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Manuscript ID number: 151503 Date of page proofs: 19 October 2018

Title of paper: Autologous non-cultured melanocyte–keratinocyte transplantation in the treatment of vitiligo: patient
selection and perspectives
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Journal Title:
Clinical, Cosmetic and Investigational Dermatology
Manuscript ID Number:
151503
Manuscript title:
Autologous non-cultured melanocyte–keratinocyte transplantation in the treatment of vitiligo:

patient selection and perspectives
Print full names of author(s):
Professor Dalia Bassiouny

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Clinical, Cosmetic and Investigational Dermatology Dovepress

open access to scientific and medical research
Review
R
Open Access Full Text Article
Autologous non-cultured melanocyte–
T
keratinocyte transplantation in the treatment
H O
AU
of vitiligo: patient selection and perspectives
O O F
Dalia Bassiouny Abstract: Autologous non-cultured melanocyte–keratinocyte transplantation procedure
PR
Samia Esmat (MKTP) is one of the simplest cellular grafting techniques. Various modifications were done
over the years to make the technique easier and more economical which led to its great popularity
Department of Dermatology, Kasr
El-Ainy Teaching Hospital, Faculty of among dermatologists. Proper patient selection and good technical skills are essential for achiev-
Medicine, Cairo University, Cairo, ing success with this technique. In this review, different patient-related and procedure-related
Egypt
factors that affect the outcome are discussed. This review may guide dermatologists to select
suitable candidates, and explains what to expect in each case and indicates different techniques
Y
which can be used. The expected complications and stability of acquired pigmentation, which
P
are an essential part of the pretreatment patient counseling, are also discussed.
O
Keywords: cellular grafting, vitiligo surgery, patient variables, procedure variables,
C
repigmentation
Introduction
r
Surgical treatment of vitiligo is the final resort to regain the pigmentation in lesions
o
failing to repigment despite various medical and light therapies. Multiple cellular and
f
tissue graft techniques are used successfully to introduce melanocytes and/or their
t
stem cells to vitiligo lesions devoid of them.1
o
Autologous non-cultured melanocyte–keratinocyte transplantation procedure (MKTP)
N n
is one of the simplest cellular grafting techniques and is currently the most popular among
i o
dermatologists. It offers 50%–100% repigmentation rates with 1:3 up to 1:10 donor-to-
t
recipient ratio and very good color matching in most of the treated cases.2–6 Since its first
a
description by Gauthier and Surleve-Bazeille in 1992,7 the technique of cellular grafting
i c
evolved over the years with various modifications simplifying it and improving the results.
l
The response to MKTP in general is affected by several factors. As with other
u b
surgical techniques, proper patient selection is a crucial point as well as good technical
p
skills. Different patient-related and procedure-related factors that affect the outcome
are discussed in this review. This review may guide dermatologists to select suitable
candidates, and explains what to expect in each case and indicates different techniques
Correspondence: Dalia Bassiouny which can be used. The expected complications and stability of acquired pigmentation,
Department of Dermatology, Kasr which are an essential part of the pretreatment patient counseling, are also discussed.
El-Ainy Teaching Hospital, Faculty of
Medicine, Cairo University, 106 Gamet
Al-Dowal Street, Floor 11, Mohandessien, Technique evolution
Cairo, Egypt
Tel +20 2 749 6759
In 1992, Gauthier and Surleve-Bazeille7 described the MKTP as a 2-day procedure.
Email daliabas73@yahoo.com On the first day, a shave biopsy was harvested from the scalp and incubated overnight
submit your manuscript | www.dovepress.com Clinical, Cosmetic and Investigational Dermatology 2018:11 1–20 1
Dovepress © 2018 Bassiouny and Esmat. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.
php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work
151503 15 October 2018 you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For
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Bassiouny and Esmat Dovepress
in 0.25% trypsin at 4°C. The recipient site was also prepared without any additives for suspending the cell pellet.3 He later
by liquid nitrogen. On the second day, the trypsinized epider- replaced trypsin inhibitor by washing the epidermis several
mis was placed in EDTA for 15 minutes, after which it was times in DMEM/F12 before separating it from the dermis.17
transferred to a calculated volume of saline. The basal layer Later, PBS was used during suspension preparation to further
was rubbed, the skin was agitated to dislodge the cells and cut the cost.18 Kumar et al19 introduced a four-compartment
finally the suspension was aspirated by an insulin syringe technique in 2014 in which pipettes, autoclaved tips, centri-
and injected into cryoblebs. fuge tube and centrifuge machine were no longer needed. The
Several modifications aiming at simplifying the technique dermatologists estimated and used the exact amount of PBS
and improving the outcome were done over the years. Tis- to prepare the suspension according to the size of the lesion
sue was harvested from the gluteal area8,9 which allowed for to be treated which was then aspirated by a syringe and spread
harvesting a larger area and was also less vascular. Shave evenly onto the denuded recipient surface.
biopsy is simple and fast but may lead to development of Finally, in order to complete the procedure in 1 day, prepara-
textural change or scar in the donor site which prompted the tion of the recipient area using dermabrasion8 or laser resurfac-
researchers to search for a solution. In vivo preparation of ing9 as opposed to cryotherapy7 was done. Not only did this
epidermal cell suspension was introduced by Gupta et al10 save time, but it produced better cosmetic outcome as the cells
with excellent response in five treated cases. MKTP was per- were evenly spread over the whole lesion. Less invasive methods
formed entirely in sterile blisters on the patient’s body with no such as dermaroller20 or fractional CO221 were recently used to
donor site scarring and very high cell viability (99%). Roofs introduce the cells into the skin to minimize the downtime. To
of suction blisters were used in another study for suspension improve cell handling, collagen sheets8 or hyaluronic acid (HA)
preparation; however, no clear data were given in the study was used to create a paste.9 This allowed using MKTP even on
about repigmentation rate.11 Nevertheless, suction blister curved surfaces with ease. Details of these changes over the
formation is a time-consuming process. years are given in Table 1. The effect of these changes on the
Since the hair follicles are the main reservoir and the response is discussed in detail later in this review.
source of melanocytes that repopulate the epidermis in non-
glabrous skin, it was only a matter of time before dermatolo- Effect of patient-related factors on
gists thought of harvesting this rich source of melanocytes for response to MKTP
cellular transplantation. In 2009, Vanscheidt and Hunziker12 Duration of disease stability
used plucked hair follicles for preparation of cell suspension A strict selection of patients with stable vitiligo is the most
which produced >90% repigmentation in 3/5 cases of vitiligo. important factor for successful outcome. Disease activity is
Mohanty et al13 used follicular unit extraction technique defined as the appearance of new lesions or enlargement of old
instead of plucking to harvest anagen hair follicles which was ones observed in the past year and/or the presence of Koebner
a more tedious process but provided a significantly higher phenomenon.5 Our only available activity score, the vitiligo
number of stem cells, as well as ten times more cell yield per index of disease activity score,22 depends on clinical history
hair follicle.14 Although this suspension was rich in highly pro- given by the patient. However, certain clinical features can
liferative melanocytes and stem cells, it lacked an abundance help the dermatologist to identify disease activity, including
of healthy keratinocytes which are essential for supplying hypomelanotic color of vitiligo lesions and poorly defined
melanocytes with growth factors needed for their prolifera- borders as opposed to amelanotic lesions with sharply demar-
tion. In a trial to get the best of both worlds, recent publications cated borders which denote stability.23 Other signs of activity
used a mixture of epidermal and follicular suspensions with include confetti lesions and trichrome vitiligo (Figure 1).24
better results than epidermal suspension alone.15,16 On reviewing the literature, earlier studies using MKTP in
Preparation of the suspension underwent major changes the treatment of vitiligo chose different durations of disease
too. Olsson and Juhlin8 incubated the skin at 37°C for 50 min- stability as an inclusion criterion. Some authors considered 6
utes in a CO2 incubator, used trypsin inhibitor to stop tissue months of disease stability to be sufficient,2,4,17,25,26 while oth-
digestion, centrifuged the cells to obtain a cell pellet and added ers required 1 year of disease stability.8,9 In the early reports
supplements such as antimicrobials and growth factors to the by Mulekar,2,4 in which cases with a minimum of 6 months
suspension medium. These additional steps increased the cost of disease stability were included, ≥95% repigmentation
of the procedure. Mulekar made the procedure easier and more occurred in 65/122, 13/19 and 36/43 cases of generalized
economical by using an ordinary incubator and DMEM/F12 vitiligo (GV), focal vitiligo and segmental vitiligo (SV),
2 submit your manuscript | www.dovepress.com Clinical, Cosmetic and Investigational Dermatology 2018:11
Dovepress
Table 1 Different modifications in autologous non-cultured melanocyte–keratinocyte transplantation technique
Number Donor tissue Trypsinization technique Medium used for Recipient site Application of Patient Reference
of days suspension preparation suspension immobilization
Dovepress
Two Day 1: superficial skin samples Day 1: cold trypsinization. Skin Saline (1 mL/1 cm2 skin) Day 1: liquid Day 2: partial aspiration 20 minutes Gauthier and
from the occipital scalp using a incubated for 18 hours at 4°C in nitrogen induced of blister fluid and Surleve-Bazeille
dermatome with a razor blade 0.25% trypsin blisters 1 and 2 cm injection of 0.1 mL of (1992)7
Day 2: skin incubated in apart cellular suspension/
EDTA for 15 minutes at room blister by a 25-guage
temperature insulin syringe
One Superficial skin sample with a Warm trypsinization. Skin sample Supplemented melanocytic A high-speed Suspension covered 4–5 hours Olsson and Juhlin
1:4–1:10 donor-to-recipient torn into 2 cm2 pieces and medium: M2 medium dermabrader, fitted by a thin collagen film, (1998)8
area ratio taken with a Goulian incubated at 37°C in 5% CO2 supplemented with basic with a diamond M2-moistened gauze and
biopsy knife for 50 minutes in trypsin/EDTA fibroblast growth factor, wheel Tegaderm
solution. Trypsin inhibitor added penicillin and streptomycin
One A shave biopsy (1/2–1/4 of following incubation Supplemented melanocytic CO2 laser resurfacing 0.5–1 mL of hyaluronic 6 hours van Geel et al
recipient area) from the gluteal medium: M199 medium acid added to suspension (2001)9
Clinical, Cosmetic and Investigational Dermatology 2018:11

