The impact of mesenchymal stem cells on the treatment of long-term non-healing wounds

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I. Horbachevsky Ternopil National Medical University

THE IMPACT OF MESENCHYMAL STEM CELLS ON THE TREATMENT OF LONG-TERM NON-HEALING WOUNDS

Dzhyvak Volodymyr Georgiyovych PhD (Medicine), MD, Assistant Professor Herasimets Yurii Mykhailovych PhD, MD, Associate Professor Lototskyi Viktor Vasyliovych PhD, MD, Associate Professor, Prodan Andrii Mykhailovych PhD, MD, Associate Professor Horishniy Ihor Myroslavovych PhD, MD, Associate Professor Levenets Sofiya Sergiivna PhD, MD, Associate Professor

Ternopil

Abstract

mesenchymal stem cell wound

Chronic wounds pose a significant healthcare burden due to their prolonged healing time, susceptibility to infection, and associated morbidity. Conventional treatment modalities often fail to achieve satisfactory outcomes in these cases, necessitating the exploration of alternative therapeutic approaches. Mesenchymal stem cells (MSCs) have emerged as a promising strategy for the management of long-term non-healing wounds, owing to their unique immunomodulatory, anti-inflammatory, and regenerative properties. This comprehensive review examines the impact of MSC therapy on the treatment of chronic wounds, drawing upon preclinical and clinical studies to elucidate the underlying mechanisms of action and therapeutic efficacy. We discuss the ability of MSCs to modulate the inflammatory response, promote angiogenesis, enhance extracellular matrix remodeling, and stimulate tissue regeneration, all of which are critical processes in wound healing. Additionally, we explore the safety profile of MSC therapy and its potential for improving wound closure rates, reducing woundrelated complications, and enhancing overall patient outcomes. Despite the promising results reported in the literature, several challenges and limitations remain, including variability in study design, cell source heterogeneity, and the need for standardized protocols. Future research directions are also discussed, including the optimization of MSC delivery methods, identification of optimal patient selection criteria, and exploration of combination therapies to augment the therapeutic effects of MSCs. Overall, this review highlights the considerable potential of MSC therapy as a novel and effective approach for the treatment of longterm non-healing wounds, while also underscoring the importance of continued research efforts to further elucidate its clinical utility and optimize treatment strategies.

Keywords: Mesenchymal stem cells (MSCs), Chronic wounds, Wound healing, Regenerative medicine, Inflammation, Standardized protocols

Анотація

Дживак Володимир Георгійович доктор філософії (медицина), асистент кафедри дитячих хвороб з дитячою хірургією, Тернопільський національний медичний університет ім. І. Я. Горбачевського МОЗ України

Герасимець Юрій Михайлович кандидат медичних наук, доцент кафедри хірургії факультету післядипломної освіти, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль,

Лотоцький Віктор Васильович кандидат медичний наук, доцент, завідувач кафедри медицини катастроф та військової медицини, Тернопільський національний медичний університет ім. І. Я. Горбачевського МОЗ України

Продан Андрій Михайловичкандидат медичних наук, доцент кафедри хірургії факультету післядипломної освіти, Тернопільський національний медичний університет імені І.Я. Горбачевського МОЗ України, м. Тернопіль,

Горішній Ігор Мирославович кандидат медичний наук, доцент кафедри дитячих хвороб з дитячою хірургією, Тернопільський національний медичний університет ім. І. Я. Горбачевського МОЗ України

Левенець Софія Сергіївна кандидат медичний наук, доцент кафедри дитячих хвороб з дитячою хірургією, Тернопільський національний медичний університет ім. І. Я. Горбачевського МОЗ України

