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Table of Contents
REVIEW ARTICLE
Year : 2021  |  Volume : 11  |  Issue : 1  |  Page : 2-10

Antimicrobial effects of platelet rich fibrin: A systematic review on current evidence of research


1 Department of Periodontics and Implant Dentistry, CSI College of Dental Sciences and Research, Madurai, Tamil Nadu, India
2 Department of Periodontics, Adhiparasakthi Dental College and Hospital, Chennai, Tamil Nadu, India
3 Department of Oral and Maxillofacial Surgery, CSI College of Dental Sciences and Research, Madurai, Tamil Nadu, India

Date of Submission02-Aug-2020
Date of Acceptance06-Jan-2021
Date of Web Publication22-Apr-2021

Correspondence Address:
Dr. V R Balaji
Department of Periodontics and Implant Dentistry, CSI College of Dental Sciences and Research, 129 East Veli Street, Madurai, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jid.jid_66_20

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   Abstract 


Background: Other than releasing a bunch of growth factors and molecules, platelet concentrates (PCs), especially platelet-rich fibrin (PRF) has a potential role in antimicrobial activities. Aim: The aim of this present systematic review was to collect, evaluate, and compare the available evidence regarding the antimicrobial efficacy of all types of PRF and to highlight the underlying mechanisms along with their potential benefits based on their actions, investigated by clinical and in vitro studies. Materials and Methods: Systematic approach was followed in the selection of studies. A detailed search was done in electronic databases such as PUBMED/MEDLINE, GOOGLE SCHOLAR, and SCIENCE DIRECT using specific search items with language restricted to English. All in vitro studies and clinical studies which assessed the antimicrobial activity of PRF alone or along with antibiotics or a type of PRF were included in the study. Other studies which included antimicrobial effects of other forms of PCs such as platelet-rich plasma (PRP), platelet gel, and animal studies were all excluded from the study. Results: After the initial and final screening of articles, only eight met the required criteria, of which seven were in vitro studies and one was a clinical study. All the studies evaluated the efficacy of one or more forms of PRF either against bacterial pathogens or showed inhibition of growth in culture. Conclusion: Based on the systematic review, PRF possesses antimicrobial efficacy against pathogens and the exact mechanism of the antimicrobial efficacy needs further investigation. The enhanced property of PRF against pathogens might be due to the release of platelets and preparation protocols such as lesser time and centrifugal speed. Further, PRF should be considered to be used as local drug delivery system which will be a potential treatment against periodontopathogens in the future.

Keywords: Antimicrobial activity, I-platelet-rich fibrin, local drug delivery, platelet concentrates, platelet-rich fibrin


How to cite this article:
Balaji V R, Thiagarajan RK, Niazi TM, Ulaganathan G, Manikandan D. Antimicrobial effects of platelet rich fibrin: A systematic review on current evidence of research. J Interdiscip Dentistry 2021;11:2-10

How to cite this URL:
Balaji V R, Thiagarajan RK, Niazi TM, Ulaganathan G, Manikandan D. Antimicrobial effects of platelet rich fibrin: A systematic review on current evidence of research. J Interdiscip Dentistry [serial online] 2021 [cited 2021 Nov 29];11:2-10. Available from: https://www.jidonline.com/text.asp?2021/11/1/2/314183




   Clinical Relevance to Interdisciplinary Dentistry Top


PRF being used widely in all fields of dentistry,its mandatory to know the certain properties of PRF such as its antimicrobial activity so that its use can be widely researched


   Introduction Top


Over the years, platelet preparations have gained great popularity in various fields such as dentistry, sports medicine, dermatology, and even in plastic surgery. The reason for widespread usage of these preparations is mainly due to growth factors released and bioactive molecules present in the alpha granules of the platelets, which are released on activation of the platelets, thereby leading to modulation of wound healing and inflammation.

In addition to the regenerative potential, which has been extensively studied and researched, the antimicrobial properties of platelet concentrates (PCs) have also been studied which can be witnessed with an increase in the publication of the same. However, there is very few literature in respect to antimicrobial effects of platelet-rich fibrin (PRF) in oral tissues.

