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MODERN POSSIBILITIES OF THE USE OF STROMAL-VASCULAR FRACTION OF ADIPOSE TISSUE IN TRAUMATOLOGY AND ORTHOPEDICS
Miromanov A.M., Miromanov M.M., Miromanova N.A.
Chita State Medical Academy, Chita, Russia
Over the last
centuries of practice in traumatology, some various conservative and surgical
techniques for treatment of locomotor system abnormalities have been developed,
as well as techniques for stimulation of reparative regeneration of tissues.
Despite of various medical technologies, the problem of fast and complete
restoration of bones, cartilages and other tissues is still actual. During the
last years, the important topic is research of influence of stem cells (SC) on
the processes of tissue regeneration [43].
Objective – to reveal the possibilities of the mesenchymal
multipotent adipose tissue cells, to compare their osteogenic and chondrogenic
differentiation with the stem cells of the bone marrow, and also to outline the
boundaries of their use in traumatology and orthopedics.
Human stem cells have become the attractive candidates
for cellular therapy promoting the lost functions of cells and tissues. These
unique cells can self-update endlessly and differentiate into other tissues [6,
13, 25]. The use of the potential of these pluripotent stem cells can offer
other variants of therapeutic treatment of various diseases. From the moment of
primary creation of SC lines in 1998, some great advances have been achieved in
better understanding of stem cell biology
and of requirements for pluripotency maintenance [42].
Confirmation of the first clinical tests of SC for
treatment of spinal cord injuries and macular degeneration in 2010 has marked
the new era in regenerative medicine [37].
When studying the fat tissue as one of the main
sources of stems cells, some scientists gave their attention to
stromal-vascular fraction used as the physiological regenerative substrate [24.
40].
This fraction promoted the provision of tissue
homeostasis and influenced on regeneration of bone, cartilaginous and other
tissues by means of an ability to self-update and differentiate in several
lines. The main component is multipotent mesenchimal stromal cells (MSCs) of
perivascular location [22, 29]. These cells can differentiate into various
tissues by means of inductors and microenvironment of the cell – “the specific niche”
[44, 45].
The bone marrow substance was considered as the source
of multipotent cells over the long time. However in 2001, Zul et al. described
the new adipose tissue-derived stem cells (ADSCs) after the procedure of liposuction
[50]. The liposuction tissue is prepared with collagenase with subsequent centrifugation
to get the packed cells on the bottom of the test tube. The packed cells are
presented by so-called stromal vascular fraction. Actually, ADSCs present the heterogenous cellular population of red
blood cells, fibroblasts, endothelial cells, smooth muscular cells, perithelial
cells and adipose tissue stromal stem cells which show the plastic adhesive
properties. After cultivation of ADSCs in vitro, the cell population
becomes homogenous over time, and is mainly presented by ADSCs [20].
Multipotent mesenchymal stromal cells of adipose tissue stromal—vascular
fraction also demonstrate the ability to differentiate into adipocytes,
osteoblasts, chondrocytes and myocytes. Moreover, the liposuction procedure is
simple, more comfortable and is associated with lower amount of complications
[12].
ADSCs are easier to derive since they are located near
the periendothelial region of vessels, and the adipose tissue with high amount
of vessels is still considered as the most common and available source of these
cells, whereas bone marrow stem cells (BMSCs) are located in deep bone
structures. The amount of ADSCs is higher than cells derived from bone marrow since
the bone marrow aspirates give 6 × 106 of nucleated cells per ml on
average, and stem cells – only 0.001-0.01 %. Conversely, 2 × 106 of
cells can be derived from 1 g of adipose tissue, and 10 % of cells are
considered as stem cells. This feature of ADSCs means the good source of cells
for clinical administration. For example, 10 ml of bone marrow aspirates of an
adult patient with only 6 × 103 – 6 × 104 of stem cells
mean the insufficient cell population for clinical use. However about
1,000-2,000 cm3 of lipoaspirate can contain about 2 × 108
– 4 × 108 of stem cells in a patient without discomfort or
complications. Such amount of SCs is sufficient for restoration of a small bone
defect. An extensive passage in vitro for receive of adequate amount of cells
is usually required for BMSCs, but not for ADSCs. The disadvantages of long
term passage in vitro are possible contamination, long term labor-dependent and
possible gene mutations during passage. Therefore, stromal-vascular fraction of
adipose tissue can be considered as the most appropriate source of SCs in
comparison with bone marrow [21, 22, 27, 30].
