.1524-4725.2010.01480.x
453
N O V E L T R E AT M E N T O F R E C A L C I T R A N T L E G U L C E R S
care, could stimulate rapid healing of chronic neurotrophic ulcers of the lower extremity in patients
with diabetes.13 PG and becaplermin appear more
effective than standard care in improving healing
rates in diabetic neuropathic foot ulcers at 20 and 32
weeks, becaplermin being more effective than PG
after 20 weeks of care.15 Topical Rh-PDGF-BB was
also found to be effective in the treatment of nondiabetic and nonpressure-related chronic ulcers.16
Finally, the use of fibrin glue (FG) (also known as
fibrin sealant), obtained by mixing a fibrinogen-rich
fraction with thrombin,17 has also been described
to facilitate the fixation of skin grafts and limit the
risk of infection in burn wounds.18,19
In spite of this progress, chronic wounds often
require skin grafts as the definite procedure for
chronic wound healing. To the best of our knowledge, the use of PG to enhance the take of skin graft
has not been documented. The purpose of this study
was to evaluate the safety and efficacy of using PG
and FG to enhance skin graft take for chronic lower
extremity ulcers.
Materials and Methods
Patients
The Institutional Review Board of Tri-Service
General Hospital, National Defense Medical Center,
Taipei, Taiwan, approved this study (Protocol
096-05-042). Eligible patients were enrolled after
informed consent was obtained. The protocol
conformed to ethical guidelines of the 1975
Declaration of Helsinki.
Preparation of Thrombin, PG, and FG
The Taiwan Blood Service Foundation (Taipei,
Taiwan) prepared human fresh frozen plasma (FFP),
platelet-rich plasma (PRP), and cryoprecipitate units
from blood collected from volunteer non-remunerated donors, following the regulations of the Taiwan
Department of Health. The blood bank of the
Tri-Service Hospital (Taipei, Taiwan) thawed FFP
and cryoprecipitate units at 301C 1 hour before
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D E R M AT O L O G I C S U R G E RY
surgery, which were delivered, together with PRP, to
the surgical suite. Thrombin was prepared as
described before.20 Briefly, 10 mL of FFP and 0.3 mL
of a 10% calcium chloride solution (Taiwan Biotech
Co., Ltd, Taoyuan, Taiwan) were introduced into
a sterile thrombin generation device (TGD-001;
Merries International Inc., Shin Tien, Taiwan). The
device was shaken gently for 30 seconds and then
put aside to let the plasma activation reaction
proceed at room temperature. After approximately
15 minutes, the thrombin-rich supernatant was
drawn aseptically using a sterile 10-mL syringe. PG
was obtained by spraying equal volumes (3 to 8 mL
depending upon the surface of the wound) of PRP
and thrombin using a spray applicator (Merries
International Inc.) and FG by applying equal
volumes (3 to 8 mL depending upon the surface of
the wound) of cryoprecipitate and thrombin using a
dual-syringe system (Merries International Inc.).
Study Design
This clinical study was a prospective pilot trial of
patients with recalcitrant lower extremity ulcers.
Patients were considered as candidates for the study
if they had had recalcitrant ulcers not curable by
traditional healing procedures for at least 3 months.
Fifteen consecutive patients with 17 ulcers met these
criteria and were treated from May 2007 to April
2008. There were five men and 10 women, aged 45
to 80. The characteristics of the patients (sex and
age), medical history, and etiology of skin ulcers are
reported in Table 1. Etiologies were venous insufficiency (7 ulcers), diabetes (4 ulcers), diabetes with
uremia (3 ulcers), trauma (1 ulcer), burn (1 ulcer),
and scleroderma (1 ulcer). The ulcers had a median
size of 54.9 cm2 (range 25–120 cm2). The median
ulcer duration before being enrolled in this study was
14.2 months (range 3 months to 10 years).
