Accepted: 6 April 2018

DOI: 10.1111/jocd.12666

ORIGINAL CONTRIBUTION

Telomere length and genetic variations affecting telomere

length as biomarkers for facial regeneration with platelet-rich
fibrin based on the low-speed centrifugation concept

Cleopatra Nacopoulos DDS, MSc, PhD1 | Kalliopi Gkouskou MSc, PhD2 |

Dimitrios Karypidis MD, PhD3 | Ioannis Vlastos MD, PhD4 | Anna-Maria Vesala DMD5 |
Joseph Choukroun MD, PhD6 | Richard J Miron DMD, DDS, MSc, PhD7 |
Emmanuel Prokopakis MD, PhD4

1
Dental Aesthetic Clinic, Athens, Greece
2
Embiodiagnostics, Heraklion, Greece
Summary
3
Plastic and Reconstructive Surgery Background: Platelet-Rich Fibrin (PRF), a fibrin matrix produced by single blood
Department of Agioi Anargyroi General centrifugation that contains leukocytes, platelets, and growth factors, is increasingly
Oncological Hospital of Kifisia, Athens and
Plastic Surgery Clinic, Private Practice, being utilized for facial regeneration purposes. However, our understanding of the
Athens, Greece involved pathophysiological mechanisms affecting regeneration is limited and cur-
4
Medical School, University of Crete,
rent protocols require better optimization. Biomarkers that are related to skin aging
Heraklion, Greece
5
Department of Dentoalveolar Surgery,
such as telomere length (TL) have been proposed as a mean to analyze patients’
Implant Surgery and Radiology, Faculty of stratification.
Dentistry, School of Health Sciences,
Aristotle University of Thessaloniki,
Objective: Our aim is to study whether the outcomes of a facial regeneration pro-
Thessaloniki, Greece tocol performed with PRF are related to TL and genetic variations affecting TL. This
6
Private Practice, Pain Therapy Center, can aid in the standardization of a surgical aesthetic protocol.
Nice, France
7 Patients and Methods: In all, 41 patients treated with PRF produced with the low-
Department of Periodontology, School of
Dental Medicine, University of Bern, Bern, speed centrifugation concept were included in this observational study. The correla-
Switzerland
tion between TL and genetic variations were assessed versus treatment outcomes,
Correspondence namely the number of sessions and aesthetic results utilizing the FACE-Q skin satis-
Cleopatra Nacopoulos, Dental Aesthetic
faction questionnaire.
Clinic, Athens, Greece.
Email: cleopatra.nacopoulos@gmail.com Results: In all, 39 of the 41 patients completed the treatment. TL correlated with
the initial responses to FACE-Q (q = .33, P = .05). Genetic variations affecting TL
was related to the change of FACE-Q (q = .35, P = .034) as well as to the number
of treatment sessions (q = .38, P = .019).
Conclusions: Telomere length (TL) was related to patient perceived facial skin
appearance. In addition, genetic variations affecting TL were related to the final out-
comes (number of sessions and improvements of FACE-Q results) and may be a
useful biomarker for future regenerative procedures performed with PRF for facial
regeneration.

KEYWORDS
biomarkers, facial regeneration, platelet-rich fibrin, telomere length

J Cosmet Dermatol. 2018;1–6. wileyonlinelibrary.com/journal/jocd © 2018 Wiley Periodicals, Inc. | 1