region using a hand dermatome supplemented with insulin, to increase viscosity

hydrocortisone, cholera toxin,
penicillin/streptomycin and
transferrin/triiodothyronine
One A shave biopsy (1/3–1/10 of Warm trypsinization No supplements: DMEM/F12 High-speed Suspension covered by Left immediately Mulekar (2003)2
recipient area) from the gluteal Ordinary incubator used followed only dermabrader fitted collagen film, DMEM/ Mulekar (2004)3
region by a silver skin grafting by addition of trypsin inhibitor with a diamond fraise F12-moistened gauze Mulekar (2005)4
knife In 2009, trypsin inhibitor step wheel and Tegaderm Mulekar et al
replaced by washing tissues (2009)17
Mulekar et al
(2010)25
Two Day 2: superficial skin samples Day 2: skin incubated for 40 Supplemented melanocytic Day 1: liquid Day 2: hyaluronic acid 2 hours El-Zawahry et al
from the gluteal region (1/10 of minutes at 37°C in an ordinary medium: Ham F12 nitrogen induced added to suspension (2011)30
recipient area) incubator followed by 1% FBS supplemented with blisters 1 and 2 cm in 1:6 ratio to form
addition to neutralize trypsin L-glutamine, penicillin– apart an injectable viscid
streptomycin, hydrocortisone, suspension
basic fibroblast growth factor,
isobutylmethylxanthine and
3′,5′-cAMP
One Anagen HFUs from the occipital HFUs incubated at 37°C for three Suspensions of all three tubes A motorized Suspension spread and Not stated Mohanty et al
region (15–25) to produce 30-minute cycles. HFUs placed combined in a single tube dermabrader fitted covered with a collagen (2011)13
ORSHFS in a new tube of trypsin–EDTA and filtered through a 70 µm with diamond fraises dressing of fish origin
and trypsin inhibitor added to cell strainer, centrifuged and used till pinpoint
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submit your manuscript | www.dovepress.com
previous tube each time suspended in DMEM bleeding appeared
(Continued)
3
Autologous non-cultured MKTP in the treatment of vitiligo
A B
Gauthier (2017)20
Benzekri and
Reference
Razmi et al
Jeong et al
(2016)11
(2017)15
immobilization
Not stated
Not stated
Not stated
Patient
mm needles repeatedly
A dermaroller with 0.2
Suspension spread and
Manual dermabrasion Suspension spread and
passed over lesion for

covered with collagen
covered with collagen
Figure 1 Clinical signs of disease activity.

Application of
Notes: (A) Active disease is characterized by ill-defined borders and hypopigmented

suspension
lesions (black arrow). Other signs of activity include Koebner phenomenon and
10 minutes
confetti-like lesions (white arrow). (B) Stable disease shows milky white lesions with
dressing
dressing
well-defined borders. Note perifollicular repigmentation at the borders of the lesion

(white arrow). (A) Courtesy of Marwa A Abdallah, Professor of Dermatology and
Venereology, Ain Shams University, Cairo, Egypt).
Abbreviations: FBS, fetal bovine serum; HFUs, hair follicle units; NCES, non-cultured epidermal suspension; ORSHFS, outer root sheath hair follicle suspension.
CO2 or Er:YAG laser
respectively. However, a high relapse rate was noted in 15

skin followed by
extending 5 mm
applied to intact
Recipient site
beyond lesion
preparation
of those responders. Huggins et al26 achieved ≥95% repig-

dermaroller
Suspension
cell suspension and centrifuged resurfacing
mentation in only 4/23 treated cases with 6-month duration

borders
of stability. In a retrospective long-term follow-up study of

cases treated over the past 6 years, 6 months of stability was
resuspended in PBS and mixed
sufficient as an inclusion criterion. More than 75% repigmen-

at 2,000 rpm for 5 minutes.
Ringer lactate added to the
Suspension centrifuged and

0.5–1 mL of Ringer lactate
Cell pellet resuspended in
cell pellet resuspended in
tation was noted in 71% and 54% of SV and non-segmental

centrifuged at 78 × g for
5 minutes and cell pellet
vitiligo (NSV) cases, respectively.27 On the contrary, a higher

NCES and ORSHFS
Medium used for
percentage of repigmentation was noted in one study where

in a ratio of 1:5
patient’s serum
suspension
all three SV and 13/17 NSV cases with 1-year stability

showed 95%–100% repigmentation8 and in another study
where all four cases achieved 84%–100% repigmentation.9
In a retrospective study by Olsson and Juhlin,28 cases that
NCES: CO2 incubator used for 1
Epidermal undersurface scraped
and stratum corneum discarded
hour, followed by rinsing in PBS
Cold trypsinization followed by

Aspirated blister fluid added to
showed stable improvement of their vitiligo had a 78% repig-

addition of patient’s serum for
Blister roof incubated at 37°C
in trypsin until a cloud of cells
ORSHFS: as in Mohanty et al
Trypsinization technique
mentation in response to different melanocyte transplantation

act as trypsin inhibitor.
techniques including MKTP after 4.8 years compared to

and cell separation
cases with unstable vitiligo that showed a 33% repigmenta-

trypsin inhibition
tion after 6.5 years. The authors recommended that patients

separated.
with extensive GV and those who have not had completely

(2011)13
stable, non-progressive vitiligo for at least 2 years should not

be chosen for transplantation.
NCES: 1:10 ratio taken from thigh
ORSHFS: 15–25 HFUs extracted
Superficial skin samples from the

Combined epidermal suspension
Active disease and the presence of Koebner phenomenon