The skin ulcers were first débrided to remove
necrotic tissue. The wounds were covered with moist
saline dressing. Daily dressing change without additional treatment was performed. Repeated débridement was necessary in five ulcers (ulcers 1, 2, 3a, 3b,
1
2
3a
3b
4
5
6
7
8
9
10
11
1
2
3
3
4
5
6
7
8
9
10
11
Patient
Ulcer
Number
F
F
M
M
M
F
M
M
F
F
F
F
Sex
62
56
55
52
56
52
45
60
55
55
65
80
Age
Diabetes with
uremia
Venous
insufficiency
Venous
insufficiency
Venous
insufficiency
Trauma
Venous
insufficiency
Scleroderma
Burn
Diabetes
Diabetes
Diabetes
with uremia
Venous
insufficiency
Cause of Ulcer
1 year
9 months
8 months
6 months
1 year
3 months
3 months
2 years
8 months
8 months
1 year
10 years
Duration
of Ulcer
TABLE 1. Review of Patients’ Demographics and Treatment
6 20 cm2,
left lower
leg
5 20 cm2,
right lower
leg
10 6 cm2,
right lower
leg
6 5 cm2, left
lower leg
15 7 cm2,
right lower
leg
5 8 cm2 right
lower leg
10 5 cm2
right lower
leg
10 6 cm2
right lower
leg
12 5 cm2
right lower
leg
5 5 cm2 left
malleolus
14 6 cm2,
left lower
leg
5 8 cm2,
right heel
Size and
Location of
Ulcer
3 weeks
3 weeks
3 weeks
1 month
Complete
Complete
Complete
Complete
Complete
Complete
2 1 cm2
graft loss
Conventional
dressing change
HBO
HBO
Multiple
débridements
Conventional
dressing change
Conventional
dressing change
HBO
3 weeks
3 weeks
3 weeks
3 weeks
Complete
Conventional
dressing change
3 weeks
Complete
Multiple
débridements
1 month
2
months
2 1 cm2
graft loss
Multiple
débridements &
HBO
Multiple
débridements
3 1 cm2
graft loss
1 month
Time to
Healing
2 2 cm2
graft loss
Take of
Skin Graft
Multiple skin grafts
with failure
Prior Ulcer Therapy
15
12
10
3
12
3
9
12
12
12
12
18
Follow-Up
Months
CHEN ET AL
36:4:APRIL 2010
455
12
3 weeks
Complete
12
3 weeks
Complete
10
3 weeks
complete
3 months
4 months
5 months
Results
HBO, hyperbaric oxygen.
65
F
15
15
F
D E R M AT O L O G I C S U R G E RY
14
14
60
Diabetes with
uremia
Venous insufficiency
Venous insufficiency
F
13
13
62
3 months
Diabetes
60
F
12b
12
During the procedure, the wound bed was sprayed
with PG, and a thinsplit-thickness skin graft with
multiple slits was put on the wound bed. Finally, FG
was sprayed on the skin graft; no sutures or staples
were necessary. A short leg polypropylene splint was
used to immobilize the skin graft.
Less than 5% of total skin graft area.
12
3 weeks
Complete
12
3 weeks
Complete
Conventional
dressing change
Conventional
dressing change
Multiple débridements & HBO
Conventional
dressing change
Conventional
dressing change
Diabetes
F
12
12a
60
Cause of Ulcer
Patient
Sex
Age
3 months
5 6 cm2 left
malleolus
5 5 cm2 right
malleolus
5 5 cm2
right heel
10 5 cm2, left
lower leg
5 6 cm2, left
lower leg
Time to
Healing
Prior Ulcer Therapy
Size and
Location of
Ulcer
Duration
of Ulcer
Ulcer
Number
TABLE 1. Continued
456
11) because of residual necrotic tissue. The interval
between the débridement and skin graft ranged from
3 to 14 days.
Take of
Skin Graft
Follow-Up
Months
N O V E L T R E AT M E N T O F R E C A L C I T R A N T L E G U L C E R S
No treatment-associated adverse reactions were observed during the study. Most (13/17) of the skin
grafts took well. Minor areas of skin graft loss,
corresponding to less than 5% of the total skin graft
area, were noted in four ulcers (2 ulcers caused by
diabetes with uremia, 1 by diabetes, and 1 by venous
insufficiency), which healed spontaneously using a
conventional saline dressing. The interval between
skin graft and complete wound healing ranged from
3 weeks to 2 months. No recurrence of ulcers was
noted during the follow-up period, which ranged
from 3 to 18 months. The most relevant cases are
presented below. Patient 1 was an 80-year-old
woman who presented with a chronic venous ulcer
on the left lower leg for 10 years, refractory to
multiple conventional skin grafts. The ulcer measured 14 6 cm2, down to the periosteum of tibia,
with soft tissue necrosis (Figure 1A). Débridement
was performed twice to remove the necrotic tissue.
