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Commentary | Open Access | Volume 3 | Issue 1 | 2022 | DOI No.:
10.46439/stemcell.3.014

MESENCHYMAL STEM CELLS AND PRP COMBINED THERAPY PROMOTES GASTRIC LEAK CLOSURE
FOLLOWING SLEEVE GASTRECTOMY

Enora Lecorgne1*, Imed Ben Amor1,2

1INSERM U1081, IRCAN, Nice Medical School, Nice, France

2The Johns Hopkins University School of Medicine, Pharmacology and Molecular
Sciences, Baltimore, MD 21205, USA

*Corresponding Author:
Enora Lecorgne
INSERM U1081, IRCAN, Nice Medical
School, Nice, France
E-mail:enora.lecorgne@univcotedazur.fr

Received date: May 02, 2022; Accepted date: May 17, 2022

Citation: Lecorgne L, Amor IB. Mesenchymal Stem Cells and PRP combined therapy
promotes gastric leak closure following sleeve gastrectomy. Arch Stem Cell Ther.
2022;3(1):18-22.

Copyright: © 2022 Lecorgne L, et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License,which permits
unrestricted use,distribution, and reproduction in any medium, provided the
original author and source are credited.

 

ABSTRACT

Sleeve gastrectomy is the most common bariatric surgery worldwide. However, such
a surgery caries risk of complications associated with morbidity and mortality.
Gastric leak can occur and represents one of the most severe complications
following sleeve gastrectomy. Since the two last decades, regenerative medicine
has emerged, offering new strategies to face to sleeve gastrectomy
complications. Among these, autologous transplantation of material appears to be
promising. Indeed, platelet rich plasma-based therapy has gained interest in
several fields since it contains many bioactive materials involved in the
hemostatic process. Moreover, mesenchymal stem cells-based approaches appear as
the gold standard strategy as it takes advantage of stem cells plasticity,
renewal and repair of damaged tissue abilities. In this article, we combined
plasma rich platelet with mesenchymal stem cells therapy on obese rat models
that went under gastric leak following sleeve gastrectomy. The data suggest that
this combined therapy appears to be promising since it favors the healing
process. Altogether, it suggests that stem cell therapy combined with plasma
rich platelet may become a new tool in the treatment of gastric leak following
sleeve gastrectomy.

 

KEYWORDS

Sleeve gastrectomy, Gastric leak, Bariatric surgery, Regenerative medicine,
Mesenchymal stem cells, Platelet rich plasma

 

INTRODUCTION

Obesity, defined as an excessive fat accumulation, is growing dramatically over
the world, increasing the risk of morbidity and mortality. According to the
World Health Organization, this disorder affected 13% of the world’s adult
population in 2016 [1]. Different treatments exist for obesity, including
non-surgical (physical activities, diets) and surgical approaches such as
bariatric surgeries, e.g., Roux-en-Y gastric bypass, laparoscopic adjustable
gastric band or sleeve gastrectomy (SG). SG has become the most common bariatric
surgery worldwide and performed in more than 50% of the bariatric surgeries
[2,3]. SG consists in a duodenal switch enabling sustained weight loss. However,
SG carries a risk of complications with an overall morbidity rate of 6% and a
mortality rate under 0.3% [2,4,5]. Among these, gastric leak represents one of
the most severe complications following SG surgery. It occurs between 0.7% and
5% of the cases and is associated to decrease in the quality of life, but also
morbitidy [6,7].

Early diagnosis and gastric leak treatment are necessary to avoid lethal
complication of SG. Gastric leak following SG requires therapeutic management
such as drainage, surgical exploration, endoscopic techniques, total
enteral/parenteral nutrition or application of plugs. Although new treatments of
gastric leak are emerging, chronic leaks or fistula, characterized by a long
healing process, are still reported.

Among the new strategies to face to gastric fistula, regenerative medicine has
emerged in the last two decades. Regenerative medicine consists in repairing
organs or damaged tissue. It encompasses two main strategies to promote
regeneration: cell therapy approach, defined by cell injection into the
circulation of the injured tissue or tissue engineering, combining cells and
biocompatible matrix injection [8]. These strategies rely on autologous
transplantation taking advantage of the patient’s material to favor healing of
damaged tissues.

Among regenerative medicine, Platelet Rich Plasma (PRP)-based therapy has
emerged. PRP is defined as a preparation of platelet concentrates contained in
plasma, obtained from autologous blood. PRP-based therapy has gained interest in
regenerative medicine among several fields such as sport medicine, dental or
maxillofacial surgery or even wound healing since it contains many bioactive
factors [9]. Platelets, stored into granules, are known to be involved in
healing processes through the release of proteins involved in clotting, enabling
hemostatic ability.

