Leukocyte and Platelet-Rich Plasma (L-PRP) in Tendon Models: A Systematic Review and Meta-Analysis of <i>in vivo</i>/<i>in vitro</i> Studies

Liu, Xueli; Li, Yulin; Shen, Li; Yan, Maorun

doi:https://doi.org/10.1155/2022/5289145

Evidence-Based Complementary and Alternative Medicine

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Abstract Introduction Results Discussion Limitations Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2022 | Article ID 5289145 | https://doi.org/10.1155/2022/5289145

Leukocyte and Platelet-Rich Plasma (L-PRP) in Tendon Models: A Systematic Review and Meta-Analysis of in vivo/in vitro Studies

Xueli Liu,¹Yulin Li,²Li Shen,¹and Maorun Yan¹

Academic Editor: Romulo Dias Novaes

Received27 Sept 2022

Revised16 Nov 2022

Accepted07 Dec 2022

Published15 Dec 2022

Abstract

Purpose. To perform a systematic review on the application of leukocyte- and platelet-rich plasma (L-PRP) in tendon models by reviewing in vivo/in vitro studies. Methods. The searches were performed via electronic databases including PubMed, Embase, and Cochrane Library up to September 2022 using the following keywords: ((tenocytes OR tendon OR tendinitis OR tendinosis OR tendinopathy OR tendon injury) AND (platelet-rich plasma OR PRP OR autologous conditioned plasma OR leukocyte- and platelet-rich plasma OR L-PRP OR leukocyte-richplatelet-rich plasma Lr-PRP)). Only in vitro and in vivo studies that assessed the potential effects of L-PRP on tendons and/or tenocytes are included in this study. Description of PRP, study design and methods, outcomes measured, and results are extracted from the data. Results. A total of 17 studies (8 in vitro studies and 9 in vivo studies) are included. Thirteen studies (76%) reported leukocyte concentrations of L-PRP. Four studies (24%) reported the commercial kits. In in vitro studies, L-PRP demonstrated increased cell proliferation, cell migration, collagen synthesis, accelerated inflammation, and catabolic response in the short term. In addition, most in vivo studies indicated increased collagen type I content. According to in vivo studies reporting data, L-PRP reduced inflammation response in 71.0% of studies, while it enhanced the histological quality of tendons in 67.0% of studies. All 3 studies reporting data found increased biomechanical properties with L-PRP treatment. Conclusions. Most evidence indicates that L-PRP has some potential effects on tendon healing compared to control. However, it appears that L-PRP works depending on the biological status of the damaged tendon. At an early stage, L-PRP may accelerate tendon healing, but at a later stage, it could be detrimental.

1. Introduction

Tendons, tight connective tissues, connect muscles and bones and transmit forces from the muscles to the bones, allowing the joint to move [1, 2]. Therefore, the tendon bears heavy mechanical loads and is prone to injury, which can affect tendon function [3]. Tendon diseases are common clinical diseases, mostly in athletes and inactive people, which constitute about approximately 30–50% percent of all sports injuries [4].

Nowadays, platelet-rich plasma (PRP) has gained a lot of interest in the treatment of tendon injuries [5]. PRP is a platelet concentrate obtained from whole blood through centrifugation [6]. A large body of literature suggests that PRP may have multiple potentials for tendon repair and regeneration because they store and release extensive growth factors, such as transforming growth factor-β (TGF-β), platelet-derived growth factor (PDGF), vascular endothelial growth factor (VEGF), and basic fibroblast growth factor (bFGF), insulin-like growth factor (IGF) [7, 8]. These growth factors are secreted by the dense granules, α-granules, and lysosomes in platelets [7, 8]. In addition to growth factors, other components including plasma, leukocytes, and residual erythrocytes also contain and/or release quite a few bioactive factors [7].

Although several studies have reported favorable therapeutic outcomes with PRP, some studies have shown less favorable results. These conflicting results are mainly ascribed to the different PRP preparation methods. A recent study investigated the cellular components of PRP and found significant differences in leukocyte concentrations between PRP preparations contrasted to platelets and fibrinogen [9]. According to whether they had more or fewer leukocytes than autologous blood, PRP can be divided into leukocyte- and PRP (L-PRP) and pure PRP (P-PRP) [10–14]. Moreover, the concentration and components of leukocytes have a significant effect on the function of PRP [15]. Most of the past research has not identified the specific components of PRP; however, because of the controversy over the therapeutic effect of PRP, a growing number of studies have identified the type of PRP based on whether it contains leukocytes or not [10, 13, 14, 16].

A systematic review will be conducted to determine if the delivery of L-PRP has promoted tendon healing in terms of methodology and reporting of the outcome. The mechanism of action of L-PRP and its efficacy in treating tendon injury will be studied in more detail and will ultimately demonstrate some benefits of L-PRP for tendon disorders in vitro and in vivo.