2 |
1 | INTRODUCTION
Genetic biomarkers are being routinely investigated in modern medi-
cine as a personalized method that may be utilized to optimize
regenerative protocols. Telomere length (TL) is a well-known indica-
tor of biologic age and a potential biomarker for several conditions.1
Skin aging is a complex process and a wide variety of invasive and
non-invasive protocols and their modifications have been proposed
for facial aesthetics and skin regeneration. However, these treatment
protocols lack standardization. In addition, biomarkers of skin aging
may prove useful tool to investigate the treatment success and the
evaluation of treating protocols.
Autologous concentrations of human platelets, such as platelet-
rich plasma (PRP) and platelet-rich fibrin (PRF), have been used in
aesthetic medicine for dermal stimulation and augmentation.2-5
Facial regeneration utilizing autologous platelet growth factors is
considered a natural approach to restore dermal degeneration in
contrast to exogenous growth factors and biodegradable substances.
Moreover, platelets preparations, apart from their bulking effects as
fillers, release numerous growth factors, cytokines and extracellular
matrix proteins upon their activation, such as fibrin, fibronectin, and
vitronectin, that bind to their specific cellular receptors and enhance
or modify the various intracellular processes that relate to cell prolif-
eration and production of additional extracellular matrix proteins.6
Platelet-rich fibrin (PRF) and platelet-rich plasma (PRP) are the
most commonly employed platelet preparations. There are numerous
studies (observational, in vitro, animal models, and clinical trials) sug-
gesting a tangible effect of both topical and injectable applications
of platelet concentrates on cellular changes and facial regeneration.7
Although platelet preparations are being widely exploited in plastic
surgery, cosmetic medicine, and other medical fields over the past
several years, their process and application protocols are constantly
evolving. For example, very recently, specific changes to PRF proto-
cols namely utilizing the low-speed centrifugation concept (LSCC)
have enhanced the numbers cell content (namely platelets and
leukocytes) and concentrations of growth factor release.8-15 Based
on these recent modifications, it is obvious that PRF application in
the field of facial esthetics requires more standardization especially
with respect to the relative quantity/volume to be utilized as well as
the total number of applications. This is especially true regarding
direct volume replacement, not only because tissue loss is a major
issue in aging face, but also because of the relatively not very well-
studied properties of PRF. For example, PRF based on the low-speed
centrifugation concept may convey additional benefits regarding vol-
ume replacement and other properties.16,17
An association between TL and either skin properties or per-
ceived skin age is not only interesting from a pathophysiologic point
of view but also possible since both skin aging and TL are being
influenced by various heritable and environmental factors.18,19 How-
ever, of greater practical interest may prove a possible association
between TL and patient satisfaction after a facial aesthetic proce-
dure. A correlation between a biomarker such as TL and regenerative
NACOPOULOS ET AL.
outcomes following facial regeneration with PRF is an important step
for the identification of a potential precision aesthetic medical
approach. Therefore, the aim of this study was to investigate a pos-
sible correlation between TL/genetic variations that have been
shown to influence TL, with the patient satisfaction after skin treat-
ment using injectable PRF.
2 | METHODS
In all, 41 otherwise healthy women offered PRF facial regeneration
based on the low-speed centrifugation concept were included in this
observational study. An ethical approval was granted (acknowledg-
ments No 1/26/09/2016), and the patients signed an informed con-
sent prior to their treatment. All patients were treated by the same
experienced physician (CN) using a standard protocol explained
below. More specifically, three sessions of PRF treatments were
offered with 2- to 3-week intervals between each session. A fourth
session was offered in cases, where both the patient and the physi-
cian concurred that an extra session would have a tangible benefit
on the final facial appearance. Two patients ceased treatment and
were excluded from the study; one for financial reasons and the
other due to the level of perceived pain associated with treatment.
In each session, 60 mL of venous blood was collected in 10 mL PRF
tubes (Orange tubes, Process for PRF, Nice, France) and centrifuged
according to the following protocols.
• 40 mL (4 tubes) 5 minutes at 1300 rpm (208 g) that results in