Blister fluid aspirated and roofs
Suction at 380 mmHg in 5 mL
Each blister: 0.785 cm2. Total

syringe(s) applied to thigh to
were found to negatively influence treatment results.5,13 Activ-

create suction blister(s)
donor 1/10 of recipient
ity resulted in failure of MKTP suspension in one study5

with a median area percentage of repigmentation of zero
Donor tissue
compared to 93% in stable cases at 12-month posttreatment

from the scalp
occipital scalp
and ORSHFS
follow-up. Similarly, 79% repigmentation occurred in cases

removed
Table 1 (Continued)
with ≥1-year stability vs only 18% in cases with <1-year

duration of stability (P=0.02) in another study.13 A signifi-
Number
cant positive correlation between duration of stability and

of days
percentage repigmentation of the lesions was also found in

One
One
One
a recent study.29
Dovepress
Dovepress Autologous non-cultured MKTP in the treatment of vitiligo
Based on the above data, since 2004 the majority of authors two times higher in the 501–1,500 cm2 group, compared with
including Mulekar3 consider 1 year as the minimum duration patients with >1,500 cm2 white area.28 Similarly, a negative
of stability needed for a favorable outcome of surgery.30–41 correlation was found between Vitiligo Area Scoring Index,
When uncertain about stability, a longer pretreatment obser- and Vitiligo European Task Force area and stage scores and
vation documented by photography or a minigrafting test42 may percentage repigmentation in a more recent study.28
be indicated to avoid unfavorable outcome of surgery. Disease A significant negative relation was found by the authors
stability should be considered in both SV and NSV. SV can of a study between the total treated surface area and the
respond to medical treatment during the first 6 months. treatment outcome (P=0.0086).6 No similar correlation
was found by other authors.29 The majority of authors used
Type of vitiligo MKTP in treatment of lesions <100 cm2 with a favorable
When it was first described by Gauthier and Surleve-Bazeille outcome.5,7,13,15,31,34,36,38,41,45 A few achieved favorable outcome
in 1992,7 MKTP was used in the treatment of localized vit- for lesions up to 250 cm2.3,8,9,18,25,26,29,30,33
iligo areas of ≤50 cm2 in three SV and eight focal vitiligo
cases. The response was better in SV cases with an average Skin type
repigmentation rate of 92% vs 41% in focal vitiligo cases with Most of the reports do not comment on the skin type of cases
4/7 cases failing to repigment. However, comparable excel- treated; however, when analyzed statistically, similar repig-
lent response (≥95% repigmentation) was found in a series mentation rates were reported in different ethnic groups26
of 25 children and adolescents with SV and focal vitiligo.25 and in different skin phototypes.6,27
SV cases showed a significantly better response than
NSV with 85% vs 70% repigmentation (P=0.011) in one Age
study6 and >50% repigmentation in 88% vs 71% of cases in Age did not affect the percentage of repigmentation in several
another study (P=0.007).40 Other studies reported a better studies.6,27 Many studies included children and adolescents
response in SV cases, although statistical analysis was not in the treated cases.2,5,6,8,17,25,27,30,31,34,36,38,41,43,46 Two studies
performed2,3,8,26,28,43 or was not significant.13,38 Immunological focused solely on the treatment outcome in this age group.
disturbances probably interfere with the outcome of trans- Mulekar et al25 treated 25 children and adolescents using
plantation in GV.28 general anesthesia with ≥95% repigmentation in 8/13 SV and
No difference in improvement according to the type of 7/12 focal vitiligo cases. New lesions developed during fol-
vitiligo was noted in a recent study using outer root sheath hair low-up in 5/12 focal vitiligo cases which could be attributed
follicle suspension (ORSHFS) in the treatment of 25 cases of to the short duration of disease stability (6 months) applied in
stable vitiligo (nine SV, eleven acrofacial vitiligo, five GV).44 this study. The second study involved 13 cases of vitiligo (six
Mixed vitiligo cases responded less favorably than SV SV, 1 focal vitiligo and six GV) with 1-year disease stability.
and GV cases to MKTP.38,40 Topical anesthesia followed by local infiltration was applied
Acrofacial type in general is less responsive to surgical in 15/19 lesions achieving >90% repigmentation.18 In both
therapy. Lesions on the fingertips were even considered an studies, the procedure was well tolerated and accepted by
exclusion criterion by some authors.2,27 Interestingly, the both children and their parents. The main concern in children
presence of vitiligo on lips and fingertips (lip-tip type) was was pain intolerability and fidgeting during the procedure.
associated with a poor response, even when MKTP was Increasing the concentration of topically applied creams
performed at other sites in the same patient.26 can be a good option in cooperative children, but general
anesthesia may be still needed in selected cases.
Extent of vitiligo and size of treated lesion
Surgical therapy in general is indicated in stable cases with Gender
limited areas of vitiligo which are nonresponsive to medical No significant difference was found in repigmentation
therapy. Several authors excluded cases with widespread between males and females.6,27,28,41
vitiligo involving >30% of the body surface area.2,37,43
The probability of a successful transplantation outcome to Disease duration
non-cultured epidermal suspension (NCES), ultrathin sheet The effect of this variable was assessed in a few studies
transplantation and cultured epidermal suspension (CES) was with no correlation found in two6,41 and a negative correla-
found to be 20 times higher (OR) in patients with <100 cm2 tion where patients with shorter disease duration got better
white areas, three times higher in the 101–500 cm2 group and treatment results in another.27
Clinical, Cosmetic and Investigational Dermatology 2018:11 submit your manuscript | www.dovepress.com
5
Dovepress
Site of lesion extremities.6 On the contrary, some authors reported an