Moreover, among autologous transplantation strategies, Mesenchymal Stem Cells
(MSCs) appear as the gold standard strategy as stem cells exhibit plasticity,
renewal and repair damaged tissue capacities [10]. According to the minimum
criteria to define MSCs of the Mesenchymal and Tissue Stem Cell Committee of the
International Society for Cellular Therapy, MSCs have the ability to adhere to
plastic, express some specific surface antigen (i.e. CD105, CD73 and CD90) and
have multipotent differentiation potential into several mesenchymal lineages
including cartilage, bone, tendon, muscle and fat, giving rise to osteoblasts,
adipocytes or chondrocytes [11,12]. Although MSCs can be easily isolated from
different sources, the primary source is the bone marrow [13,14], facilitating
their isolation and making them attractive for regenerative medicine. Since MSCs
are multipotent and self-renewal progenitor cells, in vivo experiments showed
that they can enhance wound-healing process after skin injury through the
secretion of cytokines stimulating angiogenesis upon inflammation [15,16]. Since
2003, the use of autologous MSCs as a therapy for the treatment of human complex
and chronic anal fistula has shown encouraging results with complete closure
[17,18].

Finally, PRP-MSCs combined therapy has been already tested in human for the
treatment of complex recurrent cryptoglandular fistula-in-ano allowing long-term
healing where no post-operatively adverse effect has been reported [19].
However, the effectiveness of a combinational treatment with PRP and MSCs in
gastric leak closure following SG still needs to be investigated.

 

RESULTS

 

In this study, we compared the efficacy of a combination of PRP and MSCs in the
treatment of a gastric fistula after SG in adult male obese Zucker rat model
[20]. Two groups of rats went under SG with an artificial leak. For the
experimental group, a mixture containing PRP and MSCs from a donor rat was
injected on the gastric leak edges first, then a PRP-MSCs solution also
containing calcium chloride was applied in order to form a clotted gel. Indeed,
adding calcium chloride into PRP solution, has been reported to induce platelet
activation facilitating clot formation and stability, without affecting MSC
survival [21,22].

PRP and MSC extraction were achieved from the blood and bone marrow of Zucker
donor rat, respectively. Bone marrowderived MSCs were resuspended with the PRP
solution, then calcium chloride solution was added or not, in order to obtain
the mixtures for cellular therapy. The efficacy on leak closure was evaluated by
comparing stomach histological samples after hematoxylin-eosinsaffron (HES)
staining from the two groups following one, two, three or four weeks after the
SG.

Traditionally, the healing process occurs by steps, all regulated and drove by
different cells, growth factors or cytokines. First, after an injury, platelets
are activated to form a fibrin clot. Then, an increase of permeability promotes
the migration of inflammatory cells (e.g., neutrophils) to the wounded site.
This results in a promoting hemostasis process and epithelial regeneration.
Then, fibroblast proliferation, which produces collagen, leads to the
establishment of granulation tissue. Finally, fiber reorganization and
remodeling, thickening of collagen fibers and wound contractions appear [23-25].
Altogether, these different steps contribute to the regeneration of the tissue.

In our study, we defined three histological characterizations of the samples:
inflammation, fibrosis and mucosae regeneration phases. Inflammation phase was
subdivided into acute, sub-acute or chronic signs of inflammation. Acute signs
were characterized by the presence of a high density of polymorphonuclear
neutrophils. Sub-acute signs were defined by a lower density of
polymorphonuclear neutrophils and higher density of lymphocytes and plasmocytes.
Fibrosis was evaluated and subdivided into no fibrosis, early signs of fibrosis
with cell granulomas, advanced fibrosis or major fibrosis groups. Finally,
mucosae regeneration was analyzed and sorted into no regeneration, early signs
of mucosae renewal, advanced or complete mucosae regeneration phases.

We demonstrated that using regenerative medicine combining PRP and MSCs
significantly promotes tissue regeneration and therefore fistula healing process
providing a closure of the leak site occurring after SG (Figure 1). Indeed, we
showed that cellular therapy has induced early signs of fibrosis and mucosae
regeneration from the first week after SG, whereas none of these signs have been
observed where no therapy has been applied. Moreover, these effects were more
obvious three weeks after the SG where mild signs of fibrosis and complete
mucosae renewal were observed when rats have received PRP-MSCs combination while
only early mucosae regeneration signs were described in a non-treated strategy.
Lastly, the healing process positive effect was significant four weeks after the
SG with major fibrosis and complete mucosae renewal in all rats receiving the
cellular therapy whereas none of the control ones presented complete mucosae
regeneration. Samples anatomopathological examination from all time points
following SG shows that combination of PRP and MSCs promotes faster recovery.
Altogether, these data suggest that PRP-MSCs cellular therapy following
artificial leak after SG significantly favors the healing process.

 



 

Figure 1: Summary chart recapitulating gastric leak healing process after SG
with (B) or without (A) PRP-MSCs cellular therapy. The dot line and the star
represent the SG and the fistula, respectively. 1: neo mucosae with mucosae
renewal signs. 2: intestinal lumen. 3: fibrosis with leak orificeclosure.4:
completely regenerated mucosae. 5: intestinal lumen.

