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Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.elsevier.com/locate/burns

Review

Evolution of skin grafting for treatment of burns:

Reverdin pinch grafting to Tanner mesh grafting
and beyond

Mansher Singh a,b, * , Kristo Nuutila b, K.C. Collins a , Anne Huang b

a
Department of Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States
b
Division of Plastic Surgery, Department of Surgery, Brigham & Women’s Hospital, Harvard Medical School, Boston,
MA, United States

article info abstract

Article history: Background: Skin grafting is the current standard care in the treatment of full thickness
Accepted 7 January 2017 burns. It was first described around 1500 BC but the vast majority of advancements have
Available online xxx been achieved over the past 200 years.
Methods: An extensive literature review was conducted on Pubmed, Medline and Google
Scholar researching the evolution of skin grafting techniques. The authors concentrated on
Keywords:
the major landmarks of skin grafting and also provide an overview of ongoing research
Skin grafting
efforts in this field.
History
Results: The major innovations of skin grafting include Reverdin pinch grafting, Ollier
Evolution
grafting, Thiersch grafting, Wolfe grafting, Padgett dermatome and modifications, Meek-
Future direction
wall microdermatome and Tanner mesh grafting. A brief description of the usage,
advantages and limitations of each technique is included in the manuscript.
Conclusions: Skin grafting technique have evolved significantly over past 200 years from
Reverdin pinch grafting to modern day meshed skin grafts using powered dermatome.
Increasing the expansion ratio and improving the cosmetic and functional outcome are the
1
main focus of ongoing skin grafting research and emerging techniques (such as Integra ,
1 1
Recell , Xpansion ) are showing promise.
© 2017 Elsevier Ltd and ISBI. All rights reserved.

Skin grafting was first described thousands of years ago, but the
1. Introduction
vast majority of advancements have been achieved over the past
200 years. This review highlights the evolution of skin grafting
Skin grafting is the standard treatment for full thickness skin from Reverdin pinch grafting to modern day skin grafting and
loss, generally encountered in patients with severe burns [1]. also features ongoing research efforts in this ever evolving field.

* Corresponding author at: Department of Surgery, Beth Israel Deaconess Medical Center, Boston, MA 02215, United States.
Fax: +1 617 732 6387.
E-mail address: msingh6@bidmc.harvard.edu (M. Singh).
http://dx.doi.org/10.1016/j.burns.2017.01.015
0305-4179/© 2017 Elsevier Ltd and ISBI. All rights reserved.

Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015
JBUR 5164 No. of Pages 6
2 burns xxx (2017) xxx –xxx
2. Methodology
Keys words used for this manuscript included “skin grafting”,
“history” and “evolution”. A PubMed search for “history” and
“skin-grafting” yielded 130 articles and a PubMed search for
“evolution” and “skin grafting” generated 26 articles. Another
28 articles were found using Google Scholar and Medline. A
combined total of 184 articles were reviewed independently by
two co-authors (MS, KN). The articles deemed as ‘landmarks in
skin grafting’ by both the authors were included for further
review in this manuscript.
3. Historical background
The earliest known mention of skin grafting is in the Ebers
Papyrus, an ancient Egyptian medical papyrus dating to
1500 BC [2]. It became highly developed in India, where
pedicled flaps from the cheek or forehead and grafts contain-
ing skin and subcutaneous fat from the buttocks were used to
reconstruct noses and lips [3–5]. This knowledge was docu-
mented by Sushruta in the Sushruta Samhita, one of the
foundational texts of Ayurveda, a system of medicine with
historical roots in the Indian subcontinent, dating back to the
6th century BC [2]. Eventually, this technique traveled to
Europe and was adopted by the ancient Romans and Greeks. In
the 1st century AD, a Roman encyclopaedist named Aulus
Cornelius Celsus documented various plastic surgery oper-
ations in De Medicina, one of the oldest medical treatises in
Western civilization. One of the operations Celsus described
was the use of skin flaps to repair ears, noses, and lips4.
Although much medical knowledge was lost in the Middle
Ages, reconstructive surgery was revived by an Italian surgeon
Gaspare Tagliacozzi in 1597 in his treatise on reconstruction of
amputated parts, De Curtorum Chirurgia per Insitionem [2–4]. In
particular, Tagliacozzi described a technique for rhinoplasty
using a fasciocutaneous flap from the left upper arm. However,
advances in skin grafting did not emerge until late 1800s.
4. Reverdin pinch grafting
In 1869, a Swiss surgeon Jacques-Louis Reverdin reported his
technique of “epidermic grafting,” which involved implanted
islands of epidermis to serve as centers of epithelialization and
growth on wound [2]. The detached epidermis particles were
capable of forming a permanent union with the underlying
granulation tissue and actively proliferating to form a new
epithelium [2]. The grafts were harvested by pinching the skin
between the index finger and thumb or using a sharp lancet
and shaving away small pieces of epidermis without drawing
blood [2]. It was later discovered that the grafts contained the
papillary layer of the dermis and were not truly epidermic
grafts [4].
The first case of Reverdin pinch grafting was performed by
placing two 1mm2 pieces of epidermis on the granulation
tissue of a patient who had lost the skin on his thumb. As this
technique became more widely used, it evolved to improve
clinical outcomes. It was noted that each individual graft had a
Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015
well-defined limit of proliferation; therefore, multiple grafts
were advantageous because they formed a firmer scar more
rapidly2. In addition, small grafts were better than large ones
[2]. Pinch grafting stimulated proliferation not only from the
individual grafts, in addition to repeithelialization from the
edges of the wound [2]. The grafts could be placed on
granulation tissue or fresh wound surfaces after hemostasis,
but did not take on bleeding surfaces [2]. Grafts could be taken
from other places on the body (autograft), other humans
(allograft), or from amputated limbs [2].
Although Reverdin pinch grafting was a significant step
forward in skin grafting, it had several limitations. The grafts
caused contractures that were no better than the contractures
formed around non-grafted wounds, limiting their utility
around joints [2]. The grafts also healed slowly, and the new
scar tissue was not resistant to stress and cosmetically
unsatisfactory [2].
Despite these drawbacks, Reverdin pinch grafting is still
clinically relevant today, especially for treating chronic leg
ulcers. In a single center experience in Granada, Spain, Ruiz
Villaverde et al. used pinch grafting to treat 412 ulcers in
146 patients [6]. Grafts took after 1 week, with an average
estimated healing time of 9.4 weeks. The total cure rate was
38% within 6 months of follow up. The authors recommended
pinch grafting because it is technically easy and can achieve
satisfactory results.
5. Ollier grafting
Louis Léopald Ollier, a French surgeon, introduced the next
modification of split thickness skin grafting in 1872. The
technique uses strips of skin grafts ranging from 4 to 8cm2
placed close together over the entire surface of the wound [2,4].
Because the split-thickness skin grafts included epidermis and
part of the dermis, Ollier grafting was also called “dermo-
epidermic grafting” [2]. Compared to Reverdin pinch grafts,
Ollier grafts had significant advantages. They resulted in faster
healing, less scar formation, and less contraction [2]. In
addition, the resulting skin was softer, more supple, and more
resistant to pressure and friction [2]. Despite these advantages,
Ollier’s technique was not well received in his home country of
France, and was refined and popularized couple of years later
by a German surgeon named Karl Thiersch [2].
6. Thiersch grafting
Karl Thiersch presented his technique of split thickness skin
grafts in 1876 at the 15th Congress of the German Surgical
Association (XV Kongress der Deutschen für Chirurgie) [2]. Due