On reviewing the literature, the head and neck lesions usually excellent response of lesions overlying joints with ≥95%
showed the best response, lesions on the limbs (excluding the repigmentation achieved in 54% of lesions in one study4
elbows, knees and ankles) and trunk showed an intermediate and in 100% of lesions in others.18,27 Inadequate depth of
response and lesions over the joints and acral skin tended to dermabrasion due to heavily cornified skin as well as the high
respond less favorably.6,7,26,37,46 Two exceptions were the study mobility at these sites may explain the poor response.46 Holla
by Olsson and Juhlin28 where the neck was found to show the et al35 used strict immobilization up to the extent of using
poorest response to transplantation and the study by Mulekar4 plaster casts when needed and achieved >75% repigmentation
where the response over the face was worse than other sites in 21/33 (64%) treated lesions. In another study, a diamond
and was explained by the traumatizing action of UV sunrays. fraise wheel at a high speed of 12,000–15,000 rpm was used
Other authors did not find a significant effect of the site of to assure proper dermabrasion of the thick cornified skin with
treated lesion on the rate of repigmentation.27,34,36,38,40,41,44 an excellent response achieved in 15/43 (35%) lesions over
Over the head and neck, response rates ranged from joints without applying strict immobilization.17
70% to 100% with over half of the lesions achieving ≥95% Certain sites are considered difficult to manage due to the
repigmentation.7–9,18,25,40,46 delicacy of the skin and/or the difficulty in immobilization
Acral lesions are usually resistant to medical therapy, such as the eyelids, nipples and genital skin. Manual derm-
and hence, MKTP may be one of the few available effective abrasion or diamond fraise wheel at a low speed of 5,000
modalities of therapy. It is important to note that lesions rpm was used with an excellent response achieved in 67%
over the dorsum of the hands and feet respond better than of eyelid lesions and 25% of genital lesions.17
those over the fingers or toes. Some authors do not recom-
mend treating fingertips (distal fingers) owing to the poor Effect of procedure-related factors on
response.2,27 Mulekar4 reported an excellent response in response to MKTP
62.5% of lesions over the dorsum of hands and feet and 66% Donor tissue
of those over the fingers in a series of 142 cases of NSV. Type of tissue used
Fingers and toes also responded well with 42% of lesions Currently, there are two types of suspension used in MKTP,
achieving ≥95% repigmentation in another report by the same NCES8 where the epidermis is the source of cells and
authors.17 However, it was not clear in both studies if any of ORSHFS13 where the anagen hair follicle is the source.
those lesions were over the fingertips (distal fingers). Holla Two studies compared cellular grafting in the form of
et al35 achieved >75% repigmentation in 78% of lesions over NCES to tissue grafting in the form of suction blister epidermal
the dorsum of hands and feet and 42% of lesions over fingers grafting (SBEG). The first involved two groups of cases
and toes with only 6/80 lesions over acral skin showing <50% with comparable results regarding very good repigmentation
response (two over the ankle and four in distal fingers). Fin- (≥75% repigmentation), color matching and side-effect profile.
gertips were found to show full repigmentation in one case However more cases achieved excellent repigmentation
in which cryoblebbing was used for recipient site prepara- (≥90%) in the NCES group (P=0.002). Patient satisfaction
tion29 raising the possibility that perhaps poor response was and dermatological quality-of-life score reduction were also
due to the difficulty in performing dermabrasion or laser significantly higher in the NCES group.34 On the contrary,
resurfacing at this site. Cryoblebs produce separation at the NCES, CES and SBEG were compared in the same patient
dermoepidermal junction regardless of the skin thickness. in another study with significantly better response in SBEG
In a recent study, 35% of acral lesions (excluding those lesions while NCES and CES lesions were comparable.39
on fingertips and toes) demonstrated excellent repigmentation In another study, no significant difference was found
with no difference in outcome found between difficult-to-treat between NCES and CES with >70% response achieved in
sites and other sites.27 Others however showed less favorable 62% and 52% of cases, respectively. Although CES could cover
outcome with 25%,13 15%26,28 or less5,18,29,30,38,46 of the lesions large areas using a small donor sample, it required expensive
over the hands and feet showing ≥95% repigmentation. equipment and reagents in addition to highly trained personnel.37
Similarly, lesions over the joints including elbows, knees A few studies compared NCES and ORSHFS with no
and ankles tend to respond less favorably with <30% of the significant difference found29,36 despite the significantly
lesions showing excellent repigmentation.5,7,26,28–30,43 Lesions higher total cell count yielded by NCES.29 This may be due
over the joints showed a significantly lower response com- to the higher variety of cell populations including melanocyte
pared with presternal lesions and those on the trunk and stem cells in ORSHFS.49,50 On the other hand, inferior results
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were found in ORSHFS group compared to NCES group found between cases with a 1:3 and those with a 1:5 donor-
(43% vs 90% of cases with >75% repigmentation) in another to-recipient ratio. The authors concluded that the minimum
study.41 The authors explained these poor results in ORSHFS number of melanocytes in epidermal cell suspension required
group by the higher number of elderly people and the lack of to produce satisfactory repigmentation (>75%) was probably
proper surgical skills in follicle unit extraction which led to in the range of 210–250 cells/mm2.47
the use of insufficient numbers and transected hair follicles Cell viability is another important factor. As expected,
for preparation of the cellular suspension. These comments a positive correlation was found between the percentage of
highlight the importance of proper choice of patients with repigmentation and the total number of all viable cells and
abundant dark anagen hairs as well as higher level of viable melanocytes transplanted.45
experience required for performing this technique. It should Regarding ORSHFS, a lower mean number of mela-
be noted that long-term stability of pigmentation from hair nocytes of 119 cells/mm2 was associated with optimum
follicle-derived melanocytes has not been established yet. pigmentation which may be due to the different morphology
Hair graying is known to occur with aging.48 and ultrastructural characteristics of hair follicle melanocytes.
Finally, combined NCES and ORSHFS produced superior A count of 76 cells/mm2 CD200+ stem cells was present in
repigmentation when compared to NCES in lesions over the cases achieving >75% repigmentation with a significant
joints and acral skin,15,16 while similar repigmentation rates positive correlation between repigmentation rate at 6 months
were seen over the face15 in two recent studies. and both melanocyte and hair follicle stem cell counts.38 No
similar correlation between percentage of CD200+ cells and
Anatomical site used clinical repigmentation was found in a more recent study.44
The density of melanocytes varies at different body sites
from around 900 melanocytes/mm2 on the back to around Recipient site preparation
1,500 melanocytes/mm2 in the genital region.50 The scalp was Recipient vitiligo skin may be prepared by different
originally chosen for skin harvesting.7 This site has pros and methods including cryoblebbing, 7,29,30,47 dermabras
cons. Being covered by hair, textural or color changes that ion2–4,8,15–18,25–28,33–38,41,43,44,46,51 or laser resurfacing.5,9,29,40,45,52,53
may occur are unapparent, and being rich in hair follicles, the The ideal method should be simple to perform, safe
upper part of the outer root sheath is probably included in the with minimal side effects and eff icient reaching the
sample. However, harvesting of skin necessitates shaving part dermoepidermal junction to avoid scarring or loss of the
of the scalp which may be inconvenient to the patient; also, the grafted melanocytes. Dermabrasion is more economical and
procedure is a bit more difficult as the scalp is curved and more relatively safe but requires technical skills. Pinpoint bleeding
vascular. The gluteal region3,4,8,9 or thigh18,35 is usually chosen denotes reaching the ideal level. CO2 laser resurfacing
as the donor area in MKTP. We found no significant difference produces uniform resurfacing but is more expensive.
in melanocytic cell count between both sites (unpublished However, pinpoint bleeding does not appear. Two studies
data, Bassiouny et al, 2017). However, it is better to avoid the were done comparing different ablative CO2 laser settings
front of the thigh as a scar, color or textural change may occur. with similar repigmentation rates achieved using less invasive
resurfacing. A depth of 209 vs 300 µm was used in one study,52
Donor-to-recipient area ratio while 144 vs 209 µm was used in the second.53 As expected,
Despite the fact that NCES can be prepared using donor tissue less invasive resurfacing resulted in faster healing and less
which is one-tenth the recipient area treated, a closer look at persistent erythema at 6-month follow-up.53 In the same study,
literature reveals that a donor area of one-third to one-fifth fractional laser resurfacing failed to produce an efficient
the recipient site was used in the majority of cases, with response when used for recipient site preparation.53 In a pilot
1:10 ratio reserved for cases with a relatively large recipient study, dermabrasion using a high-speed dermabrader fitted
area.3,4,8,9,17,18,33,40,45 with a diamond fraise wheel produced better repigmentation
The ratio of donor to recipient areas will be reflected on than fractional CO2 laser resurfacing,21 but the latter was
the cell count and number of transplanted cells/cm2. Olsson faster and simpler to perform. In our experience, laser
and Jhulin8 suggested that a melanocytes count of 190/mm2 resurfacing surpassed manual dermabrasion in improving
was the lower limit capable of producing repigmentation. In repigmentation following MKTP in acral and non-acral
an interesting study of effect of donor-to-recipient area ratio lesions (unpublished data, Esmat et al, 2014).
on repigmentation, a significant difference in total and mela- Cryoblebbing must be done 24 hours before MKTP,
nocytes cell counts as well as extent of repigmentation was and therefore, the procedure is done over 2 days. It also
7
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requires longer healing time; however, it may have a role in explore the impact of post-MKTP phototherapy in different
certain sites like the fingertips.30 Only one study compared skin types.
cryoblebbing to laser resurfacing. Cryoblebbing produced
≥75% repigmentation in significantly more lesions (38 vs 10 Complications
lesions) (P=0.001) mainly due to excellent response achieved MKTP is a safe technique with minimal complications. These
over the distal fingers.29 include short-term complications in the form of infection or
Less invasive methods of cellular suspension delivery erythema and long-term complications, the most important
were recently described. Benzekri and Gauthier20 delivered of which are scars and color mismatch.
cellular suspension using a dermaroller equipped with 0.2
mm microneedles with >75% repigmentation in 3/5 cases Short-term complications
with lesions over the face. Successful migration of viable Infection
melanocytes to the basal epidermal layer was demonstrated A low incidence of infection in 5%–16% of cases was reported
using this minimally invasive technique. However, larger by some authors.18,31,37,44,46 A slightly higher incidence of 29%
case series are needed to assess this innovative method. was reported in cases where cryoblebbing was used at the
Intralesional injection of NCES was also attempted in a recent recipient site. This was attributed to the moist nature of the
study involving a large number of cases (300) where >50% lesion and longer healing time.29 In all cases, infection was
repigmentation was obtained in 32.2% of treated patches well controlled by broad-spectrum systemic antibiotics.
(1,060) 9 months after therapy.54
Persistent erythema
Postoperative dressing and wound care A bright pink color or mild erythema which lasts for a few
The type of dressing used postoperatively was found to weeks is expected after MKTP.2,5 Sometimes, erythema per-
affect the outcome of repigmentation at 12 months. In one sisted for a few months, especially in cases where CO2 laser
study, 83% of cases where collagen dressing was used vs resurfacing was used for recipient site preparation. This was
63% of those where HA was used achieved ≥50% response reported less frequently when more superficial full ablation
(P=0.017).40 Collagen dressing was compared to petrolatum- was performed (50% of lesions at 144 µm vs 70% of lesions
impregnated gauze in the same patient in a pilot study with no at 209 µm depth of ablation).53b
significant difference in repigmentation. However, the gauze
was more difficult to remove after 1 week.21 This encouraging Long-term complications
finding is useful when collagen sheet is unavailable or too Color mismatch
expensive to use in certain developing countries. This is probably the commonest long-term complication.
Treated lesions may appear slightly darker or slightly lighter
Factors enhancing repigmentation after MKTP than the surrounding skin. It was reported in several studies
A few solar exposures lead to coalescence of pigmented areas in varying percentages ranging from 5%–20%3–5,15,18,26,33,34,43
in the earliest description of MKTP.7 Over the years, several to >50% of cases treated.2,6,9,27,36,40,47
studies used post-transplantation phototherapy5,20,29,30,40,44 or This mismatch improved after 6–8 months in some stud-
sun exposure18,43 to enhance repigmentation. No comparative ies.2,5,9 A degree of mismatch persisted in 64% of lesions
studies were done to confirm this enhancing role; in fact, (36% darker, 28% lighter) 16.5 months after MKTP in one
targeted phototherapy (UVB + UVA) post-grafting did not study, but this did not bother most of the cases (79%).6 Sun
significantly improve the rate or the final repigmentation exposure can have an effect on improving6 or worsening2
outcome at 12-month follow-up when compared to cases the color mismatch as mentioned earlier. In another study,
where it was not used.40 Interestingly, hyperpigmentation was hyperpigmentation was more frequent over the joints
linked to sun exposure recommended by the dermatologist which led the authors to suggest it may be due to frictional
postoperatively in one study in an Indian population,2 while melanosis.35
sun exposure had a significant beneficial effect on color Paul33 linked color mismatch to donor-to-recipient tissue
mismatch in another study performed in Belgium.6 This ratio. He noticed that hyperpigmentation occurred in cases
is probably related to skin type as darker skin types have where a larger donor area (<1:5 ratio) was harvested while
a higher tendency of tanning. More studies are needed to hypopigmentation affected cases in which the donor-to-
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recipient ratio was more than 1:10. A similar observation was of melanocytes from the repigmented epidermis.56 Similar
reported by Sahni et al18 where hypopigmentation was found improvement was reported by other authors.18,27
in 1/13 treated cases in whom a large donor-to-recipient ratio Details about patients’ data and technique used in cited
of 1:10 was used. papers are included in Table S1.
Hypopigmented halo Recommendation for a successful MKTP