10-11 mL of PRF
• 20 mL (2 tubes) 3 minutes at 700 rpm (60 g) that results in 2 mL
of PRF
using a preprogramed centrifuge with a radius of 110 mm (Process
for PRF, Nice France) producing a total of 12-13 mL PRF of reduced
density. Additional 5 mL of vein blood was collected prior to the
first PRF session for genomic DNA analysis using a PureLink Geno-
mic DNA Mini Kit Assay (Life Technologies), according to the manu-
facturer’s instructions.
PRF produced by the two abovementioned centrifugation proto-
cols is mixed and a full face injection technique is applied. This
means that both endodermal and subdermal injections are utilized in
upper face (temples and zygoatic area), mid face (malar and infra-
orbital), and lower face (nasolabial folds, marionette lines, oral com-
missures, mandible, and pre-jowl sulcus). The technique of injections
is the same (point by point or micropapular); however, the relative
volumes may differ depending on the skin conditions (eg, relatively
greater endodermal injections in thick, dehydrated older faces).
Patient age and their response to the FACE-Q satisfaction with
skin validated questionnaire (FACE-Q)20 was assessed just prior to
the beginning of the first session, 2 weeks after the third session,
and 2 weeks after the fourth session (to those offered a 4th ses-
sion). Mean TL was measured using a quantitative PCR-based
NACOPOULOS ET AL.
technique (Quant Studio 12K real-time PCR system) in all sam-
ples.21,22 This method analyzes the expressed telomere length as a
ratio (T/S) of telomere repeat length (T) to copy number of a single
copy gene (S), within each sample. To standardize across plates, a
standard curve was generated using serially diluted genomic DNA.
Telomere length was reflected by the relative telomere/single copy
gene ratio (T/S) values: T/S ¼ 2DCt ðDCt ¼ Ct telomere
Ct b  globinÞ. Samples were run as triplicates. Additionally, DNA
samples were genotyped for seven single nucleotide polymorphisms
(SNPs) (rs11125529, rs10936599, rs7675998, rs2736100,
rs9420907, rs8105767, and rs755017) using TaqMan Pre-Designed
SNP genotyping assays from Applied Biosystems (ABI, Foster City,
USA). TaqMan genotyping reactions were performed on a Quant
Studio 12K (Applied Biosystems) real-time PCR system with 2 lL of
(10 ng/lL) of genomic DNA following the manufacturer’s instruc-
tions. To assess the impact of these variants on risk of disease and
TL, a multiple SNP risk score analysis was performed as previously
described.23 TL and genetic score results were not available to the
patient nor the physician prior to the end of the treatment. Statisti-
cal analysis was performed using Spearman’s q correlation coeffi-
cients. A P value of .05 or less was considered statistically
significant.
3 | RESULTS
Mean patient age, baseline FACE-Q scores, FACE-Q scores 2 weeks
after the completion of the treatment, as well as the number of ses-
sions requiring PRF facial regeneration are shown in Table 1. Possi-
ble correlations of these parameters with TL and its genetic score
(genetic variations affecting telomere length) are also presented in
Table 1. It was found that TL was related to the initial FACE-Q
results but not following its change after therapy with PRF. Genetic
variations affecting telomere length were related to the change of
FACE-Q following treatment as well as to the number of total regen-
eration sessions.
4 | DISCUSSION
Autologous sources for soft tissue augmentation have been sought
by physicians, especially in the field of aesthetic medicine due to the
possible transient effects associated with foreign materials including
the possibility of granuloma formation and chronic or delayed infec-
tions caused by biodegradable foreign substances.24 Furthermore,
exogenous autologous growth factor safety, especially in relation to
cancer, has not been established. As a result, autologous platelets
products containing growth factors such as platelet-derived growth
factor (PDGF), transforming-growth factor (TGF, especially TGF-b),
vascular endothelial growth factor (VEGF), insulin-like growth factor
(IGF), and epidermal growth factor (EGF), have been studied exten-
sively over the last decade.25 Apart from their direct bulking effects,
platelet concentrates promote angiogenesis and cause an enhanced
| 3
T A B L E 1 Variables of interest and their correlation with TL and
genetic score as calculated by guidelines from the study of genetic
variations affecting telomere length
Telomere
Length Genetic score
(correlation (correlation
coefficient coefficient
/P value) /P value)
Age (mean/SD) 49.7/4.4 .08/.634 .117/.483
Initial FACE-Q 30/3.3 .33/.05 .09/.595
(mean/SD)
FACE-Q change 3(0-4) .04/.791 .35/.034
(median/quartiles)
Number of sessions 3 .05/.753 .38/.019
(median)
Statistically significant results are presented in bold letters.