The German surgeon Gustav Neuber (1850-1932) used the
fat tissue for grafting in surgery in 1893. He used the adipose autograft for
correction of the lower boundary of the orbit [34]. Simultaneously, the German
surgeon Eugene Hollaender (1867-1932) offered the mixture of human and mutton
fat to prevent the reabsorption and, as result, complications after grafting
[28]. However the highest amount of such operations were inefficient since the
adipose tissue did not survive to the full degree, and oil cysts appeared in
the region of its extinction, with subsequent transition into the necrosis zone
under influence of microcirculation disorders [36].
Subsequently, Erich Lexer (1867-1937) published a
study of clinical use of fat tissue for correction of posttraumatic deformation
of the face, asymmetry of glandula mammaria and Dupuytren's contracture. He
became one of the first authors who had shown the accuracy of collection of the
allograft for successful survival [19].
After the detailed study of adipose tissue, M. Rodbell
separated it into two fractions: mature adipocytes and stromal-vascular
fraction including fibroblasts, perithelial cells, endothelial cells and pre-adipocytes
[39].
Currently, separation and grafting of the fat
autograft is both possible and safe [46]. Moreover, the valuable experience has
become the estimation of the inductors influencing on differentiation of the
stem cell into other tissues (the table) [2, 4, 5, 7, 17, 21, 48, 50].
Table. The inducing factors influencing on differentiation of multipotent mesenchimal stromal cells of stromal-vascular fraction of adipose tissue in other tissues
|
Author |
Phenotype |
Differentiation |
Differentiation-inducing factors |
|
Gronthos S. еt al. (2001) |
Positive: Negative: |
In vitro: |
Osteogenic: Adipogenic: |
|
Zuk P.A. еt al. (2001) |
Positive: Negative: |
In vitro: |
Osteogenic: Chondrogenic: Myogenic: Neurogenic: |
|
Brzoska M. еt al. (2005) |
Positive: Negative: |
In vitro: |
Epithelial: |
|
Cao Y. еt al. (2005) |
Positive: Negative: |
In
vitro: In vitro, in vivo: |
Osteogenic: Adipogenic: Endothelial: |
|
Astori G at al. (2007) |
Positive: Negative: |
In
vitro: |
Osteogenic: Adipogenic: Chondrogenic: |
Considering the osteogenic differentiation of ADSCs
and BMSCs, one should note the much better characteristics of BMSCs in relation
to development of the bone matrix for future clinical administration. The determinate
drug resistance factor is based on the issue: do ADSCs demonstrate much better
osteogenic potential than BMSCs? If the answer is yes, ADSCs can be undoubtedly
used instead of BMSCs for formation of the bone matrix [3].
In 2001, Zuk P.A. et al. firstly described the
derivation of ADSCs from fat tissue and conducted some experiments for
estimation of the phenotype and multiple potency. In their study, they found
that the activity of alkaline phosphatase was higher in the human osteoinduced
ADSCs than in BMSCs within three weeks of induction, whereas six weeks of
induction caused 35 times higher matrix calcification in ADSCs and 68 times
higher in BMSCs. Moreover, the authors realized the gene expression (specific
osteogenic gene osteocalcin, alfa-1 subunit, Runt-associated transcription
factor 2, osteonectin, osteopontin, bone morphogenic protein-2) of osteoinduced
ADSCs and BMSCs. They showed the efficiency of ADSCs for recovery of both bone
(filling of intraosseous cysts or for acceleration of bone tissue consolidation
after surgery) and cartilaginous tissue [14, 16, 31, 50].
The positive results in treatment of cartilaginous
defects of surfaces of big joints were noted by other researchers. After
introduction of ADSCs into the joint cavity, the examination with magnetic
resonance imaging showed the complete closure of defect by homogenous tissue
with structure similar with cartilaginous tissue after one month. Moreover, the
homeostasis of intraarticular system was noted with fast decrease in the
inflammation factor with subsequent disappearance of pain syndrome [32, 38].
The efficiency of conservative therapy was identified
in a study by Startseva O.I. et al. (2016) who investigated the combined
intraarticular introduction of ADSCs and platelet-enriched fraction of the
blood [39].
ADSCs also are used for recovery of biceps function by
means of remodeling of brachial plexus. This fraction was put onto the nerve
suture. It accelerated the regeneration process and increased the
hyperexpression of neurotrophic factors in the site of the suture [18].