DISCUSSION

Since the two last decades, regenerative medicine is a promising alternative
option in the treatment of a chronic wound. One of the first application of MSCs
in the gastro-enterology field consisted in treating a rectovaginal fistula in
perianal Crohn’s disease where autologous MSC transplantation has been
successfully achieved, resulting in fistula closure [26]. Indeed, MSCs can exert
their regenerative properties through their ability to migrate toward the injury
site where C-X-C motif Chemokine 12 (CXCL12), growth factors such as basic
Fibroblast Growth Factor (bFGF), Insulinlike Growth Factor-1 (IGF-1), Vascular
Endothelial Growth Factor (VEGF), Platelet-Derived Growth Factor (PDGF) or
Transforming Growth Factor-β1 (TGF-β1) appear to be important as homing factors
[27-32].

PRP therapy has several clinical applications such as in dental and
maxillofacial surgery but more recently in a context of traumatic injury for its
regenerative effect on several tissues (e.g. bone, tendon, muscle, cartilage)
[33,34]. Importantly, it has been shown that platelet degranulation provides
growth factors and cytokines such as TGF-β, PDGF, IGF, bFGF and VEGF [35,36].
Furthermore, platelet containing PRP is used in tissue regeneration strategies
where all these factors can activate MSCs promoting angiogenesis, proliferation,
differentiation or stem cell homing, which can in return enhance the healing
process [10,37].

Numerous studies have demonstrated the feasibility of using PRP in order to
activate MSCs in many fields [38,39]. As a matter of fact, it has been shown
that PRP isolated from rats enhances proliferation rates and self-renewal of
MSCs from rat endometrium in vitro, suggesting that such a combination may be
beneficial in a context of infertility treatment [38]. Moreover, other teams
have demonstrated the in vitro synergistic effect of PRP and MSCs where such a
combination promotes tissue regeneration of rats irradiated submandibular
salivary glands [40] or enhances mice myofibroblast proliferation and
differentiation as a therapeutic strategy for skeletal muscle damages [41]. In
this context, autologous formulation derived from patients and combining PRP and
MSCs may have a synergistic effect on tissue regeneration.

However, despite PRP is known to be source of essential growth factors
participating in the healing process, growth factor concentration has to be
taken into consideration as it can affect biological affects in a dose-dependent
manner. Indeed, Cho et al. have demonstrated that PRP induced MSC proliferation
in a dosedependent manner [42]. For that reason, characterizing growth factors
composition and concentration within the PRP could bring new insights
considering PRP activity. In addition, PRP component variability, PRP
concentration, and PRP harvesting methods will need to be standardized in order
to treat patients in the clinic.

Moreover, PRP-MSCs takes advantage of the patient autologous material, where PRP
can be extracted from the peripheral blood sample and MSCs from a bone marrow
puncture, avoiding transplant resection issues.

Then, this strategy appears to be promising despite raising questions concerning
the characterization of the different actors involved into the wound healing
process and molecular pathways mediating beneficial effects of such a therapy.
Indeed, in depth characterization of the cellular and molecular mechanisms
driving PRP-MSCs-induced wound healing response will help to optimize this
innovative technique for the treatment of fistula. In addition, PRP-MSC-based
therapy could also be used in other fields of regenerative therapy including
sport medicine, dental or maxillofacial surgery. While fibrosis is a
non-physiological scarring process, it can affect tissue architecture and reduce
tissue function. Considering that, more research will need to be conducted in
order to characterize the fibrotic tissue after PRP-MSCs treatment and to define
whether or not this fibrosis response became uncontrolled and pathologic.
Understanding the mechanisms driving gastric leak closure after SG may
facilitate to extent this therapy to another range of disease.

Finally, after this study on rats, Debs et al., have reported complete fistula
resolution after SG for two patients that went under PRP-MSCs cellular therapy
injection around the fistula tract [43]. More importantly, complete fistula
resolution have occurred faster with the cellular therapy and without any
adverse effect compared to the recovery time needed for a more common strategy
[43,44].

 

CONCLUSION

 

Managing acute fistulas following SG remains a challenge since actual treatments
require emergency surgical exploration and long-term care treatment regarding
leak closure. Moreover, acute fistula can evolve into chronic leak, requiring
surgical approaches. Unfortunately, this treatment remains problematic since
there is still a high percentage of leakage with very low healing process [45].
Here we show that PRP and MSCs promote tissue regeneration enabling the fistula
closure occurring after SG. In conclusion, it is now getting clear that using
PRP-MSCs-based regeneration medicine is promising for the treatment of gastric
leak after SG. However, more research will need to be conducted to study the
impact of PRPMSCs on the leak closure and also to characterize long term and
potential adverse effects on stomach and surrounding tissues.

 



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