to Ollier’s contributions in developing this technique, it is also
called the Ollier–Thiersch grafting. First, the wound bed was
prepared by removing the granulation tissue with a razor,
because it was believed that this would relieve contractures. In
addition, clean surfaces took grafts better than granulation
tissue3. Subsequently, the entire surface of the wound was
covered with strips of thin split-thickness skin grafts (STSGs).
These grafts had a thickness of 0.008–0.010 inches (0.2–
0.25mm) [2]. Thiersch grafting was quickly adopted by
JBUR 5164 No. of Pages 6
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surgeons across Europe and the United States and used as the
standard of skin grafting until the 1940s.
In general, Thiersch grafts had good graft take ratio and was
technically easy to prepare. A review of outcomes of
629 Thiersch grafts performed by the plastic surgery unit of
the London County Council was conducted in 1940 [7]. In
primary grafts placed over newly created surgical wounds, 83%
of 391 grafts had complete or very good (defined as over 75%)
take [7]. In secondary grafts placed over long-standing wounds
or granulating areas, 41% of 144 grafts had complete or very
good take [7]. The authors also observed that thinner grafts
were advantageous because they were associated with higher
probability of take. In addition, thicker grafts had delayed
healing by secondary intention of the donor site, leading to
increased risk of scarring and keloid formation. Common
reasons for failure included surface mixed infections by
pyogenic organisms, improper preparation of the granulating
wound surface, hematoma, and inadequate fixation of the
graft7. Infection and hematoma caused mechanical separation
of the epithelium from the wound bed by pus or blood
accumulation, leading to graft failure. Other limitations of the
Thiersch graft technique included contractures, ulceration
and sloughing if exposed to trauma, and a tendency to contract
and ridge [2]. While discussing Thiersch grafting, it is
imperative to discuss Blair and Brown’s review of this
technique [8]. While, the authors lauded the Thiersch graft
for ease and certainty of ‘graft take’, good final appearance of
the recipient site and timely healing of the donor site; they also
noted some shortcomings. The thinner grafts may not give
sufficient protection to a bearing surface, may not correct the
inequalities of the underlying surface and may subsequently
contract when placed on a freshly made raw surface with a
movable base and movable edges.
Thiersh grafting continues to have clinical applications
today. In 2013, Xu et al. reported the use of Thiersch grafts to re-
epithelialize portions of newly created mastoid cavities or
surgically altered external auditory canals [9]. In 120 cases,
they found high rates of graft survival, reduced rates of post-
operative otorrhea and patchy mucosalization, and no donor
site complications.
7. Wolfe grafting
Another skin grafting technique created in the late 1800s was
Wolfe grafting. It used a single, large, full thickness, fat-free
flap of skin to cover wounds, especially ophthalmic defects like
entropion [2,3]. John R. Wolfe, a Scottish ophthalmologist,
reported this technique in 1875 in a case report about repairing
a defect of the lower eyelid with a full thickness skin graft
measuring 2.55cm [4]. He is credited for introducing full
thickness grafts into ophthalmic practice [5]. In 1893, a German
surgeon named Fedor Krause advised the use of Wolfe grafts at
the 23rd Congress of the German Surgical Association (XXIII
Kongress der deutschen Gesellschaft für Chirurgie), particu-
larly in cases where Thiersch grafts had unsatisfactory
results5. Because Krause popularized the use of Wolfe grafts
in general surgery, they are also called Wolfe–Krause grafts.
Compared to Thiersch grafts, Wolfe grafts had several
important advantages. They had a minimal tendency to
Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015
3
contract and wrinkle, had better color and texture, and were
able to withstand more mechanical stress [10]. However, they
had several disadvantages that restricted their widespread
use. Wolfe grafts had lower rates of success compared to
Thiersch grafts [2]. They were limited in size because the donor
site often had to be closed with a Thiersch graft, so they could
not be used to cover large defects9. Finally, Wolfe grafts were
harder and more tedious to use [10].
8. Limitations of skin grafting during the late
19th and early 20th centuries
During the late 19th and 20th centuries, Thiersch and Wolfe
grafts were commonly used techniques in skin grafting. The
grafts were cut freehand with a large knife, making it difficult
to standardize the thickness of the skin graft. Although various
knives, such as the Humby knife, were invented to address this
problem, there were still unavoidable differences in graft
thickness among grafts cut by different surgeons and among
multiple grafts cut by the same surgeon.
Another limitation was that the thickness of the dermis
needed for successful take was not yet established during this
time. An American surgeon named Earl Padgett studied the
factors determining dermal thickness, which included the
wound base, location of recipient area, location of donor area,
and age of the patient [11]. He concluded that the granulating
wound bases should be covered with thinner skin grafts
compared to denuded, aseptic wound bases. Also, thicker skin
grafts should be used to cover recipient areas that are subject
to trauma and where it is necessary to avoid contractures. The
location of the donor area also dictates the thickness of the