A rim of hypopigmentation at the edges of the lesion was Success in MKTP is achieved by fulfilling certain criteria
reported in 6%–25% of cases in several studies. 3,27,33,41 with 12-month stability being its cornerstone. In our opinion,
Extending the dermabrasion 2–3 mm into normal skin a minigrafting test is essential to predict the response to
decreased the occurrence of this complication.33 MKTP and should be routinely done in all cases because a
clear-cut objective method of ensuring disease stability is still
unavailable. The site and size of the lesions are influential
Scars or textural change
factors too. Some sites such as the face, trunk and limbs
Textural changes or scar may occur at the donor site,6,29,45,52
are easier to resurface with ability to secure the dressings
and therefore, tissue should be harvested from a relatively
used postoperatively. Technique adjustments are needed at
concealed area over the thigh or buttocks.
other sites such as delicate skin of eyelids or genitals where
gentle resurfacing is needed as opposed to thick acral skin
Stability of acquired pigmentation or skin overlying the joints where aggressive resurfacing is
A few long-term follow-up studies have emerged which mandatory. Lesions over the fingers remain a challenge; the
gave a clear idea about stability of repigmentation achieved authors are dedicating research focusing on the best option
following MKTP. Excellent retention of acquired repigmen- especially in periangual lesions; cryoblebbing seems to give
tation was found in cases of SV on long-term follow-up.3,6 hope and splints using a tongue depressor are a simple way of
Repigmentation was maintained in 19/23 (83%) treated cases limiting movement. The procedure is more suited to patients
after 5 years of follow-up in one study.40 In GV, the major- with limited extent of vitiligo, while cases with extensive
ity of cases retain acquired repigmentation. However, some lesions involving >30% of the body surface area are less
GV cases may lose some of this repigmentation especially likely to respond.
if disease activity occurs. This was reported in 4%,4 16%,6 The tissue harvested for suspension preparation is another
11%40 and 21% of cases27 in long-term follow-up studies. variable to consider. Keeping the ratio of donor to recipient
It is therefore essential to inform these patients clearly that areas around 1:3 or 1:5 when feasible increases the cell count/
MKTP is not a cure for vitiligo and does not prevent new mm2 improving the response. Exposing the donor area to
lesions from appearing in the future in order to avoid patient ultraviolet rays a few weeks before grafting was found to
frustration. significantly increase the melanocytic count in NSV cases
Improvement of repigmentation continued for a mean (unpublished data, Bassiouny et al, 2017) which can further
period of 10 months in one study.6 More pigmentation was boost the response. Finally, the use of mixed suspension
reported in 67% and 62% of treated areas in SV and NSV (NCES and ORSHFS) may be beneficial in acral skin. Postop-
cases, respectively, during 12–24 months of follow-up.27 erative wound dressing and phototherapy are also important
This increase was significant in SV cases. These data are and are still fresh fields for exploring.
very useful since patients sometimes require a second ses- Most of the SV cases achieve an excellent response to
sion of MKTP to achieve full repigmentation. It would be MKTP because they possess many good prognostic factors,
therefore wise to wait for several months for full response namely long periods of disease stability and small-sized
to be judged. lesions located over the face. Paying special attention to
Finally, patients are sometimes concerned about associ- details of the technique can improve the response in NSV
ated leucotrichia. An interesting retrospective study found even in difficult-to-treat areas. Knowing what to predict
that >90% repigmentation of hair occurred in 58% (10/17), and how to handle each case allows for successful outcome
28% (2/7) and 12% (2/16) of lesions over the trunk, scalp and and realistic expectations (Figure 2). MKTP is an effective
face, respectively, after MKTP.55 The authors noticed that the method of treatment in stable cases of vitiligo which produces
skin repigmented first followed by hair repigmentation after long-lasting repigmentation with very good color matching
a lag period which was attributed to retrograde migration offering a beam of hope for vitiligo patients.
9
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Figure 2 How to proceed in a case of vitiligo resistant to medical therapy in whom MKTP is considered?
Abbreviations: BSA, body surface area; MKTP, melanocyte–keratinocyte transplantation procedure.
Disclosure 12. Vanscheidt W, Hunziker T. Repigmentation by outer-root-sheath-derived