Ten days after the second débridement, the wound
bed was sprayed with PG (Figure 1B). A thin-splitthickness skin graft was then applied to the wound.
Finally, FG was sprayed on the skin graft (Figure
1C), which took well. A minor area of skin loss
(B2 2 cm2) was noted, which healed spontaneously
using a conventional saline dressing for 3 weeks. The
postoperative course was uneventful, and the patient
has durable wound coverage 18 months after skin
graft (Figure 1D).
Patient 4 was a 65-year-old man who presented with
chronic skin ulcer caused by burn injury for 2 years.
CHEN ET AL
Figure 1. Patient 1. (A) Chronic venous lower leg ulcer for 10 years, refractory to multiple conventional skin grafts. (B) After
repeated débridements, the wound bed was sprayed with platelet glue. (C) Thin-split-thickness skin graft with multiple slits
covering the wound bed; fibrin glue was sprayed on the skin graft. (D) Durable wound coverage 18 months later.
The ulcer measured 10 6 cm2 (Figure 2A). Three
days after adequate débridement, the wound
bed was sprayed with PG (Figure 2B), and a thin-
split-thickness skin graft was applied to the wound.
Finally, FG was sprayed on the skin graft (Figure
2C), which took without any loss. The wound
Figure 2. Patient 4. (A) Chronic lower leg burn ulcer for 2 years. (B) Three days after débridement, the wound bed was
sprayed with platelet glue. (C) Thin-split-thickness skin graft with multiple slits covering the wound bed; fibrin glue was
sprayed on the skin graft. (D) Durable wound coverage 12 months later.
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healed completely 3 weeks after the skin graft. The
postoperative course was uneventful, and the patient
has durable wound coverage 12 months after the
skin graft (Figure 2D).
Discussion
The results of clinical studies using PG to treat
chronic skin ulcers are conflicting. Encouraging
results when treating skin ulcers with autologous or
allogeneic PG have been reported.1–4,8 It was found
that patients with various skin ulcers treated with PG
experienced quicker healing, although in other clinical studies, neither platelet products nor recombinant growth factors appear to have exhibited any
clear adjuvant effect on chronic venous ulcer
healing.21,22 Chronic wound fibroblasts generally
exhibit a poorer mitogenic response to PDGF-AA,
PDGF-BB, basic fibroblast growth factor, TGFb1,
and EGF than normal or acute wound fibroblasts.
High levels of proteases are found in wound fluid
from chronic venous ulcers, impairing the healing
process by degradation of exogenous added growth
factors. The discrepancies reflect not only differences
of technical protocols for preparing PG, but also the
complexity of chronic ulcer healing. It is beyond the
scope of this study to debate whether PG alone is
effective for healing of chronic skin ulcers. From a
clinical point of view, skin grafting is commonly
required as a definite procedure for healing of
chronic skin ulcers.
In this article, we present a new approach developed
specifically for healing recalcitrant leg ulcers. A
combination of three therapeutic components is used
sequentially. First, after careful débridement of the
wound, PG, obtained by mixing PRP with an equal
volume of human thrombin, is applied using a double-syringe device equipped with a spray applicator.