ВПЛИВ МЕЗЕНХІМАЛЬНИХ СТОВБУРОВИХ КЛІТИН НА ЛІКУВАННЯ РАН, ЩО ДОВГО НЕ ЗАГОЮЮТЬСЯ

Хронічні рани становлять значний тягар для охорони здоров'я через тривалий час загоєння, сприйнятливість до інфекції та пов'язану з цим захворюваність. У цих випадках звичайні методи лікування часто не дають задовільних результатів, що вимагає пошуку альтернативних терапевтичних підходів. Мезенхімальні стовбурові клітини стали багатообіцяючою стратегією для лікування ран, які довго не загоюються, завдяки своїм унікальним імуномодулюючим, протизапальним і регенеративним властивостям. У цьому всебічному огляді розглядається вплив терапії МСК на лікування хронічних ран, спираючись на доклінічні та клінічні дослідження для з'ясування основних механізмів дії та терапевтичної ефективності. Ми обговорюємо здатність МСК модулювати запальну відповідь, сприяти ангіогенезу, посилювати ремоделювання позаклітинного матриксу та стимулювати регенерацію тканин, що є критично важливими процесами в загоєнні ран. Крім того, ми досліджуємо профіль безпеки терапії MSC та її потенціал для покращення показників закриття ран, зменшення ускладнень, пов'язаних із ранами, та покращення загальних результатів для пацієнтів. Незважаючи на багатообіцяючі результати, про які повідомляється в літературі, залишається кілька проблем і обмежень, включаючи варіабельність дизайну дослідження, неоднорідність клітинного джерела та потребу в стандартизованих протоколах. Також обговорюються майбутні напрямки досліджень, включаючи оптимізацію методів доставки МСК, визначення оптимальних критеріїв відбору пацієнтів і дослідження комбінованої терапії для посилення терапевтичних ефектів МСК. Загалом, цей огляд підкреслює значний потенціал терапії МСК як нового та ефективного підходу до лікування довгостроково незагойних ран нижніх кінцівок, а також підкреслює важливість продовження дослідницьких зусиль для подальшого з'ясування клінічної користі та оптимізації стратегії лікування.

Ключові слова: Мезенхімальні стовбурові клітини (МСК), Хронічні рани, Загоєння ран, Регенеративна медицина, Запалення, Стандартизовані протоколи

Statement of the problem

Chronic wounds represent a significant clinical challenge, characterized by prolonged healing times and frequent treatment resistance. These wounds, often resulting from underlying vascular, neuropathic, or metabolic abnormalities, impose substantial morbidity on affected individuals and place a considerable burden on healthcare resources [1,2]. These wounds commonly affect the legs, ankles, and feet, and can result from various underlying conditions such as vascular insufficiency (e.g., peripheral arterial disease), neuropathy (e.g., diabetic neuropathy), pressure injuries (e.g., venous stasis ulcers, diabetic foot ulcers), or a combination of factors [3]. Chronic wounds often exhibit impaired healing processes due to compromised blood flow, decreased tissue oxygenation, inflammation, infection, and impaired cellular responses [4]. Management of chronic wounds requires a comprehensive approach, including addressing underlying comorbidities, optimizing wound care techniques, and sometimes utilizing advanced therapies such as bioengineered skin substitutes, negative pressure wound therapy, or in certain cases, surgical interventions. Failure to effectively manage chronic wounds can lead to complications such as infection, tissue necrosis, osteomyelitis, and may ultimately necessitate limb amputation in severe cases. Despite advancements in wound care modalities, a subset of patients continues to experience non-healing or recalcitrant wounds, leading to debilitating consequences such as infection, limb loss, and impaired mobility. Traditional therapeutic approaches, including wound debridement, topical dressings, and offloading measures, have limitations in addressing the complex pathophysiology of chronic wounds, necessitating the exploration of novel treatment strategies [5].

Mesenchymal stem cells (MSCs) have emerged as a promising therapeutic intervention for long-term non-healing wounds due to their unique regenerative and immunomodulatory properties [6]. These multipotent progenitor cells, derived from various tissue sources such as bone marrow, adipose tissue, and umbilical cord blood, possess the capacity to differentiate into multiple cell lineages, including keratinocytes, fibroblasts, and endothelial cells [7]. Additionally, MSCs exert paracrine effects through the secretion of bioactive factors, including growth factors, cytokines, and extracellular vesicles, which modulate inflammatory responses, promote angiogenesis, and enhance tissue repair processes. Despite the promising potential of MSC therapy, several challenges and knowledge gaps exist that hinder its widespread clinical implementation in the management of chronic wounds. Issues such as optimal cell sourcing, standardization of isolation and expansion protocols, and determination of dosing regimens require further investigation to ensure the safety, efficacy, and reproducibility of MSC-based interventions [8]. Moreover, the heterogeneity of chronic wounds, varying etiologies, and patient-specific factors necessitate tailored approaches to treatment, highlighting the need for personalized medicine strategies in wound care [9].