graft. Skin from the inner arm and inner thigh is generally
thinner than skin from the outer thigh, abdomen, and back.
Finally, younger patients have thinner grafts. He divided skin
grafts into four standardized thicknesses: Thiersch grafts
(0.008–0.010 inches; 0.2–025mm), STSGs (0.012–0.016 inches;
0.3–0.4mm), three-quarter skin grafts (0.018–0.022 inches; 0.45–
0.55mm), and full thickness skin grafts (0.030–0.038 inches;
0.75–0.95mm) [11].
9. Padgett dermatome and modifications
In 1939, Earl Padgett and his engineering co-worker George J.
Hood, developed a semi-cylindrical calibrated dermatome
[12,13]. The Padgett dermatome consists of a drum with a
movable knife fixed at a defined distance from the drum
[12,13]. This distance could be altered in 0.001inch increments
using calibrated screws, and grafts were cut in standard
rectangles of 4-by-8 inches. The skin graft was fixed to the
drum using rubber cement. Grafts cut by the dermatome had
many advantages compared to freehand cut grafts. In a study
comparing the properties and surgical outcomes of skin grafts
cut by dermatome versus freehand, the dermatome could
produce larger grafts (average size 357cm2) that could be
applied in a single operation compared to freehand grafts
(average size 89.6cm2) [12]. Dermatome-cut grafts also had
higher rates of take compared to freehand-cut grafts across
different graft thicknesses11. In thin skin grafts, 81/81 (100%) of
JBUR 5164 No. of Pages 6
4 burns xxx (2017) xxx –xxx
grafts cut by the dermatome had greater than 80% take
compared to 56/93 (60%) of freehand grafts. The certainty of
graft take allowed surgeons to attempt complex reconstruc-
tions that could not be done previously. In addition, the
dermatome gave surgeons better control over the thickness of
the graft and allowed them to take grafts from any uneven
surface, which increased the availability of donor areas [13].
The numerous advantages of the Padgett dermatome caused
George Warren Pierce, one of the founding members of
American Board of Plastic Surgery, to call it the “greatest
contribution in many decades to the technique of skin
grafting” [13].
One limitation of the Padgett dermatome was the technical
difficulty of using it. In particular, the graft often separated and
curled away from its rubber cement backing during the cutting
[14]. Several modifications were made to address this problem.
The rubber cement backing was replaced by various materials,
such as Pilofilm, Dermatape, and Micropore surgical tape, to
simplify separation of the graft from the drum and to prevent
shrinking and wrinkling of the graft [10,14]. In 1948, a young
American surgeon named Harry M. Brown developed the first
powered dermatome, which formed the basis of the modern-
day Zimmer dermatome [15]. He conceived the idea of this new
instrument while being retained as a prisoner of war during
World War II [16].
10. Meek-wall microdermatome
In 1958, an American surgeon named C. Parker Meek proposed
expansion of skin grafts by cutting 2.5cm square (1 square
inch) of skin into 256 smaller squares [17]. It had been observed
that skin grafts grow outward from the periphery, so Meek’s
theory was to increase the length of margin while using the
same total surface area of skin graft. He devised a micro-
dermatome that recut a square inch of split-thickness grafts
into 1/16-inch squares, increasing the length of margin from
4 inches to 64 inches [17]. The graft squares were then placed
on prefolded gauzes to achieve a regular distribution. The first
case report of microdermagrafting on a 14year old girl with a
25% total body surface area (TBSA) burn had good outcomes
and complete healing of the burn wound after 10days [18].
Although the meek technique could expand grafts up to a
1:9 ratio, it did not gain widespread clinical application
because the device for mincing of the skin grafts was expensive
and the method was labor intensive. The skin graft squares
had to be placed dermal side down, which was technically
challenging and time consuming.
Modifications of the Meek technique have been described
in multiple studies. The ultra postage stamp skin graft was
described by Vandeput et al. in 1966 [19]. Ultra postage stamp
grafts are 0.050-by-0.050-inch skin particles created by doubly
meshing a sheet graft. These grafts had an expansion ratio up
to 1:7 and re-epithelialized in 12–15days [19]. Kreis et al.
combined a modified Meek technique with an overlay of
glycerol-preserved allografts to treat 10 patients with exten-
sive burns (mean TBSA 64%) with good results [20]. The mean
take after 1 week was 92% and the mean epithelialization rate
was 90% after 5 weeks. Hsieh et al. have also described good
outcomes in using the modified Meek technique to treat
Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015
severely burned patients (mean TBSA 73%) [21]. The viability of
the graft after 10days was 90–95%. Overall, the modified meek
technique has high rates of successful take, rapid healing time,
and more resistance to infection. It is particularly useful when
donor sites are limited.
11. Tanner mesh grafts
Sieve grafts, or skin grafts with staggered cuts, had been
described in early 1900s to increase coverage and promote
drainage [3], and [22]. In 1908, Lanz described an accordion-like
expansion of the Thiersch graft by making serial longitudinal
incisions in the graft and stretching it transversely. One half of
the skin strip, expanded to form an accordion, was trans-
planted and the other half, also expanded, was sufficient to
cover the defect created at the donor site [22]. There were