Within 5 to 10 seconds after mixing, the fibrinogen
present in the PRP polymerizes into a fibrin gel,
leading to the formation of a PG that adheres to the
wound. Second, a thin-split-thickness skin graft is
applied to the wound, on top of the PG. Third, FG,
obtained by mixing equal volumes of cryoprecipitate
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D E R M AT O L O G I C S U R G E RY
and human thrombin, is sprayed on the graft. The
blood products were of allogeneic origin because
some patients were too old or not healthy enough to
donate blood and the production of cryoprecipitate
to prepare enough autologous FG would require a
large volume (200 mL) of plasma that is not easy to
process into cryoprecipitate within hospitals. In this
procedure, the mixing of human thrombin and PRP,
a fraction with a 5 times greater platelet concentration than baseline values in whole blood,23 leads to
an activation process that releases multiple GFs from
the platelet a-granules.5 In wound healing, platelets
play an essential physiological role because their agranules are rich with GFs. Although concentrations
of GFs depend upon several factors, such as the
platelet preparation method24,25 and thrombin and
calcium concentration,26 various systems for preparation of PRP result in a considerably greater release
of GFs than levels in whole blood.27 In addition,
blood banks preparing the platelet concentrates used
should adhere to strict specifications in platelet
count, thereby reducing the risk of variability in GF
content. However, we cannot exclude that the
amount of GF released varied somewhat, within a
given range, between the various procedures described in this study. Several studies have shown that
PDGF-AB and TGF-b1 are present in activated
platelet releasates at 100 to 200 ng/mL,28–31 PDGFBB at approximately 10 ng/mL,28 EGF and VEGF at
1 to 5 ng/mL, and TGF-b2 at approximately 0.5 ng/
mL,28 whereas IGF-1, which circulates in plasma, is
found at approximately 100 ng/mL.32 These GFs are
important for re-epithelization and neovascularization by mesenchymal cell recruitment and extracellular matrix synthesis. The PG also induces little
inflammatory reaction between the graft and the
recipient area, resulting in favorable conditions for
graft incorporation. Therefore, we postulate that it
provides a favorable physiological environment for
the success of the grafting procedure. The use of PG
was found to enhance the take of the skin graft after
adequate débridement of the wound. All of the skin
grafts took without major loss, and the patients
achieved durable wound healing in the follow-up
period. Application of the FG, a product already
CHEN ET AL
used for skin grafting and hemostasis,17–19 allowed
more secure and stable placement of the skin
graft, particularly because it could penetrate the
thin-split-thickness skin graft and come into direct
contact with the wound, contributing to the safety of
the procedure. The procedure avoids the use of
staples or sutures, which was of major benefit to
patients because their removal is painful.
Although the clinical effectiveness of this study
derived from a pilot study rather than from randomized controlled trials, the procedure provides
useful advantages in skin grafting to treat recalcitrant ulcers because PG functions as a delivery
system of powerful mitogenic and chemostatic
factors and FG as a hemostatic tissue sealant.
Acknowledgments This study was supported in
part by National Defense Medical Center, Taiwan,
R.O.C. under grant DOD96-21, in part by Children
Burn Foundation, Taiwan, R.O.C., and in part by The
Chen-Han Foundation for Education, Taiwan, R.O.C.
9. Margolis DJ, Kantor J, Santanna J, et al. Effectiveness of platelet
releasate for the treatment of diabetic neuropathic foot ulcers.
Diabetes Care 2001;24:483–8.
10. Valbonesi M, Giannini G, Migliori F, et al. The role of autologous
fibrin-platelet glue in plastic surgery: a preliminary report. Int
J Artif Organs 2002;25:334–8.
11. Bolander ME. Regulation of fracture repair by growth factors.
Proc Soc Exp Biol Med 1992;200:165–70.
12. Henderson JL, Cupp CL, Ross EV, et al. The effects of autologous
platelet gel on wound healing. Ear Nose Throat J 2003;82:598–602.
13. Steed DL. Clinical evaluation of recombinant human platelet-derived
growth factor for the treatment of lower extremity ulcers. Plast
Reconstr Surg 2006;117(7 Suppl):143S–9S; discussion 50S-51S.
14. Smiell JM, Wieman TJ, Steed DL, et al. Efficacy and safety of
becaplermin (recombinant human platelet-derived growth factorBB) in patients with nonhealing, lower extremity diabetic ulcers: a
combined analysis of four randomized studies. Wound Repair
Regen 1999;7:335–46.
15. Kantor J, Margolis DJ. Treatment options for diabetic neuropathic foot ulcers: a cost-effectiveness analysis. Dermatol Surg
2001;27:347–51.
16. Harrison-Balestra C, Eaglstein WH, Falabela AF, Kirsner RS.
Recombinant human platelet-derived growth factor for refractory
nondiabetic ulcers: a retrospective series. Dermatol Surg
2002;28:755–9; discussion 9–60.
17. Radosevich M, Goubran HA, Burnouf T. Fibrin sealant: scientific
rationale, production methods, properties, and current clinical
use. Vox Sang 1997;72:133–43.
18. Vedung S, Hedlung A. Fibrin glue: its use for skin grafting of
contaminated burn wounds in areas difficult to immobilize. J Burn
Care Rehabil 1993;14:356–8.
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Address correspondence and reprint requests to: Thierry
Burnouf, HPPS, Human Protein Process Sciences, 18 rue
Saint-Jacques, 59800 Lille, France, or e-mail: tburnou@
attglobal.net