Furthermore, while preclinical studies and early-phase clinical trials have demonstrated encouraging results regarding the use of MSCs in wound healing, larger-scale randomized controlled trials are warranted to establish robust evidence supporting their efficacy and safety in diverse patient populations. Additionally, cost-effectiveness analyses and long-term outcome assessments are essential to evaluate the economic implications and durability of MSC-based therapies in the context of chronic wound management. While mesenchymal stem cell therapy holds promise as a transformative approach in the treatment of long-term non-healing wounds, several critical issues need to be addressed to realize its full clinical potential [10].

Analysis of the latest research and publications

The issue of long-standing non-healing wounds is an acute one in modern times, so the search for new treatment methods is a topical issue in many scientific papers.

The aim of this article

To review the current literature related to the topic of this work, namely the study of the use of mesenchymal stem cells (MSCs) in the treatment of chronic non-healing wounds. This review article is aimed at systematically analysing current research that highlights the effectiveness and prospects of MSC therapy in the context of healing severe and long-term wounds. By analysing the available literature, the aim is to enrich the understanding of wound healing processes and identify

Presentation of the main material

Long-term wounds are injuries to the skin or tissues that do not heal over a long period of time. Long-term wounds can occur for a variety of reasons, such as trauma, chronic medical conditions (e.g. diabetes, venous or arterial insufficiency), and infection.

These wounds can be difficult to treat due to a number of factors, such as poor blood supply, infection, uncontrolled mechanical stress on the wound, problems with the body's immune response, etc. Treatment of long-term wounds usually requires an individual approach and may include measures such as regular disinfection and bandaging of the wound, the use of special products to accelerate healing (e.g. gels or ointments), and surgical interventions, if necessary. Table 1 provides a brief description of each type of long-term wound, including its cause, characteristics and treatment strategies. It facilitates quick comparison and understanding of the key aspects of each type of wound [11,12,13].

Table 1

Systematic review of types and management of long-term wounds

Mesenchymal stem cell (MSC) therapy is a promising regenerative medicine approach that utilizes multipotent progenitor cells to promote tissue repair and regeneration in various medical conditions. MSCs are a type of adult stem cell found in numerous tissues throughout the body, including bone marrow, adipose tissue, umbilical cord blood, and others [14,15,16]. They possess unique properties that make them attractive candidates for therapeutic use (Table 2):

Table 2

Functional Properties of Mesenchymal Stem Cells

MSC therapy has shown promising results in preclinical studies and earlyphase clinical trials across various medical specialties, including orthopedics, cardiology, neurology, and dermatology. Some of the key applications of MSC therapy include [17,18,19,20] (Table 3):

Table 3

Applications of Mesenchymal Stem Cell Therapy Across Medical Specialties

While MSC therapy offers exciting potential for regenerative medicine, several challenges and considerations exist, including standardization of cell manufacturing processes, optimization of delivery methods, determination of optimal dosing and timing, safety concerns related to tumorigenicity and immunogenicity, and regulatory hurdles [21]. Ongoing research efforts are focused on addressing these challenges and expanding the clinical applications of MSC therapy, with the ultimate goal of improving patient outcomes and quality of life across a wide range of medical conditions [22].