multiple modifications of the techniques over next few
decades but none of them achieved widespread acceptance
[3]. In 1964, James C. Tanner, an American plastic surgeon,
used this idea to create the Tanner–Vandeput mesh derma-
tome [23]. The mesh dermatome processed split-thickness
sheet grafts into a mesh with 0.050-inch wide ribbons of skin.
The 0.050-inch width was chosen because it was the minimal
size for an independent skin particle to take and grow [23]. In
250 clinical cases, Tanner found a mean take of over 90% [24].
Stone and Hobby also reported 98% take in 49 patients and a
marked decrease in mortality [25].
There are many advantages to Tanner mesh grafting [23].
Mesh grafts can be expanded up to six times, increasing the
area that can be covered and decreasing the donor-site area.
They also have an increased percentage of take and faster
healing compared to sheet grafts. The gaps in the mesh allow
for improved drainage, preventing the accumulation of serum
or exudate and increasing resistance to infection. Mesh grafts
are also more flexible than sheet grafts, allowing them to have
better success on irregular areas such as the neck and axilla.
Finally, mesh grafts had less contracture, keloid formation,
and ulcerations.
One major limitation of mesh grafts is that they leave a
permanent fishnet pattern, making them cosmetically inferior
to sheet grafts [23]. Sheet grafts also offer better vasculariza-
tion and re-innervation, so they are more stable, provide
greater function, and are preferred to cover vital structures.
However, because of its multiple advantages, mesh grafts were
rapidly adopted and are used today as the standard of care.
12. Future perspectives
Meshed split-thickness skin grafts (STSG) which are harvested
with a powered dermatome continue to be the most commonly
used skin grafting technique currently. In a very large burn
wound with limited donor site for STSG, the skin graft is
meshed and expanded up to 6 times (possibly 9 times) but the
donor sites may still not suffice [17,18]. There has been a recent
push towards developing grafting technique with higher
1
expansion ratio. In 2012, Hackl et al. described Xpansion
technique using 0.8-by-0.8mm (0.031-by-0.031 inch) micro-
grafts [26]. Compared to Meek micrografts and ultra postage
JBUR 5164 No. of Pages 6
burns xxx (2017) xxx –xxx
stamp grafts, this technique is faster and easier to apply since
the grafts can be placed on the wound without regard to
dermal orientation while providing fast re-epithelialization in
a moist or wet environment. In porcine models, complete
epithelialization occurred within 14days with a 100 times
expansion ratio. This technique has been successfully used in
a 25year old patient with a 54% TBSA burn in a U.S. Army
military hospital in the Iraq war zone [25,27].
Uses of bioengineered skin substitutes are also gaining
1
significant interest. The Integra dermal regeneration tem-
plate has been studied and reported extensively in multiple
studies. It provides a bilayered skin regeneration template
[28–30]. The top layer is a thin film of poly(dimethyl siloxane)
that limits bacteria invasion and controls moisture flux to
physiologic levels. The bottom layer is a highly porous
scaffold, a graft copolymer of type I collagen and chondroi-
tin-6-sulfate, that induces regeneration of the dermis in the
1
full-thickness skin wound [28,29]. The Integra template is
applied following the excision of the wound to viable tissue.
Following the regeneration of dermis in about 3 weeks, the
silicone layer is removed and is replaced by a thin (0.004–
0.008 inch) autograft [28,29]. In a study of 29 patients with
43% total body surface area burn, Integra take was reported
to be 82% with no foreign body reaction [30]. The dermal
regeneration was similar to normal dermis. Autologous non-
1
cultured cell therapies such as ReCell Technology have also
been studied in partial thickness wounds [31]. With this
technology, intercellular detachment of the donor STSG is
initiated by incubation in trypsin solution at 37  C for 20 min.
After digestion, the sample is mechanically agitated to
separate the cells. Finally, the cells are suspended in a
lactate solution and sprayed over the wound [31]. It can be
performed in approximately one hour and enables treatment
of large wounds without a need of scaffold [32].
Conclusions
Skin grafting techniques have developed significantly over
past 200 years from Reverdin pinch grafting to meshed skin
grafts using powered dermatome. Increased expansion ratio
and improved cosmetic and functional outcome of skin grafts
are the main focus of ongoing skin grafting research and
1 1 1
emerging techniques (Integra , Recell , Xpansion ) are show-
ing promise in treatment of burns.
Conflict of interest and financial disclosure:
All authors have made substantial contributions to all of the
following: (1) the conception and design of the study, or
acquisition of data, or analysis and interpretation of data, (2)
drafting the article or revising it critically for important
intellectual content, (3) final approval of the version to be
submitted.
The authors have no conflicts of interest to disclose with
respect to research, authorship and/or publication of this
article. They have not received any financial support for this
research work.
Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015
5
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Please cite this article in press as: M. Singh, et al., Evolution of skin grafting for treatment of burns: Reverdin pinch grafting to Tanner
mesh grafting and beyond, Burns (2017), http://dx.doi.org/10.1016/j.burns.2017.01.015