2. Method

2.1. Literature Search

We performed this literature review of in vivo/in vitro studies through foreign databases including PubMed, Embase, and Cochrane Library up to September 2022. The search terms were a combination of medical subject heading (MeSH) terms and their synonyms. The search query used was as follows: ((tenocytes OR tendon OR tendinosis OR tendinitis OR tendinopathy OR tendon injury) AND (platelet-rich plasma OR PRP OR autologous conditioned plasma OR leukocyte- and platelet-rich plasma OR L-PRP OR leukocyte-richplatelet-rich plasma OR Lr-PRP)).

2.2. Exclusion and Inclusion Criteria

Only in vitro and in vivo studies that assessed the potential effects of L-PRP on tendons and/or tenocytes are included in our review. We carefully reviewed the specific methodology of each included study, especially to accurately determine leukocyte concentration in the final PRP product used for tendon injection. L-PRP was characterized as PRP with a leukocyte concentration exceeding that of whole blood, whereas P-PRP was defined as PRP with a lower leukocyte concentration than that of whole blood [10–14]. When insufficient information was provided in the article, the study authors were contacted to acquire leukocyte concentrations. If the study authors did not record leukocyte concentrations, the manufacture’s documentation of the PRP system they used was consulted to extract details about it. At the same time, according to the relevant literature analysis of PRP systems, it was decided which PRP system can produce L-PRP and included in this study, such as the Mini GPS III system, Smart PreP autologous platelet concentrate system, and platelet concentration collection system (PCCS), whereas the Arthrex autologous conditioned plasma double-syringe system, the Selphyl system, and the Endoret systems are known to produce leukocyte-poor PRP [15, 17–21]. With these methods, all formulations can be clearly classified into either class L or class P. Articles of undefined types of PRP and only P-PRP were excluded.

Of the studies that included additional therapeutic variables, only those trials that compared L-PRP directly to the control group (no treatment, saline solution, or control cell medium) were evaluated.

The study excluded randomized controlled trials and case studies. Only English-language studies published in peer-reviewed journals were considered.

Two authors (YLL and MRY) searched separately, determined articles based on inclusion and exclusion criteria, and completed the PRISMA guidelines (Figure 1). Studies that met the criteria were cross-checked and included. In case of discrepancies, discussions and decisions were made by the senior researcher.

2.3. Data Extraction

Two authors extracted the article data and developed a standardized data table. Data collected included descriptions of PRP, study design and methods, outcomes measured, and results.

In vitro studies were analyzed for cell proliferation, cell migration, cell differentiation, the content of collagen types I and III, inflammatory mediation, and catabolic response. In vivo studies were analyzed for signal intensity in magnetic resonance imaging (MRI), collagen fibril diameters, histologic assessment of tendon repair, angiogenesis, inflammatory mediation, the content of collagen types I and III, cross-sectional area (CSA), lesion percent of the involved tendon, and biomechanical testing.

3. Results

3.1. Literature Search

In total, 740 articles were found through electronic searches; after removing 217 replicates, the remaining 523 related articles were analyzed and their titles and abstracts were screened, 443 articles were excluded due to the lack of adequate coverage of topics of interest. After full-text assessment, 63 additional articles were excluded because they did not meet the inclusion criteria (Figure 1). Thus, in total, 17 articles are included in this study. Of these, 8 are strictly in vitro studies [22–29] (Table 1), and 9 are strictly in vivo studies [30–38] (Table 2).

All included studies described the method of preparing PRP. Among them, thirteen studies (76%) recorded basic cytologic results involving white blood cells (WBC) counts of L-PRP [23–25, 27–31, 34–38]. Four studies (24%) were judged to be L-PRP relying on the commercial kits mentioned above [22, 26, 32, 33].

3.2. In vitro Studies

A total of 8 in vitro studies were conducted, of which 2 examined the effect of L-PRP on tendon stem cells (TSCs) (all two come from rabbits [28, 29]), 3 examined the effect on tendon explants (2 horses [24, 26], 1 human [22]), 1 examined the effect on tendon cell from rats [27], 1 examined the effect on human tendinopathic cells [25], and 1 examined the effect on human tenocytes [23] (Table 1).

Five of the studies stated the effect of L-PRP on cell proliferation, of which 4 studies showed significant increases in TSCs, tendinopathic cells, tenocytes, and tendon cells [23, 25, 27, 29]. In addition, 1 of them demonstrated a significant decrease in TSCs [28] (Table 3).

Only 1 in vitro study reported the influence on cell migration, which illustrated increased cell migration after the application of L-PRP [25].

Less is known about the influence of L-PRP on cell differentiation. Among the eight in vitro studies, 2 reported cell differentiation data, with 1 study demonstrating significant increases in the differentiation of TSCs into active tenocytes [29] and another demonstrating nontenocyte differentiation of TSCs [28].