The article Slobodyanyk et al. delves into the intricate domain of chronic wounds, scrutinizing contemporary methodologies in their management predicated upon scholarly sources [23]. It elucidates that chronic wounds are characterized by protracted non-closure, bacterial colonization, and a preponderance of degenerative processes vis-a-vis regenerative mechanisms. A plethora of nomenclature, such as "intractable" or "complex" wounds, has been posited to encapsulate the essence of chronic wounds, emblematic of the heterogeneous interpretations surrounding their conceptualization. Furthermore, the discourse broaches the stratification of chronic wounds predicated upon their surface area, with proponents advocating for stratification ranging from diminutive to voluminous classifications. Additionally, the narrative traverses the realm of mesenchymal stem cell (MSC) therapy in chronic wound management. MSCs, derived from diverse bodily tissues including bone marrow and dermal adipose reservoirs, exhibit multifarious capacities encompassing regenerative propensities and differential potentiality towards diverse cellular lineages contingent upon microenvironmental cues and differentiation signals. The exposition delineates the salient anti-inflammatory and immunomodulatory attributes inherent to MSCs. Empirical investigations underscore the promising efficacy of MSC therapy in chronic wound resolution, attaining favorable outcomes in a substantive cohort of patients. Nonetheless, elucidation of optimal therapeutic regimens and exploration of novel avenues for research remain exigent imperatives. In summation, the exegesis underscores chronic wound management as a profound quandary in contemporary medical praxis, with extant modalities frequently yielding suboptimal outcomes. The burgeoning field of MSC therapy emerges as a beacon of promise, accentuating the imperative for sustained inquiry and innovation in this sphere.

Tronko et al. article show that mesenchymal stem cells (MSCs) possess the remarkable ability to differentiate into chondrocytes, osteoblasts, and adipocytes, making them a promising candidate for therapeutic intervention in a multitude of diseases including diabetes mellitus (DM), Alzheimer's disease, amyotrophic lateral sclerosis, and various others [24]. The clinical application of MSCs offers several advantages, including their immunomodulatory properties, which allow for the utilization of both autologous and allogeneic MSCs with minimal risk of rejection by the host immune system. Additionally, MSCs exert beneficial paracrine effects by secreting a variety of cytokines and growth factors that promote tissue repair and homeostasis. These cells can be sourced from diverse tissues such as the placenta, umbilical cord blood, bone marrow, pancreas, and adipose tissue. The immunomodulatory function of MSCs is further facilitated by the secretion of extracellular vesicles (EVs), which deliver bioactive molecules to recipient cells without inducing adverse effects. MSC-based therapy has demonstrated efficacy in the treatment of type 1 diabetes (T1D) and its complications, with studies indicating their potential to regenerate pancreatic islets and modulate immune responses. Furthermore, MSCs have shown promise in the treatment of type 2 diabetes (T2D) through their ability to differentiate into insulin-producing cells (IPCs) and promote tissue regeneration. The therapeutic potential of MSCs extends to other diseases such as diabetic nephropathy, where MSC transplantation has been shown to attenuate disease progression. Moreover, MSC-derived exosomes (MSC-EXOs) have emerged as a promising avenue for non-cellular therapy, with studies demonstrating their ability to ameliorate diabetes-related complications and enhance tissue regeneration. Overall, authors summary MSCs represent a versatile and potent tool for the treatment of various metabolic and autoimmune disorders, with their immunomodulatory properties and regenerative potential holding significant clinical promise.

The article Summer E. Hanson et al. discusses the challenges posed by chronic wounds in modern medicine and explores the potential of cell therapy, particularly using mesenchymal stem cells (MSCs), as a novel approach to address these wounds [25]. MSCs, which are multipotent adult progenitor cells, are highlighted for their unique immunological properties and regenerative potential. The article reviews preclinical and clinical studies demonstrating the efficacy of MSCs in wound healing and tissue engineering, including their application in aesthetic and reconstructive surgery. It emphasizes the importance of understanding MSC biology and the mechanisms through which they interact with nonhealing wounds. Clinical studies investigating the use of MSCs, particularly bone marrow-derived MSCs, in wound healing are discussed, along with considerations such as wound bed preparation, cell isolation methods, delivery techniques, and the need for standardized protocols and randomized clinical trials. Overall, the article underscores the promising role of MSC-based therapies in addressing the challenges of chronic wounds and advancing the field of plastic and reconstructive surgery.