melanocytes: proof of concept in vitiligo and leucoderma. Dermatology.
The authors report no conflicts of interest in this work. 2009;218(4):342–343.
13. Mohanty S, Kumar A, Dhawan J, Sreenivas V, Gupta S. Noncultured
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based review. Br J Dermatol. 2013;169(Suppl 3):S57–S66. 14. Kumar A, Gupta S, Mohanty S, Bhargava B, Airan B. Stem Cell Niche
2. Mulekar SV. Melanocyte-keratinocyte cell transplantation for stable is Partially Lost during Follicular Plucking: A Preliminary Pilot Study.
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3. Mulekar SV. Long-term follow-up study of segmental and focal vitiligo 15. Razmi TM, Parsad D, Kumaran SM. Combined epidermal and follicular
treated by autologous, noncultured melanocyte-keratinocyte cell trans- cell suspension as a novel surgical approach for acral vitiligo. J Am Acad
plantation. Arch Dermatol. 2004;140(10):1211–1215. Dermatol. 2017;76(3):564–567.
4. Mulekar SV. Long-term follow-up study of 142 patients with vitiligo 16. Razmi TM, Kumar R, Rani S, Kumaran SM, Tanwar S, Parsad D.
vulgaris treated by autologous, non-cultured melanocyte-keratinocyte Combination of Follicular and Epidermal Cell Suspension as a Novel
cell transplantation. Int J Dermatol. 2005;44(10):841–845. Surgical Approach in Difficult-to-Treat Vitiligo: A Randomized Clinical
5. van Geel N, Ongenae K, de Mil M, Haeghen YV, Vervaet C, Naeyaert Trial. JAMA Dermatol. 2018;154(3):301.
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vitiligo: a pilot study. Dermatol Surg. 2001;27(10):873–876. Prospective comparison of recipient-site preparation with fractional
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Noncultured Epidermal Suspension Grafting in Patients With Vitiligo. phenomenon with disease activity and therapeutic responsiveness in
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histological findings are potential indicators of activity in lesions of cultured melanocytes transplantation and non-cultured epidermal cell
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of patients presenting with vitiligo have a clinical sign of activity. J Am 40. Gan EY, Kong YL, Tan WD, Thng ST, Goh BK. Twelve-month and
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36. Singh C, Parsad D, Kanwar AJ, Dogra S, Kumar R. Comparison between 53. Lommerts JE, Meesters AA, Komen L, et al. Autologous cell suspension
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11
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Supplementary material
Table S1 Details of prospective and retrospective MKTP studies
Authors No. of cases/ Vitiligo Skin type Age Technique Area (cm2)
Study design no. of lesions type
D:R ratio R Suspension
Gauthier and 12 SV: 3 Not stated 20–65 D: ≥2 cm2 Cryo Cold trypsin 4–50
Surleve-Bazeille1 NSV, all R: ≤50 cm2 Saline
Prospective focal: 8
Olsson and Juhlin2 20 SV: 3 Not stated 13–52 1:4–10 DermA Mel medium 7–194
Prospective NSV:17 Collagen film
van Geel et al3 4 SV: 2 III: 2 30–52 1:2–4 CO2 laser Hyal A 36–110
Prospective pilot NSV: 2 IV: 2 Mel medium
study
Olsson and Juhlin4 132 SV: 15 GV: Not stated 12–61 CES: 8 cm2 DermA Collagen dressing or CES: 60–500
Retrospective CES: 5 107 Focal: 2 NCES: 10 cm2 silicone netting EpS and
EpS: 1 NCES: not
NCES: 8 stated
Muleker5 184 SV: 43 Not stated 12–70 1:10 DermA Ordinary incubator Not stated
Prospective GV: 122 Collagen film
Focal: 19
van Geel et al6 28/66 NSV (19 II–IV: 25 15–65 1:1 CO2 laser Hyal A 0.2–8.9
Prospective stable and 9 Mel medium
double blinded active)
placebo
controlled
Mulekar7 64 SV: 49 Not stated >12 1:3–10 DermA DMEM/F12 medium 1–120
Prospective Focal: 15 Collagen film
Mulekar8 142 GV Not stated 18–70 1:10 DermA DMEM/F12 medium 2–298
Prospective Collagen sheet
Pandya et al9 27 SV: 2 Not stated >8 1:10 DermA Supplemented Not stated
Prospective NSV: 25 medium/collagen
controlled dressing
Tegta et al10 20 SV: 4 Not stated 10–54 1:3 vs 1:5 Blister (suction, Injection into blister 6–24
Prospective Two different GV: 11 liquid N2 or from floor
comparative cellular Focal: 5 UVA)
dilutions
Mulekar et al11 49 SV: 9 Not stated 7–65 1:3–10 DermA DMEM/F12 medium Not stated
Prospective NSV: 40 Collagen sheet
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Stability Average % Response according to Follow-up Complications

repigmentation site No. of lesions with (months) *Remarks
≥95% response/total no.
(% pigmentation)
Not stated SV: 92% H&N: 2/4 (90) 3 *1 case of nevus depigmentosus
NSV: 41% Joints: 0/4 (40) showed 80% repigmentation
Extremity: 1/2 (50)
Hands: 0/2 (35)
>1 year SV: 100% H&N: 7/12 (80) 6–12 None mentioned
Except 2 cases NSV: 78.5% Joints: 5/5 (100) *Patient rested 4–5 hours after the
Extremity: 9/12 (82) procedure
Trunk: 4/5 (97)
H&F: 2/5 (72)
>1 year SV: 90% Face: 1/2 (92) 6–20 Color mismatch (disappeared in 5
NSV: 88% Presternal: 0/2 (88) months)
Not stated SV: ≥95% in 14/15 cases (5 CES, 1 H&N: 13/65 12–84 *Halo nevus: 3
EpS, 8 NCES) Joints: 10/78 Pieb: 5
GV: 42% CES, 59% EpS, 49% NCES Extremity: 33/108 All ≥95% response
Focal: 100% in 2 (NCES) Trunk: 11/26
H&F: 14/92
6 months SV: 92% Not stated 12 Color mismatch (darker)
GV: 57% disappeared in 6–8 months
Focal: 68% Relapse in 15 cases (12 NSV, 3 SV)
>1 year vs active Stable: 77 Joints: 5/18 (70) 3–12 Color mismatch (darker): 5/66
Active: 0 Extremity: 1/20 (88) lesions improved in 6 months
(placebo-treated lesions: 20% Trunk: 4/12 (72) *Combined by NB-UVB or PUVA
response in 3 cases) H&F: 0/10 (37)
Fingers: 0/6 (0)
1 year SV: ≥95 in 41/49 H&N: 26/34 12–60 Color mismatch (lighter in 8 cases,
Focal: ≥95 in 11/15 cases Joints: 1/1 darker in 1 case)
Extremity: 6/7 P halo in 4 cases
Trunk: 13/14 New lesions in 2 cases
H&F: 3/3
6 months ≥95 in 80 cases; ≥65 in 15 H&N: 19/49 12–72 Relapse in 15 cases
Joints: 64/119 Color mismatch in 11 cases
Extremity: 54/84 P halo in 6 cases
Trunk: 19/35
H&F: 40/64
Fingers: 12/18
2 years Excellent in 52% NCES vs 50% in 4 H&N: 2/2 6 Infection: 7% of donor, 11% of
CES cases Joints: 1/2 recipient sites
Control patch in 20 cases, no Extremity: 6/17 Koebner donor 1
pigmentation Trunk: 1 *CES: 4 cases (cells <1,000/mm2)
H&F: 4/28
1 year >75% response Not stated 3 Color mismatch: darker in 3 cases,
5/10 cases of 1:3 ratio lighter in 8 cases
0/10 cases of 1:5 ratio *Vitiligo >10% BSA excluded
6 months SV: ≥95% in 3/9 lesions Eyelids: 6/9 6–12 *No trypsin inhibitor. No
NSV: ≥95% in 29/72 lesions Joints: 15/43 immobilization of joints
Areola: 5/6
Fingers and toes: 8/19
Genital: 1/4
(Continued)
13
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Table S1 (Continued)
Study design no. of lesions type D:R ratio R Suspension
Mulekar et al12 25 SV: 13 Not stated 4–16 1:3–10 DermA DMEM/F12 medium 4–123
Retrospective Focal: 12 Collagen sheet
van Geel et al13 87 SV: 33 II, III: 77 9–65 CO2 laser Hyal A Not stated
Retrospective NSV: 33 IV–VI: 10 Mel medium
Mixed: 6
Others: 15
El-Zawahry et al14 25 SV: 2 Not stated 8–45 1:10 Cryo Mel medium Not stated
Prospective NSV: 23 Hyal A
(2 focal)
Toossi et al15 8/14 NSV Not stated 13–43 1:5–10 DermA DMEM/F12 1–7
Prospective Collagen sheet
controlled
Sahni et al16 13/19 SV: 6 Not stated 8–17 1:2–10 DermA PBS 3–200
Prospective GV: 6 Cold trypsin
Focal: 1
Vasquez-Martinez 11 Not stated Not stated 35–48 1:10 DermA DMEM/F12 Not stated
et al32 Collagen dressing
Prospective
comparative
Paul18 49 Not stated Not stated Not 1:5–1:10 DermA Er:YAG DMEM/F12 2–230
Retrospective stated on eyelids Collagen sheets
Mohanty et al19 14 SV: 3 Not stated 17–32 15–25 HF DermA DMEM/F12 4–96
Prospective GV: 8 Collagen dressing
ACF: 3
Huggins et al20 23/29 SV: 2 II–III: 12 18–60 1:10 DermA DMEM/F12 1–116
Prospective GV: 15 IV–VI: 11 Collagen dressing
Focal: 6
Budania et al21 41/54 SV: 16 Not stated 12–40 NCES 1:10 DermA CO2 incubator 3–35
Prospective NCES (21/28) GV: 15 PBS
comparative vs SBEG Focal: 10 Collagen dressing
(20/26)
Holla et al22 36/80 GV: 33 Not stated 16–47 1:10 DermA Cold trypsin Not stated
Retrospective Focal: 3 ±Mel medium, serum
Dovepress