A weak correlation was found between TL and initial self-estimation of
skin (FACE-Q, skin satisfaction questionnaire), whereas genetic score—as
calculated by seven single nucleotide polymorphisms that are related to
TL—is correlated both with the change in the satisfaction score and the
number of sessions.
production of collagen and fibronectin.26 They have been shown to
retain their chemotactic and/or mitogenic action for various cells
including monocytes, fibroblasts, stem cells (Figure 1; Table 1),
smooth muscle cells, endothelial cells, and keratinocytes.13
In addition, platelet preparations upon their activation release
numerous proteins such as fibrin, fibronectin, and vitronectin that
bind to their specific cellular receptors and enhance or modify the
various intracellular processes that relate to cell proliferation and
production of extracellular matrix proteins.26-28 Moreover, different
preclinical and clinical studies have shown the effect of platelets in
the process of regeneration in hard and soft tissues.15,29 However,
little is known about the role of platelet concentrates in the mecha-
nism of skin regeneration. Depending on the site of application, pla-
telet concentrates can be used in the cosmetic field for the
stimulation of both the superficial dermis and the deep layers of the
skin.2-5 In addition, platelet concentrates can be used as a filler by
being injected into the deep dermis or into the subdermal tissues.
This is done to volumize and reshape the skin in a manner similar to
the techniques commonly used for fillers.6 Thus, as a natural source
of growth factors and an autologous product for soft tissue engi-
neering, platelet preparations are currently being studied for facial
regeneration.
The various platelet preparations have been shown to possess
different properties.7 Typically, dual-speed centrifugation allows for
the isolation of platelet-rich plasma (PRP). In addition to the multiple
centrifugation, this system requires the addition of external anticoag-
ulants. Initially, plasma containing platelets are separated from the
red blood cell layer. Then, a second spin concentrates the platelet
plug by its separation from the platelet-poor plasma.
By contrast, platelet-rich fibrin (PRF), which is considered a sec-
ond-generation platelet concentrate, requires only a single round of
centrifugation in tubes absent of anticoagulants that makes it a fully
4 |
(A)
FIGURE 1 In picture A 10 mL tubes were centrifuged for 5 min at 1300 rpm, whereas in picture B the tubes were centrifuged for 3 min at
700 rpm
autologous system. This method provides an easily applicable tech-
nique in the praxis and results in larger absolute volumes of platelet
concentrates that include plasma and proteins can be achieved
including most notably fibrin. Moreover, a more gradual release of
growth factors has been reported.9,11 In general, differences in plate-
let formulations of PRF can be obtained depending on the time of
centrifugation and the revolution per minute (RPM/relative centrifu-
gal force) resulting in different concentrations of growth factors and
cells.7 As a consequence, different PRF clots and consistencies can
be obtained utilizing these different preparation protocols.
The low-speed centrifugation concept (LSCC) has arisen lately
more attention due to the beneficial properties of the resulted plate-
let concentrates.9,10 By further reducing the time of centrifugation,
PRF may be obtained in a more liquid form that retains the biologic
properties of the initial PRF, thereby allowing for the injection of
these products in minimally invasive procedures.14 Several PRF
preparation protocols have been proposed and are constantly being
modified for treatments such as facial regeneration. In addition, apart
from the variations of platelet preparation protocols, existing differ-
ences in the application procedures: for example, the amount of PRF
that can be utilized, the plane of application, and the number of ses-
sions can further hamper the establishment of an accepted method
of utilizing PRF in the field of facial plastics. A thorough examination
of all these protocols and methods in terms of developing a high-
quality evidence-based medical practice therefore remains necessary.
Precision medicine approaches that involve the utilization of
biomarkers can be of use in the standardization of procedures by
influencing the regenerative choice made by patients or physicians.
Telomere length and especially the genetic variations that influ-
ence TL are both potential candidates to investigate individual
biomarkers.30,31 The present study showed that these biomarkers
are related to validated patient satisfaction questionnaires. Another
interesting factor may be the influence of the genetic polymorphisms
on the total volume of PRF or sessions required to achieve a maxi-
mum satisfactory result.