The article Ji-Ping Zou et al. discusses the challenges posed by chronic wounds in modern medicine and explores the potential of mesenchymal stem cells (MSCs) in healing these wounds. It highlights the growing interest in using MSCs, which have been shown to contribute to tissue repair and regeneration, particularly in nonhealing wounds [26]. The review systematically analyzes recent research in animal models and clinical trials to evaluate the role of MSCs in chronic wound healing. It discusses the various mechanisms through which MSCs could potentially aid in wound healing, including paracrine effects, microvesicles, and cell-to-cell interactions. The article also addresses challenges and considerations in using MSCs clinically, such as cell source, isolation methods, safety concerns, and optimal administration techniques. Despite the promising results observed in animal models and preclinical studies, further research is needed to better understand the biological properties of MSCs and to optimize their clinical application, potentially through combinations with gene therapy or skin engineering techniques. Overall, MSCs represent a promising approach for healing chronic wounds, and future studies should focus on elucidating their mechanisms of action and developing effective therapeutic strategies.

The article Giovanni Marfia et al. discusses the complexity of wound healing and the challenges associated with treating chronic non-healing wounds [27]. It highlights the emerging potential of regenerative medicine, specifically the use of mesenchymal stem cells (MSCs), as a new clinical approach to wound healing. The understanding of molecular mechanisms involved in wound healing has led to the development of various therapies, including the topical administration of growth factors. However, definitive treatments for chronic wounds remain elusive, and research is ongoing to identify optimal wound care strategies based on the efficacy and cost-effectiveness of emerging therapies. They provides an overview of the novel approaches to wound healing using stem cell therapy, with a focus on difficultto-treat wounds associated with conditions such as diabetes and Systemic Sclerosis. It discusses current treatment approaches and highlights recent advances in the field, while also considering future directions for research and clinical applications.Recent advancements in both basic and translational research have brought significant hope to the field of stem cell therapy, particularly in the modulation of stem cell behavior in laboratory settings and the development of targeted clinical applications. Progress in bioengineering and nanotechnology has enabled the precise manipulation of microenvironments, replicating important cues necessary for tissue regeneration. Mesenchymal stem cells (MSCs) have demonstrated the ability to secrete various trophic factors that promote tissue repair through angiogenic, anti-apoptotic, and anti-fibrotic mechanisms. Adipose tissue has emerged as a promising source of multipotent progenitor cells for regenerative therapies due to its clinical relevance and ease of harvest. Experimental studies, both in vitro and in vivo, have shown the efficacy of adipose-derived stem cells (ADSCs) in wound repair and tissue regeneration. However, while these results are promising, they are currently limited to small patient cohorts and require validation in larger, controlled studies. Based on the compelling evidence available, MSCs cell therapy holds promise as a significant strategy for repairing chronic wounds in the near future. Understanding the mechanisms that regulate MSCs' homeostasis, particularly their anti-inflammatory and immunomodulatory effects, has challenged established beliefs regarding their therapeutic mechanisms. However, further studies focused on elucidating the role of adult stem cells in wound healing are necessary to improve the efficacy of this therapy. Moreover, the ability to obtain a final cell product containing viable adipocytes, pre-adipocytes, and stem cells without the need for enzymatic digestion or other manipulations presents an attractive option not only for applications in plastic and reconstructive medicine but also in research and regenerative medicine.

Conclusions

Mesenchymal stem cell therapy presents a promising avenue for the treatment of long-term non-healing wounds. Our review of the existing literature reveals several key findings that underscore the potential efficacy of MSCs in this context. MSCs possess unique immunomodulatory and regenerative properties that make them well-suited for promoting wound healing and tissue repair. Through their ability to regulate inflammation, promote angiogenesis, and stimulate the proliferation and differentiation of local cells, MSCs contribute to the restoration of tissue integrity and function.

Prospects for further research Further research into the therapeutic potential of MSCs for the treatment of long-term non-healing wounds holds promise for improving patient outcomes and addressing unmet clinical needs. By addressing the aforementioned research priorities, we can advance our understanding of MSC biology and optimize their clinical utility in the management of chronic wounds.

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Література

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