(% pigmentation)
6 months SV: 79% H&N: 12/20 (78) 9–54 New lesions in 5/12 NSV cases
Focal: 85% Joints: 1/1 (100) *General anesthesia and O2 by face
Extremity: 1/1(98) mask
Trunk: 2/2 (98)
H&F: 3/5 (93)
No 77% Genital > extremity, trunk > 11–92 Color mismatch: 80% of cases
Koebnerization SV: 85% dorsum, H&F > H&N > joints (improved by sun exposure)
NSV: 70% 7.9 patient satisfaction score Loss of color: 3/45 NSV cases
Mixed: 37% (activity)
Stable (89%) vs active (48%)
>1 year SV: 60% H&N: 1/4 (46) 6–17 *Distal fingers showed 100%
NSV: 50% Joints: 2/22 (47) repigmentation in 1 case
Extremity: 3/5 (87)
Trunk: 1/9 (43)
H&F: 3/33 (42)
Fingers: 10/10 (100)
>1 year 58% (≥95 in 4 lesions, ≥65 in 1 lesion) Joints: 1/3 4–6 Infection 1 case
6 lesions DermA only: no response Extremity: 1/2
Trunk: 1/1
H&F: 1/2
>1 year >90% responsea >90% response 12 Infection: 1 case
SV: in all cases H&N: 7/8 Color mismatch: 3 lesions
GV: in 8/12 lesions Joints: 4/4 *Combined with sun exposure
Focal: in 1 case Extremity: 1/1
Trunk: 3/3
H&F: 0/2
>1 year No significant difference in area of Trunk: 64% 12 *Image analysis for % repigmentation
repigmentation DermA + NCES vs Extremity: 27%
DermA Face: 9%
1 year 32 cases: >90% Response according to site not 24 Color mismatch: 10 cases (6
9 cases: 70%–89% stated darker), donor darker in 5
4 cases: 30%–69% Relapse in 8 cases (3 lost grafted
4 cases: <30% pigmentation)
P halo: 12
≥1 year: 11 cases SV: 87% H&N: 0/2 (70) 1–15
<1 year: 3 cases GV: 53% Joints: 1/1 (95)
ACF: 80% (79% stable vs 18% active) Trunk: 0/6 (70)
Extremity: 1/2 (93)
H&F: 1/4 (38)
6 months SV: 1/2≥95%, H&N: 3/12 3–6 Color mismatch lighter: 5
GV: 215≥95% Focal: 1/6≥95% Joints: 1/6
Extremity: 1/9
Trunk: 1/5
H&F: 1/6
1 year ≥90% response Not stated but no significant effect 4 Color mismatch darker: 7 lesions (4
NCES: 20/28 of site on response NCES, 3 SBEG)
SBEG: 7/26 lesions NCES higher satisfaction & DLQI lighter: 7 lesions
reduction (2 NCES, 5 SBEG)
>1 year >75 in 51/80 >75% response 6–18 Color mismatch
50–75 in 23/80 Joints: 21/33 *Strict immobilization (sometimes
<50 in 6 (2 ankles, 4 distal fingers) H&F: 22/28 plaster casts)
Fingers/toes: 8/19
(Continued)
15
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Singh et al23 30/54 SV: 11 Not stated 13–35 NCES 1: 10 DermA CO2 incubator 4–48
Prospective NCES (15/24) GV: 15 ORSHFS: PBS
comparative vs ORSHFS Focal: 4 15–25 HF Collagen dressing
(15/23)
Holla et al24 31/42 SV: 16 Not stated 10–38 1:10 DermA Cold trypsin ± Mel Not stated
Retrospective GV: 12 Manual medium, serum
Focal: 3
Verma et al25 25 SV: 2 Not stated Not NCES 1: 10 DermA Collagen dressing Not stated
Prospective CES (6) vs NSV: 20 stated CES
comparative NCES (19) Focal: 3 1: 100
Vinay et al26 30/60 SV: 2 Not stated 8–38 ORSHFS DermA Collagen sheet <100 cm2
Prospective GV: 11
Focal: 17
Komen et al27 10 SV: 5 Not stated 34 1:5 CO2 laser ReCell Kit 27
Prospective Pieb: 5
RCT
Bao et al28 83 SV: 40 Not stated 25 CES 1:20 CO2 laser Vaseline gauze and CES: 40–80
Prospective NSV: 43 NCES 1:5 F12-soaked gauze NCES: 20–40
comparative CES vs using suction SBEG: 2–10
NCES vs blister roof
SBEG SBEG 1:1
Gan et al29 177 SV: 77 III: 2 34±15 1:5 CO2 laser Collagen sheet vs Not stated
Retrospective NSV: 98 IV: 152 Hyal A
Mixed: 2 V: 23
Donaparthi and 11 SV: 1 Not stated 12–42 NCES: 1:10 DermA Collagen sheet 1–64
Chopra30 NSV: 9 ORSHFS:
Prospective Focal: 1 15–25 HF
comparative NCES: 6;
ORSHFS: 5
Shah et al31 20 SV: 3 Not stated 18–43 20–25 HF DermA Collagen dressing Mean: 37
Prospective GV: 8
ACF: 6
Focal: 3
Silpa-Archa et al32 83/200 SV: 43 I–II: 25 9–60 1:10 DermA (CO2 Collagen sheet 2–250
Retrospective NSV: 40 III–IV: 29 laser in 5 cases
V–VI: 29 with large or
delicate sites)
El-Zawahry et al33 37/174 NSV Not stated 13–58 NCES 1:5 CO2 laser vs NCES vs ORSHFS 5–160
Prospective NCES vs ORSHFS: 1 cryo No significant
comparative ORSHFS HF/cm2 No significant difference (P=0.6)
difference
(P=0.3)
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(% pigmentation)
1 year NCES: ≥90 in 20/24 lesions (83%) Not stated but no significant effect 4 Color mismatch: darker 11 lesions
ORSHFS: ≥90 in 15/23 lesions (65%) of site on response (6 NCES, 3 ORSHFS), lighter 6
NCES higher satisfaction, similar lesions (3 in each group)
DLQI reduction
Not stated Not stated improvement according to Leucotrichia improved >90% 6–12 *20 min/day sun
vitiligo type Scalp: 2/7 lesions Methylcobalamine
Face: 2/16 lesions
Body: 10/17 lesions
1 year >70% response Face, lips, trunk and legs better 6 Infection: 1 NCES, 5 CES
≤30% BSA NCES: 62% response than acral and joint lesions Relapse: 2 cases
CES: 52% CES: 100–200/cm2
*Plus PUVA sol
1 year >90% response >90% response 6 Color mismatch: 23/60 darker
SV: 1/3 lesions H&N: 2/8 (38%), 2/60 lighter (3%)
GV: 1/25 lesions Trunk: 0/3
Focal: 8/32 lesions Extremity: 7/31
H&F: 1/18
Not stated Median response: 78% in NCES Not stated 6 Mild textural change in 2 donor sites
0% in CO2 only
0% in control
1 year ≥90% response ≥90% response 12 Color mismatch (darker 22 SBEG)
CES: 55% CES, NCES, SBEG *SBEG significantly better than
NCES: 53% H&N: 24, 22, 30/33 NCES and CES (both comparable)
SBEG: 76% of cases Extremity: 6, 6, 12/24
Trunk: 16, 16, 21/26
1 year SV: 88% of cases ≥50% ≥50% response 12–60 Color mismatch in 56% of cases
NSV: 70% of cases ≥50% H&N: 67/85 Donor darker 14, HTS 8
Mixed: 33% of cases ≥50% Extremity: 15/17 Loss of pigmentation: 11.5%
SV > NSV Trunk: 17/24 (activity)
Stable > active H&F: 9/14 *Plus targeted phototherapy (45%
Collagen > Hyal A of cases)
1 year >75% repigmentation in 90% of NCES Site did not affect response 6 Color mismatch in ORSHFS
vs 43% in ORSHFS 30 lesions/group P halo in NCES
Most of lesions over extremities:
70% in NCES vs 93% ORSHFS
1 year Overall: 80% Sites treated: LL > H&N > trunk > 6 Color mismatch: darker in 75% of
SV: 88% hands > UL cases
NSV: 80% Response according to site not
(>90% in 12/20) stated
6 months >90% response >90% response 12–72 Color mismatch 6% of cases
SV and Focal: 58% H&N: 27/57 P halo in 18% of NSV
NSV: 36% of cases Joints: 15/39 *67% (SV), 62% (NSV) continued
Extremity: 10/17 improvement 12–24 months
Trunk: 5/14
>1 year Overall >90% response 18 NCES: donor site scar in 12/31
≥90%: 6 cases H&N: 2/6 cases
75%–50%:16 cases Joints: 3/39 Cryo: infection in 6/21 and longer
<50%: 15 cases Extremity: 3/5 healing time
Trunk: 1/11 High patient satisfaction in 8/37
H&F: 5/88 cases
Fingers: 10/24
(Continued)
17
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Benzekri and 5 SV: 4 Not stated 20 1:1 Dermaroller (0.2 Cold trypsin 4–10
Gauthier34 Post halo mm) Patient plasma
Prospective pilot nevus: 1
study
Razmi et al40 5/12 GV: 3 Not stated 21–33 ORSHFS and DermA Collagen sheets 6–40
Prospective Focal: 1 NCES mixed
comparative ACF: 1 in a ratio of
1:5 vs NCES
Ramos et al35 20 SV: 12 II, III: 14 10–50 Up to 1:10 DermA Collagen sheet
Prospective GV: 7 IV: 6
ACF: 1
Lommerts et al36 10 SV: 3 Not stated 18–62 1:4 CO2 laser ReCell Kit 16
Prospective Full (2 levels) Pieb: 7
RCT vs FrCO2
Silpa-Archa et al37 6/35 SV: 2 I, II: 2 20–65 1:10 DermA vs Collagen dressing vs 21–204
Comparative GV: 4 IV, V: 4 FrCO2 PG gauze
intrapatient
Kumar et al38 25/54 SV: 8 Not stated 18–36 50 HF DermA DMEM + antibiotic, Not stated
Prospective GV: 5 antifungal
ACF: 12 Collagen dressing
Orouji et al39 300/1,060 SV: 10 Not stated 12–71 1:3–1:10 Intralesional Overnight cold Mean 86
Prospective GV: 231 0.05–0.1 mL, 0.5 incubation dispase II
Focal: 59 cm apart second day trypsin
EDTA
Cells in
saline +10% own
serum
Note: ≥95% not stated in manuscript.
Abbreviations: ACF, acrofacial vitiligo; BSA, body surface area; CES, cultured epidermal suspension; D, donor; DermA, dermabrasion; DLQI, Dermatology Life Quality Index;
EpS, epidermal suspension; FrCO2, fractional carbon dioxide; GV, generalized vitiligo; HF, hair follicle; H&F, hands and feet; H&N, head and neck; Hyal A, hyaluronic acid; LL, lower
limb; MKTP, melanocyte–keratinocyte transplantation procedure; NB-UVB, narrow-band ultraviolet B; NCES, non-cultured epidermal suspension; NSV, non-segmental vitiligo;
ORSHFS, outer root sheath hair follicle suspension; Pieb, piebaldism; P halo, perilesional hypopigmented halo; PUVA, psoralen and ultraviolet A; R, recipient; RCT, randomized
controlled trial; SBEG, suction blister epidermal grafting; SV, segmental vitiligo; UL, upper limb; Mel, melanocytes; PUVA sol, Psoralen plus sun exposure; PG, petrolatum gauze;
HTS, hypertrophic scar; Sol, solar light.
5. Mulekar SV. Melanocyte-keratinocyte cell transplantation for stable