Even though there are various classifications of PCs, the following classification proposed by Choukroun,[1],[2],[3],[4] based on low centrifugation protocol shall be considered in this review. The concept of low speed was proposed by Ghanaati et al.,[5] which led to more number of cells, such as leukocytes.

  1. I-PRF (injectable PRF) – 700 rpm/3 min
  2. I-PRF + (injectable PRF+) – 700 rpm/5 min
  3. A-PRF (L) – A-PRF (LIQUID) – 1300 rpm/5 min
  4. A-PRF (advanced PRF)– 1300 rpm/14 min
  5. A-PRF+ (advanced PRF+) – 1300 rpm/8 min.


The mechanism of antimicrobial effects of PRF is still unclear. Hence, the aim of this present systematic review was to collect, evaluate, and compare the available evidence regarding the antimicrobial efficacy of all types of PRF and to highlight the underlying mechanisms along with their potential benefits based on their actions.


   Materials and Methods Top


A detailed electronic search was performed by two independent authors on electronic databases (PUBMED/MEDLINE, GOOGLE SCHOLAR, and SCIENCE DIRECT), using the following search terms, alone and in combination: “platelet-rich fibrin,” “antimicrobial,” and “antimicrobial effects of PRF” from 1975 to 2020. The language was restricted to English. The authors also checked for references in the selected articles for the search of additional studies.

All available studies (in vitro studies and clinical studies) which assessed the antimicrobial activity of PRF either alone or along with antibiotics or a type of PRF were included in the study. Other studies which included antimicrobial effects of other forms of PCs such as PRP, platelet gel, platelet glue, fibrin gel, fibrin glue, and animal studies were all excluded from the study as they did not fall into the inclusion criteria.

After retrieving the titles and abstracts of all the potential articles by a team of two independent authors, the articles which did not address the inclusion criteria were excluded from the study. When the title nor the abstract gave any relevant information to make a decision, full text of those articles were obtained and if relevant were included, if not were excluded from the study. This was the first stage of screening which led to the second stage where the full text of the studies which fulfilled the inclusion criteria were obtained for data collection and for further quality assessment. The attributes and characteristics of the selected studies were examined and were divided into the following five groups:

  1. PRF incorporated with antibiotics as local drug delivery
  2. PRF along with systemic antibiotic
  3. I-PRF alone and against other PCs
  4. PRF versus other PCs
  5. PRF alone


  1. Based on preparation protocol
  2. Against specific periodontopathogens.



   Results Top


The flow chart was prepared based on the PRISMA guidelines. This flow chart reveals the selection process [Figure 1]. After the review and screening of all the studies, only 12 studies were included in the review. Since one study was not related to oral tissues, it was excluded from the review. Moreover, two studies were excluded as they were systematic reviews and there was one letter to the editor, which was also duly excluded. Hence, after all the screening, only eight studies were included in the review as they fulfilled the criteria set for the review. The articles were selected in a period between 1975 and May 2020 and the selected articles evaluated the antibacterial/antimicrobial effects of various PRF available. Of the eight studies selected, seven were in vitro study and one was a clinical observational study. There was considerable variation in the study design in all the studies and different types of bacteria were tested for antimicrobial efficacy.
Figure 1: Flow chart followed by PRISMA guidelines revealing the selection process

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In Group 1, PRF along with systemic antibiotic administration was included. It is the only clinical study which evaluated the antimicrobial effect of PRF. In the study by Pock et al., antibiotic was taken 1 h before dental implant surgery and leukocyte-PRF (L-PRF) was prepared according to the protocol. The PRF membrane was then subjected to antimicrobial study and assessed for antimicrobial activity. The L-PRF prepared after systemic administration of antibiotics provided a measurable antimicrobial activity for 24 h till 48 h. After 48 h, the antibiotic activity was reduced. This reduced activity was proposed due to smaller size of antibiotic, rapid diffusion of the antibiotics, and also limited binding capacity of the antibiotic. Moreover, the drug used namely amoxicillin has no known affinity to fibrin which can explain the lesser time of the antimicrobial agent. This suggests that the antibiotic has been concentrated more in the plasma and not structurally bound to the matrix of L-PRF [Table 1].
Table 1: Platelet-rich fibrin with systemic administration and as local drug delivery