For many years, it has been well known that telomere length
shortens during chromosome replications; thus, it is strongly related
to cell aging.31 Lately, there has been growing evidence that lifestyle
factors may also affect the health and lifespan of an individual by
affecting telomere length.32 Regarding aesthetic medicine, lifestyle
factors such as western type diets, sedentary life, and smoking
NACOPOULOS ET AL.
(B)
negatively affect skin appearance may also contribute to TL shorten-
ing. This can explain the correlation found between lower facial skin
satisfaction scores and TL.
Since the present study was performed as an observational study,
our initial intention was to examine whether TL is correlated to the
outcomes following a replicative PRF facial regeneration method and
not to identify correlations of TL with the results of various PRF facial
regeneration protocols. Regarding the proposed standardized facial
regeneration protocol here, absolute TL values did not seem to qualify
as a robust prognostic tool or as another simple stratification parame-
ter. On the contrary, genetic variations that influence TL are signifi-
cantly correlated with outcomes, namely patient satisfaction scores
and the number of required treatment sessions.
There are several possible explanations for these findings. TL is
influenced by a number of factors, both genetic and environmen-
tal,33 which can bias the outcomes or, in other words, influence the
results in various often contradictory ways. Moreover, determination
of TL and its associated methodology has inherent difficulties in
quantifying the exact estimation of TL. Despite the fact that the
methodology used in this study is well established and likely the
most commonly utilized technique to determine TL,22 small varia-
tions in TL calculation can influence results reaching statistical signif-
icance in small sample sizes studies that include subjects of a narrow
age distribution.
On the contrary, future research aims to investigate the detection
of single nucleotide polymorphisms (SNPs) detection (determines the
genetic effect on TL) that has been deemed highly accurate, especially
when utilizing a multiplex PCR method. Specificity for the detection of
the seven SNPs is strongly correlated with TL and exceeds 95%. In
addition, SNPs detection is not affected by environmental factors,
such as nutritional intake, smoking habits, psychological situations, and
other lifestyle factors that exert a strong effect on TL. Thereby, future
research aims to investigate whether genetic factors can be utilized as
biomarkers or predictors for regenerative protocols with PRF in vari-
ous fields of medicine including in the field of facial esthetics.
5 | CONCLUSION
The present study showed that telomere length (TL) that is affected
by various environmental and genetic factors is related to patient
NACOPOULOS ET AL.
perceived facial skin appearance. Moreover, genetic variations affect-
ing TL were determined to qualify as potential biomarkers and poten-
tial predictors during various regenerative procedures with PRF. TL
and genetic variations affecting TL can therefore be of potential value
in future studies when facial regeneration is performed with PRF. Fur-
thermore, this biomarker analysis can potentially aid not only in the
understanding of the pathophysiological mechanisms that involve
growth factors, functional and structural proteins and skin aging, but
also possibly in the stratification of patients in the various studies that
are arising on PRF facial regeneration.
ACKNOWLEDGMENTS
An ethical approval was granted by the Ethical and Scientific Com-
mittee of the Plastic and Reconstructive Surgery Department of
Agioi Anargyroi General Oncological Hospital of Kifisia, Athens,
Greece (No 1/26/09/2016).
CONFLICT OF INTEREST
KG is the owner of Embiodiagnostics laboratory that provides a
range of comprehensive genomic services to assist individuals to
reach decisions on diet and lifestyles based on their DNA profile. JC
is the owner of “Process for PRF.” The remaining authors disclose
no conflict of interest.
AUTHOR CONTRIBUTION
CN treated the patients; KG performed the molecular biology experi-
ments; AMV assisted with data recording; CN, KG, IV, and AMV
wrote the initial draft; DK supervised initial patient treatment and
revised the draft; CN, KG, IV, JC, RJM, and EP designed the study;
DK, JC, RJM, and EP revised the draft.
ORCID
Cleopatra Nacopoulos http://orcid.org/0000-0001-7274-0997
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How to cite this article: Nacopoulos C, Gkouskou K,
Karypidis D, et al. Telomere length and genetic variations
affecting telomere length as biomarkers for facial
regeneration with platelet-rich fibrin based on the low-speed
centrifugation concept. J Cosmet Dermatol. 2018;00:1–6.
https://doi.org/10.1111/jocd.12666