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Dovepress

(% pigmentation)
1 year >75% in 3 cases Face all cases 6 *Plus NB-UVB
26%–50% in 2 cases
Control patch dermaroller only: 2
cases poor response
1 year Combined: 94% (7/6 >90%) Face: 0/2 4 Color mismatch: darker in 1 case
NCES: 78% Extremity: 1/2 only NCES
(1/5 >90%) Trunk: 1/2 lesions
H&F: 3/6 lesions
1 year SV: 72% (4/12 cases ≥90%) H&N: 2/8 (80) 3–12 Color mismatch: 3 cases (2 darker )
NSV: 52% (1/8 cases ≥90%) Joints: 0/4 (50) Koebner donor 1
Extremity: 0/2 (80) *>30% BSA excluded, plus sun
Trunk: 0/5 (53) exposure
H&F: 0/2 (60)
Genitals: 0/1 (0)
1 year Full CO2 at 209 µm: 69% Extremity: 6 cases 6 Color match: 10% darker
Full CO2 at 144 µm: 58% Trunk: 2 cases Scar 2 donor sites
FrCO2 and control: zero% Joints: 2 cases Mild erythema: 70% of 209 vs 50%
Response according to site not 144
stated
1 year >90% response >90% response 3–11 Color mismatch: darker (35%
SV: 2 DermA, 1 FrCO2 H&N: 3/6 FrCO2, 18% dermA)
GV: 3 DermA, 1 FrCO2 Joints: 2/6 P halo: 12% DermA
Extremity: 1/1 Scar: 1 case
H&F: 4/8 *DermA >FrCO2
Dressings similar
1.5 years SV: 41% H&N: 49% better than bony parts 6 Color mismatch: 11/25 (darker)
GV: 69% 39% but not significant (P=0.6) Infection: 4/25
ACF: 45% *Plus phototherapy
1 year >50% response at 12 months in 35% H&N and trunk significantly better 6–30 Pigment loss in 20% of lesions
of lesions than extremities mainly during the first year
GV better than SV Recipient: ecchymosis
Donor: 11% hyperpigmentation
Keloid: 2 cases
Koebner: 6 cases
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dilutions in the treatment of vitiligo. Int J Dermatol. 2006;45(2): vitiligo: a clinical trial in an Iranian population. J Eur Acad Dermatol
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vitiligo: a long-term study of localized vitiligo treated by noncultured et al. Treatment of vitiligo with a melanocyte-keratinocyte cell suspen-
cellular grafting. Pediatr Dermatol. 2010;27(2):132–136. sion versus dermabrasion only: a pilot study with a 12-month follow
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halo naevi, piebaldism and naevus depigmentosus. Br J Dermatol. Suspension Transplantation in Vitiligo: Indian Experience. J Cutan
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14. El-Zawahry BM, Zaki NS, Bassiouny DA, et al. Autologous melano- 19. Mohanty S, Kumar A, Dhawan J, Sreenivas V, Gupta S. Noncultured
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21. Budania A, Parsad D, Kanwar AJ, Dogra S. Comparison between Hair Follicle Outer Root Sheath Cell Suspension for Transplantation
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Autologous non-cultured melanocyte–

Bassiouny and Esmat Dovepress

Clinical, Cosmetic and Investigational Dermatology 2018:11

region using a hand dermatome supplemented with insulin, to increase viscosity

Bassiouny and Esmat Dovepress

Manual dermabrasion Suspension spread and

passed over lesion for

covered with collagen

Figure 1 Clinical signs of disease activity.

Notes: (A) Active disease is characterized by ill-defined borders and hypopigmented

well-defined borders. Note perifollicular repigmentation at the borders of the lesion

respectively. However, a high relapse rate was noted in 15

of those responders. Huggins et al26 achieved ≥95% repig-

mentation in only 4/23 treated cases with 6-month duration

of stability. In a retrospective long-term follow-up study of

sufficient as an inclusion criterion. More than 75% repigmen-

Suspension centrifuged and

cell pellet resuspended in

tation was noted in 71% and 54% of SV and non-segmental

vitiligo (NSV) cases, respectively.27 On the contrary, a higher

percentage of repigmentation was noted in one study where

all three SV and 13/17 NSV cases with 1-year stability

hour, followed by rinsing in PBS

Cold trypsinization followed by

showed stable improvement of their vitiligo had a 78% repig-

mentation in response to different melanocyte transplantation

techniques including MKTP after 4.8 years compared to

cases with unstable vitiligo that showed a 33% repigmenta-

tion after 6.5 years. The authors recommended that patients

with extensive GV and those who have not had completely

stable, non-progressive vitiligo for at least 2 years should not

Superficial skin samples from the

Active disease and the presence of Koebner phenomenon

Each blister: 0.785 cm2. Total

were found to negatively influence treatment results.5,13 Activ-

donor 1/10 of recipient

ity resulted in failure of MKTP suspension in one study5