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Group 2 included PRF which was incorporated with antibiotics and used as a local drug delivery agent. Antibiotics when used as local drug delivery systems can deliver higher concentrations of antibiotics at the local site, usually exceeding more than 1000 fold of its minimal inhibitory concentration (MIC). According to the study by Polak et al., 0.5 ml of the tested antibiotics showed no evidence of interference with PRF formation and this provided higher antimicrobial activity of the PRF. Their study also showed higher concentrations of antibiotics interfered with clot formation and also the integrity of the PRF network. The addition of antibiotics also revealed significant inhibition of both aerobic Staphylococcus aureus and anaerobic Fusobacterium nucleatum growth compared to PRF alone, without a difference between the clot or membrane forms of PRF. In the PRF alone group, there was an inhibition of S. aureus but no effects with F. nucleatum. The antibiotics incorporated into the PRF preserved their activity for at least 4 days, suggesting its use as postsurgical slow-release antibacterial agent. Further, they also showed compression of the clot or without compression along with antibiotics exhibited similar antimicrobial activity. Thus, any form of PRF with antibiotics shall exhibit greater antimicrobial activity when compared with PRF alone [Table 1].

Group 3 included two studies which compared I-PRF alone with other PCs [Table 2]. In one of the studies in this group, Perna et al. evaluated the antimicrobial efficiency I-PRF against other PCs (PRF and PRP) and also assessed the amount of platelets in each concentrates. In this study, it was observed that, when compared to whole blood, I-PRF, PRP, and PRF had 50.3%, 46.4%, and 87% of platelets, respectively. I-PRF had more platelets and it shall release more growth factors compared to other PCs. The antimicrobial efficacy was higher in the I-PRF group, followed by PRF and PRP. In this study, no specific microbes were tested, instead, supragingival plaque samples were taken for culture, and zones of inhibition were assessed.
Table 2: I-platelet-rich fibrin alone and versus other platelet concentrates

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In another study in Group 3, Sharmila et al. evaluated the in vitro antimicrobial and antibiofilm effects of I-PRF against oral pathogenic biofilm-producing Staphylococcus bacteria isolated from patients with dental and oral abscess. The antibacterial activity of I-PRF was determined through broth microdilution as MIC and minimal bactericidal concentration. In order to increase the reliability of the study, the authors have used nonbiofilm forming bacteria (Staphylococcus epidermis) and biofilm-forming bacteria (Staphylococcus aureus). In their study, I-PRF exhibited a wide spectrum of activity against weak, moderate, and strong biofilm-producing Staphylococcus strains, and also there was a significant reduction of biofilm formation by all oral biofilm producers in the presence of I-PRF. It was observed in this study that antimicrobial and antibiofilm activity of I-PRF is probably related to permeability proteins, lactoferrin, defensins, heparin-binding protein, cathelicidins, and phospholipase A2. These molecules interfere with the metabolic activity of bacterial cells, which lead to apoptosis and necrotic stages.

Group 4 also included two in vitro studies which compared PRF with other PCs [Table 3]. PRP, PRF, and I-PRF were compared for their antibacterial effect against Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans in a study by Kour et al. Antibacterial activity was seen with both PRP and PRF, though the zone of inhibition was significantly wider with PRP. In this study, in case of P. gingivalis, similar results were found, with I-PRF having the maximum antibacterial activity followed by PRP, and the least antibacterial activity was shown by PRF. However, the difference was insignificant when comparing I-PRF and PRP. Furthermore, in the case of A. actinomycetemcomitans, PRP showed the maximum antibacterial activity and PRF and I-PRF did not show any significant difference. The higher antimicrobial activity with I-PRF in case of P. gingivalis could be purely due to the higher concentration of platelets and other blood cells such as leukocytes in I-PRF as compared to the other PCs.
Table 3: Platelet-rich fibrin versus other platelet concentrates

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In another in vitro study by Badade et al., who evaluated the antimicrobial activities of PRP and PRF against periodontal disease-associated bacteria, they also observed that PRP was capable of inhibiting P. gingivalis at 3–4 days of incubation and A. actinomycetemcomitans at 48 h of incubation. However, PRF was not able to inhibit these bacteria. This could be due to the fact that PRF is a matrix of autologous fibrin, in which a large quantity of platelets and leukocyte cytokines are embedded intrinsically during centrifugation leading to their progressive release over time (7–11 days) as the network of fibrin disintegrates.