The effect of L-PRP on collagen types I and III was reported in 7 studies, 6 of which showed significant increases in collagen I and III or collagen I/collagen III ratio [22–24, 26, 28, 29], and only 1 showed a significant decrease [25].

Five of these studies reported the influence of L-PRP on inflammatory mediation, and all 5 studies showed a significant increase [22, 24, 25, 28, 29].

Finally, the catabolic response was also analyzed. 4 of 5 studies reported L-PRP to have significant increases in it [22, 24, 25, 29], and the remaining 1 study demonstrated no difference [26].

3.3. In vivo Studies

In the 9 in vivo studies, the animal models used included 5 rabbits [31, 33, 34, 36, 38], 2 mice [35, 37], 1 rat [32], and 1 horse [30]. Animal models were established by different methods, of which 4 were injured by surgery [30, 32, 35, 37], 3 were established by collagenase injection [34, 36, 38], and 2 were normal tendons [31, 33] (Table 2).

Signal intensity in MRI with L-PRP treatment is analyzed in 3 studies, 2 of the studies demonstrated a significant decrease in T2 mapping signal intensity in MRI [34, 36], while the third study showed no change [38] (Table 4).

Three studies reported data on collagen fibril diameters, and all of them demonstrated significant increases with the use of L-PRP [34, 36, 38].

Six of 9 in vivo studies reported histologic assessment of tendon repair after L-PRP treatment. Four of the studies reported that L-PRP significantly improved the quality of tendon injury tissue [34–37], whereas 2 studies demonstrated no change [32, 38]. Three studies reported data on angiogenesis, with 2 of the studies reporting L-PRP significantly accelerated angiogenesis of tendon, which then gradually decreases with the tendon healing process [35, 37], whereas the third study showed a significant decrease [34].

The effect of inflammatory mediation with L-PRP treatment was most widely researched. Seven of the 9 in vivo studies reported inflammatory mediation. Among them, 5 studies showed a significant decrease [31, 33, 34, 36, 37] (4 of them reported an initial increase, but a decrease over time), and 2 studies showed no difference [32, 38].

The effect of L-PRP on collagen types I and III was also analyzed in a small amount of literature. Three studies reported collagen type I, 2 of which showed a significant increase [34, 36] whereas the third study showed no difference [38]. Meanwhile, 2 studies reported collagen type III, and all of 2 showed a significant decrease [34, 36].

Three studies reported data on the cross-sectional area (CSA) or lesion percent of the involved tendon. Three of them reported CSA, 2 of which showed a significant decrease [34, 36], and 1 showed no difference [38]. Two studies reported lesion percent of the involved tendon, 1 showed a significant decrease [36], and 1 showed no difference [38].

For biomechanical testing, such as failure load, tensile stress, and stiffness, all three studies showed that L-PRP significantly improved biomechanical properties [30, 32, 34].

4. Discussion

Nowadays, the application of PRP has progressed rapidly without a large amount of data to support its safety or clinical efficacy [39]. Although many meta-analyses have reported the clinical role of PRP, the results are still confusing, somewhat favorable, somewhat unhelpful, and somewhat even harmful [13, 14, 40, 41]. Literature on PRP preparation methods as well as platelet concentration and cytology reports are inconsistent. Among them, leukocyte concentration is one of the most vital factors influencing PRP function [13, 15, 24, 40].

In this literature review, we searched basic science articles on the use of L-PRP on tendon disease. Unfortunately, because the number of studies included is too small, data could only be qualitatively analyzed. Further research must be conducted to support our findings in the future.

In in vitro studies, parameters such as cell proliferation, the content of collagen types I and III, catabolic response and inflammatory mediation have generally been used to assess the efficacy of L-PRP treatment for tendon repair, while in in vivo studies, the criteria of evaluation of L-PRP treatment are histologic assessment and inflammatory mediation. Most evidence indicates that L-PRP has several beneficial effects on these parameters compared to control.

Four of 5 in vitro studies reporting cell proliferation showed a significant increase in the proliferative ability of tendon associated cells by L-PRP, and merely one showed a significant decrease. Tendons are rich in collagen, with the most abundant collagen being type I collagen, which accounts for approximately 95% of total collagen. Six of 7 in vitro studies reported collagen type I and III significant increase, and only one showed significant decrease. Meanwhile, in the in vivo studies, 2 of 3 studies that reported collagen type I demonstrated significant increases in the content of collagen type I, with the remaining 1 study showing no difference. Both 2 in vivo studies reported that L-PRP significantly decreases the content of collagen types III. After tendon injury, collagen type I content is down-regulated and the synthesis of type III collagen is enhanced. As the tendon heals, type III collagen gradually converts into collagen type I. Thus, it seems that L-PRP could promote collagen type I synthesis but not collagen type III to facilitate tendon repair in both in vivo and in vitro studies.