One should note that the great potential of
differentiation into various tissues makes the risk of oncologic predisposition
of this type of cells. According to the authors’ opinion, it was always the stumbling
block for wide use of SCs in medicine. One of few studies of influence of ADSCs
on breast cancer cells (in vitro and in vivo model) showed that ADSCs really
increased the growth of active, but not resting cells of breast cancer cells.
The authors state that extrapolation of these results can suppose the ability
of ADSCs to stimulate breast tissue regeneration, but without influence on
condition of dormant residual cancer cells [49]. A decrease in apoptosis rate
in presence of ADSCs supposes the increasing growth of a tumor in the medium
with ADSCs, despite of absence of increasing formation of timorous vessels
[47].
In the individual mice model, the combined
transplantation of ADSCs and active cells of prostate cancer cause more than
three times increase in the tumor volume in comparison with mice without
administration of ADSCs [33].
Other studies showed that human ADSCs, which were
cultivated with triple negative cellular lines of breast cancer, did not
influence on growth in the culture, but stimulated the metastases in other
organs of mice in vivo. Such effects were not observed in the control group
without ADSCs. One case showed the increase in vascular endothelial growth
factor and density of microvessels. It means the increase in tissue
angiogenesis, which can cause the disorders in the tumor bed [15, 35].
The short review of studies estimating the influence
of MSCs (including human ADSCs) on growth of tumors and metastases indentified
some difficulties in estimation of safety already at the preclinical stage.
Having the data indicating the influence of MSCs on stimulation or alternative
inhibition of tumor growth, the authors concluded that our modern knowledge on
the mechanisms of MSCs influence is still poor, i.e. behavior of the cells is
impossible to predict reliably. The authors note the absence of any signs of
formation and growth of a tumor directly relating to the use of MSCs in all
treated patients [26].
It is evident that subsequent reproducible studies are
required. These studies should minimize the discrepancies in donor tissues,
recipient cells, time of MSCs administration and parameters of monitoring.
However the available findings are probably sufficient to exclude the use of
grafts with ADSCs since there are few data on possible recurrence of tumor and
metastases. Also the disadvantage of ADSCs is their difficult derivation. The
first way is manual derivation with washing in saline with phosphate buffer to
remove the blood cells, with collagenase (for simplification of subsequent
derivation of various types of cells) and centrifugation for production of
sediments including the vascular stroma and stem cells [8, 9, 23], or use of
the special column with unwoven viscose and polyethylene fibers for derivation
of cells of stromal vascular fraction from solutions. In contrast to
centrifugation, this technique precludes the extensive process of hemolysis,
resulting in provision of quality and purity of the derived material [10].
Another technique includes the use of automated equipment which is combined into
the single system to prevent the influence of the human factor on the process.
It decreases the risk of negative influence of external factors and precludes
the microbial contamination [11, 41]. Active mitotic division of the fraction
is initiated after three days. Moreover, the acceleration of this process
requires for condition of physiological hypoxia of the cell, when intracellular
level of oxygen is 5 % [1].
All above-mentioned facts suppose the availability of
big laboratories, but it is impossible for many facilities. Unfortunately, the
use of automated blocks for derivation and selection of SCs will be possible in
the Russian Federation only in 2020. Certainly, this technique is the
perspective direction in traumatology and orthopedics, but it requires for
further extensive researching to decrease the various risks and to successfully
use these findings for increase in efficiency of treatment.
CONCLUSION
Therefore, over the last years, the multiple experimental models of SCs in regeneration of organs and tissues have been developed. SCs show their restorative potential both through direct way of differentiation and through indirect way of influence on the “cellular niche”. The special interest is associated with adipose tissue-derived cells, i.e. stromal-vascular fraction including both mature and multipotent cells. The improvements in the modern technologies and tools have allowed to find and characterize the molecular mechanisms of regeneration of injured tissues. However due to great differential potential it is impossible to make the final conclusion on their clinical efficiency. Moreover, the studies of the differentiation of ADSCs in natural conditions did not find any evident results mainly due to absence of standards for use of this material. Certainly, the main task is creation of standard protocols for derivation, selection and differentiation of this cellular culture that will allow using this technology in traumatology and orthopedics in treatment of abnormal processes.
Information on financing and conflict of interest
The study was conducted without sponsorship. The authors declare the absence of any clear or potential conflicts of interest relating to this article.
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