In Group 5, two in vitro studies were included [Table 4]. In one study, there was a difference in preparation protocols and evaluation of the antibacterial activity. Alefiya et al. evaluated the variations in the fibrin network pattern, platelet count, and antimicrobial efficacy of PRF procured using variable centrifugation speed and time duration in different age groups. Three PRF membranes were obtained at 1400, 2800, and 3500 rpm for 8 min, while the other three membranes were obtained after 15 min of centrifugation, respectively. The relative centrifugal force values were within the spectrum of 228–1425 g. In this study, more than 90% of platelets were entrapped in the PRF membrane at a centrifugation speed of 228 g for 8 min regardless of the age group. As the time and speed increased, there was the presence of 50% of platelets. The antimicrobial efficacy of PRF was evaluated by measuring the zone of inhibition around the samples. The authors reported that reducing the centrifugation speed and time resulted in a clearly increased tendency in antimicrobial potential. In all three age groups, the group that had lower speed and lower time (228 g for 8 min) revealed the widest diameter zone of inhibitions indicating higher antimicrobial effect of PRF.
Table 4: Platelet-rich fibrin only-preparation protocols

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In another in vitro study, Castro et al. evaluated the antibacterial property of L-PRF membrane and exudate against the most common periodontopathogens which are cultured on agar plates and in planktonic solution [Table 5]. Even though the membrane showed antibacterial effect against P. intermedia, F. nucleatum, and A. actinomycetemcomitans, the increased effect was seen against P. gingivalis. Moreover, the PRF exudate also showed more effect against P. gingivalis. They also found that PRF exudate showed decreased number of viable P. gingivalis in a dose-dependent way, while A. actinomycetemcomitans showed increased growth in the planktonic solution. This is the only study which evaluated and aimed to study the efficacy of PRF against periodontopathogens.
Table 5: Platelet-rich fibrin only-against periodontopathogens

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   Discussion Top


The last two decades saw the regenerative potential of autologous PCs and studies were more pertained to it, but the antibacterial/antimicrobial properties of PRF have not been explored much. Even though the antimicrobial properties of PRP have been investigated in the literature, the antimicrobial effects of PRF are scarce. There are various types of PRF which are obtained by protocols as prescribed by Choukoran and Dohan Ernfest.

The PRF layer is found to be rich in fibrin, platelets, leukocytes, monocytes, and growth factors.[6] The PRF obtained promotes microvascularization, migration of epithelial cells, and accelerated healing.[7] It has been used in various surgical applications such as treatment of intrabony defects, dental implants, postextraction healing, and reducing the rate of postsurgical complications.[8],[9] Thus, the PRF obtained can be used as a clot or exudate or can be compressed to achieve a membrane.