Furthermore, all of 3 in vivo studies that reported collagen fibril diameters demonstrated that L-PRP significantly increases collagen fibril diameters. In in vivo studies, 4 of the 6 studies that reported the histological changes of tendons showed a significant increase in the quality of tendon healing by L-PRP, and the other 2 studies reported no difference. Parameters used to assess the quality of tendon histological repair include better fiber structure and arrangement, less cell density, less angiogenesis, and less inflammation.

Four of the 5 in vitro studies reported that L-PRP significantly increases catabolic cytokines, such as matrix metalloproteinases-9/11 (MMP-1/9). MMPs are zinc endopeptidases that regulate the extracellular matrix components, which may inhibit matrix formation. Some literature have proposed that L-PRP could have both catabolic and anabolic properties [31, 42]. Nevertheless, this function appears to be time-dependent as there is less benefit in delaying L-PRP administration after the early injury.

All the 5 in vitro studies reporting inflammatory mediation revealed that L-PRP significantly exacerbates inflammation in a short time. However, 5 of 7 in vivo studies demonstrated that L-PRP significantly decreases inflammation, 4 of which showed a short term increase but a long-term decrease while the other 2 studies showed no difference. Consistent with inflammation mediation, 2 of 3 in vivo studies reported that L-PRP significantly decrease signal intensity in MRI in T2 mapping, which means a decrease in local inflammation. It is worth noting that in these two works of literature, animal tendon injury models were established by injection of collagenase, and L-PRP treatment was applied 1 week after collagenase injection, which is generally considered to be the acute stage of tendon injury or the early stage of tendinopathy. However, when L-PRP treatment was applied 4 weeks after collagenase injection (usually considered to be later stageof tendon injury), there were no significant inflammation changes observed by both MRI T2 mapping and inflammatory mediation in histology. Interestingly, this is consistent with the histologic assessment of tendon repair. The application of L-PRP to the early phase of collagenase injection improved the histology results, while there was no difference when applied to the later phase of collagenase injection. It demonstrates that the effects of L-PRP are multifactorial, and the timing of application may alter its anti-inflammatory capacity and overall efficacy.

Inflammation is an essential process for tendon healing, and leukocytes contained in L-PRP are instrumental. During the inflammatory phase, inflammatory cells such as neutrophils, monocytes, and macrophages migrate to the damaged tissue and remove necrotic material by phagocytosis [43–45]. Several studies have shown that early administration of L-PRP accelerates the repair of tendinopathy in rabbits more than late administration, suggesting that L-PRP may promote inflammation in the early stage to accelerate tendon healing, while the beneficial effect of L-PRP in the late stage of tendon lesion was not obvious [29, 34, 36, 38].

Finally, for tendon function, all 3 in vivo studies demonstrated improved biomechanical testing, such as the failure load, stiffness, and ultimate tendon stress, meaning that L-PRP improves tendon outcomes and allows the tendon to return to life and exercise earlier.

5. Limitations

In this study, the lack of uniform methodology and reporting of results was the major limitation for more detailed and in-depth analysis and comparison, as previously described. This study also lacked a risk of bias assessment for the included studies. However, there is currently no effective tool to assess the existence of bias in basic scientific research. A tool that could provide a more objective assessment of our topic should be available to evaluate the quality and bias risks of these basic scientific studies.

In vivo and in vitro studies also have some inherent limitations. For in vivo studies, tendon injuries in animals are distinctly different from those in humans. In animals, the lesions are usually small, and the tendon thickness is thinner. In addition, animal models with surgical incisions or injections of collagenase cannot truly mimic clinical human tendon disease.

Because of these limitations, it is hard to apply our findings to the clinic. However, basic scientific research remains essential to evaluate the efficacy and mechanisms of L-PRP for tendon therapy.

6. Conclusions

In this review of the literature, it was found that L-PRP is beneficial to these parameters in comparison with controls, including angiogenesis, collagen synthesis, inflammation, and biomechanical property. It appears that L-PRP works depending on the biological status of the damaged tendon. At an early stage, L-PRP may accelerate tendon healing, but at a later stage, it could be detrimental. Furthermore, study methodology, including the timing of PRP administration, is not standardized across studies, which hinders comparisons of the efficacy of L-PRP.

For a better understanding of L-PRP’s role in tendon pathology, more rigorous controlled experiments and consistent evaluation criteria must be set up in future basic scientific and clinical studies.

Data Availability

All data generated or analyzed during this study are included in this article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

XLL, MRY, and YLL searched the articles and analyzed the data. XLL and LS designed and wrote the study. All authors read and approved the paper.

Acknowledgments

This research was supported by the Scientific Research Project of the Zigong Health Committee (21zd001).

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Copyright © 2022 Xueli Liu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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