The aim of this review is to explore the antimicrobial properties of the various PRF that is being used in wound healing. It has been shown that platelets play a key role against infections caused by microorganisms by the following facts, suggesting that platelets possess antibacterial properties.[10],[11] Platelets possess similar surface receptors and cytoplasmic granules which are comparable in structure and function to neutrophils, monocytes, or macrophages. Hence upon activation, platelets prevent the spread of microbes by phagocytosis. It has also been observed that they initiate or amplify the complement fixation. Platelets have also been shown to generate oxygen metabolites, which contribute to their antimicrobial activity. Platelets possess microbicidal proteins such as platelet microbicidal protein (PMPs) and thrombin-induced PMPs (t-PMPs) which are released on stimulation by the microbes. The presence of leukocytes not only provides immune responses but also possesses innate antibacterial property and also stimulates platelets to be proactive against pathogens. The following facts emphasize the role of leukocytes in PRF.[12] Leukocyte is an active member in the process of healing of which one of the main roles is to produce inflammatory cytokines and battery of growth factors. Macrophages also produce collagenase, release of transforming growth factor as well as platelet-derived growth factor (which was considered specific for thrombocytes), release interleukin-1, fibroblast growth factor, and tumor necrosis factor. Neutrophils not only contain growth factors but also are rich source of natural antibacterial proteins. The two granules primary and secondary granules contain numerous bactericidal factors. The azurophil granules (primary) contain defensins, cathelicidins, serprocidins, bactericidal/permeability-increasing protein of gram-negative bacteria, myeloperoxidase, and cytoplasmic calprotectin, whereas the specific granules (secondary) are rich in antibacterial proteins such as lysozyme, collagenase, gelatinase, lactoferrin, phospholipase A2, transcobalamin-1, and membrane proteins.

Studies have shown that there might be a part of antimicrobial activity which is mainly due to the presence of these bactericidal proteins in the granules. However, because of the centrifugal force, there might be some disruption of these granules releasing the proteins. The effects of bactericidal activity are best seen in circulation, but the role after it has been removed from the circulation and applied directly on to the site with fibrin, overlooking the normal physiological process needs to be researched further.

Careful principles were followed in the selection of various studies which evaluated the aim of the review. Even though an attempt was made to check on the quality and methodology, this review should be interpreted with caution and should be confirmed by further future studies. Even though the studies have shown both inhibition and noninhibition of a variety of microorganisms, the discrepancies may be due to variable strains of bacteria used in the studies. Another variability may also be due to different types of preparation of PCs used. In order to standardize, the groups were divided based on the preparation protocols and usage of drugs locally or systemically (five groups).

In the systemic antibiotics group, one clinical study was reported which included administration of antibiotics, i.e., amoxicillin 1 h before implant surgery. This novel method provided antibacterial activity for only 24–48 h.[13] This low duration of antibacterial activity was mainly due to no affinity of the given antibiotic to the fibrin which may have led to the lower time of antibacterial action.

In PRF as local drug delivery group, one in vitro study reported no interference of PRF formation when antibiotics were incorporated into the PRF.[14] However, PRF with antibiotics provided higher antibacterial activity when compared with PRF alone as local drug delivery. Moreover, antibiotics preserved the activity of PRF, for more than 4 days which led to the conclusion that this system can be used as a slow-release antibacterial agent which may be the future in periodontal regeneration.

In the I-PRF group, two in vitro studies were included in the review. One study reported that I-PRF had a greater number of platelets and hence more amount of growth factors were released; in this study, only subgingival plaque samples were taken to see the zones of inhibition, and no microbes were utilized.[15] Another study reported both antibacterial and antibiofilm activity of I-PRF, which was mainly due to the release of proteins such as lactoferrin, defensins, heparin-binding protein, cathelicidins, and phospholipase A2 ultimately leading to interference with bacterial cell wall and necrosis.[16]

In PRF with other PC group, two in vitro studies were included. One of the in vitro studies compared the antibacterial effects of PRP, PRF, and I-PRF.[17] This study revealed that I-PRF had more antibacterial activity over P. gingivalis which may be due to increased platelet release and increased concentrations of leukocytes in I-PRF. However, PRP showed significant antibacterial activity when compared to I-PRF and PRF over A. Actinomycetamcomitans. Another in vitro study which compared PRF with PRP revealed an increased antibacterial effect of PRP over PRF.[18] The authors also reported that even though the components are the same in PRF and PRP, the extra added calcium chloride in the PRP might be the contributing factor for the increased antimicrobial property of PRP.

In PRF alone group, which included two in vitro studies, one which reported antibacterial activity based on the preparation protocols and other study based on the antimicrobial property against periodontopathogens. Based on preparation protocols of the study lower speed, the lower time provided increased zone of inhibition which led to the proposed increased antimicrobial activity.[19] They also evaluated the number of platelets which was found to be higher in the lower speed and lower time group, which explains the fact that the more the number of platelets more the growth factors which may be attributed to the higher antimicrobial activity. A first in vitro study on the role of L-PRF against periodontopathogens reported that both membrane and exudate of PRF showed antibacterial property against periodontopathogens, especially Prevotella intermedia, F. nucleatum, and A. actinomycetemcomitans, but an increased effect was seen against P. gingivalis.[20] However, they also reported that PRF exudate showed an increased growth of A. actinomycetemcomitans when compared to P. gingivalis which was decreased in planktonic solution.

The antibacterial effect of PRF and its exact role needs to be studied in depth for better understanding on the action of PRF upon all the regenerating tissues. The plasma consists of complement system, which on activation leads to bacterial cell lysis and recruitment of leukocytes.[21] This relation between the plasma and the complement might also contribute to the antimicrobial effects of PRF. A recent in vitro study has shown that PRF has more effective antibacterial action against P. gingivalis compared to A. actinomycetamcomitans. This is mainly due to the proteinase inhibitors such as human alpha-2 macroglobulin, which inhibits the actions of gingipain (virulence factor) leading to cellular invasion and cell death. Two theories have been proposed for the action of L-PRF against P. gingivalis. (1) The cells seen in the PRF matrix released antimicrobial proteins constantly against the specific bacteria (2) the peptides entrapped in the matrix were released slowly along with the disintegration of the fibrin. However, the L-PRF membrane showed inhibition of A. actinomycetamcomitans, by affecting the aggregation of these bacteria and also by the leukotoxic effect of serum against these bacteria.

A new modification of PRF, namely A-PRF has shown superior properties when compared with standard PRF such as the increased release of proteins and growth factors,[22] proliferation of fibroblasts, its migration, and expression of growth factors.[23] Hence, when A-PRF is combined with antibiotics, it shall provide advanced wound healing properties and also can be used as local delivery devices along with any biomaterial as mentioned by Miron and Zhang.[24]

To the best knowledge of the authors, this is the only review so far which has reviewed the antibacterial efficacy of PRF in oral tissues. However, the limitations of the review include, the variability seen in each of the study included in the review, in terms of microorganisms where only one study evaluated the effect on the periodontopathogens while others evaluated the oral bacteria in general. Furthermore, there was variation in the microbes tested in these studies. One of the main drawbacks of all the studies reviewed, none of them evaluated the concentration of various growth factors which were invovled in antimicrobial activity. Moreover, there are variations seen in the aims and design protocols among the studies considered in the review. Since there is diversity of variations in all the studies, an accurate standardization is required to conclude with sufficient evidence.


   Conclusion Top


Sufficient research and clinical studies are needed to evaluate the potential benefits of PRF in terms of antimicrobial activity. It is evident with the available data that PRF has antimicrobial activity against microbial pathogens. Based on the review, it can be concluded that of the various PCs, especially PRF has the potential antimicrobial activity compared to other PCs. This activity can be enhanced by preparation protocols such as lowering the centrifugal speed and lowering the time, incorporating antibiotics into the fibrin matrix which can act as a slow-releasing drug delivery system. Considering its antimicrobial effect on periodontopathogens, PRF should be considered as a potential local drug delivery system and also natural regenerative material which should make this biological material unique from the rest of the biomaterials used now. Future research should focus on the exact role of antimicrobial property of each growth factor and molecules present in the PRF along with patient parameters such as age, sex, blood parameters, and drug interactions. Utilizing one's own blood for regeneration shall imbibe more values in minds of the patient and also the treating surgeon, which shall be a boon to mankind.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Choukroun J. Advanced PRF and i-PRF: Platelet concentrate or blood concentrate? J Periodontal Med Clin Pract 2014;1:1-4.  Back to cited text no. 1
    
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Miron RJ, Fujioka-Kobayashi M, Hernandez M, Kandalam U, Zhang Y, Ghanaati S, et al. Injectable platelet rich fibrin (i-PRF): Opportunities in regenerative dentistry? Clin Oral Investig 2017;21:2619-27.  Back to cited text no. 3
    
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