Potential Implications of Blood Flow Restriction Exercise on Vascular Health a Brief Review
Introduction
Blood period restriction (BFR) can limit the blood menses and increase the mechanical pressure level to the working muscle during exercise, resulting in local hypoxia/ischemia. Low-load grooming with BFR is more than conducive to increasing musculus strength (Lixandrão et al., 2018) and endurance (Kacin and Strazar, 2011) than that without BFR, which may be attributed to improved oxygen commitment and extraction of working skeletal muscles during BFR training. The combination of these mechanisms increases the peripheral vascular arrangement adaptability (Kacin and Strazar, 2011). A recent meta-analysis demonstrated that resistance training impacts more positively on arterial compliance regulation equally the chapters to restrict blood flow increases (Liu et al., 2021). Compared to traditional resistance training, this positive consequence on vascular function was significantly higher when the preparation time does not exceed 4 weeks (Liu et al., 2021). Nevertheless, the relevant mechanism of BFR-training regulating the peripheral vascular system (PVS) remains unclear.
The neogenesis of peripheral capillaries has been suggested as ane of the underlying mechanisms through which BFR-preparation regulates the PVS. A previous study that indirectly assessed the skeletal musculus microvasculature using the capillary filtration technique showed that BFR exercise enhanced capillary growth (Hunt et al., 2013). In the report of Mueller et al. (2014), 21 young men were divided into two groups for viii weeks of resistance training intervention. Their results showed that the synergism of whole-torso vibration and blood menstruum restriction could further meliorate the capillary-to-fiber ratio, which were not observed by resistance training solitary. Furthermore, the expression of some angiogenic genes was reported to be significantly enhanced post-obit depression-load resistance exercise with BFR (Larkin et al., 2012). The increase of angiogenesis gene expression is closely related to angiogenesis after exercise (Olfert et al., 2016). Therefore, further analysis is required to determine the physiological or molecular mediators of this response.
One of the main growth factors in the circuitous pathways involved in angiogenesis is the vascular endothelial growth factor (VEGF) (Olfert et al., 2010). During low-load resistance practise with BFR, the resulting decrease in muscle oxygen levels may stabilize hypoxia-inducible gene 1α (HIF-1α) for targeted activation of VEGF transcription (Barjaste et al., 2021). Furthermore, VEGF efflux from the skeletal musculus was promoted through the action of endothelial nitric oxide synthase (eNOS) after the generation of nitric oxide due to shear stress (Gielen et al., 2011). These events improved the availability of VEGF at EC-receptor sites for vascular endothelial growth factor receptor 2 (VEGFR-2) activation (Shen et al., 1998) and facilitated the angiogenic effect of VEGF (Milkiewicz et al., 2005), whereas the expression of skeletal muscle VEGF was mainly mediated by peroxisome proliferator-activated receptor-gamma co-activator blastoff (PGC-1α) (Leick et al., 2009). Conclusively, VEGF secretion may be regulated by BFR in diverse ways to promote angiogenesis.
There is information paucity regarding the issue of BFR exercise on various angiogenesis-related factors in skeletal muscle. Research findings take demonstrated that BFR exercise could facilitate the expression of VEGF by enhancing HIF-1α (Larkin et al., 2012; Ferguson et al., 2018), whereas other researchers have contradicting views (Taylor et al., 2016; Preobrazenski et al., 2020). This review was conducted to compare the effects of BFR practise and non-BFR on angiogenesis-related factors, and to explore the effects of various do programs on VEGF and HIF. The findings will improve the electric current body of knowledge on the role of BFR exercise in angiogenesis.
Methodology
Protocol and Registration
The review protocol was registered on June 18, 2021, with the International Platform of Registered Systematic Review and Meta-Analysis Protocols (PROSPERO registration number: CRD42021261367).
Information Sources and Report Selection
Because the exam methods and experimental instruments in the early research are very dissimilar from those at present, the inquiry in recent twenty years is searched. The systematic search was conducted using iv databases: Scopus, PubMed, Web of Science and EBSCO. Studies published betwixt January 2001 and June 2021 were considered while the terminal retrieval date was June 18, 2021. The search terms used were "blood menstruation restriction," "kaatsu," "blood flow restricted," "HIF," "VEGF," "NOS," "PGC," "grooming," and "exercise." Both the search strategy for each database and the corresponding results are presented in Appendix A. To minimize bias during the literature search, the titles and abstracts retrieved from the databases were screened by two independent investigators.
Boosted relevant information such as the outset author's proper name, the year of publication, sample size, exercise plan, age, BFR method and main findings were documented. Outcome variables included VEGF, VEGFR-2, PGC-1α, HIF-1α, and eNOS. When necessary, the respective authors were contacted via email to clarify whatever unclear information. A third investigator was assigned to provide an opinion if the 2 principal investigators disagree on any data from the manufactures. On that note, the disagreement was resolved later discussing and reaching a consensus. The article selection procedure is summarized in Effigy 1.
Figure i. Preferred reporting items for systematic reviews and meta-analysis (PRISMA) flow diagram of search results.
Inclusion and Exclusion Criteria
The inclusion criteria entailed full-text manufactures written in English, cross-sectional written report blueprint, participants were good for you individuals betwixt 18 and 40 years old, the experimental group was do combined with BFR while the control (CON) group was exercise without BFR. Studies were also eligible for inclusion if the sampling method entailed vastus lateralis musculus biopsy taken either before exercise or two to four hours after exercise. Other literature such every bit abstracts, briefing proceedings, posters, or presentations were excluded.
Quality Cess
A pre-designed quality assessment tool, the NIH quality assessment tool for observational cohort and cross-exclusive studies, was used to assess all the included studies. Study Quality Assessment Tools -- NHLBIone, accessed 15 June 2020) has a total of fourteen questions. The quality of each report was classified as "poor," "fair," or "practiced."
Adventure of Bias Assessment
A funnel plot was used to analyze the publication bias of the study. Sensitivity analysis was performed if more than 5 studies include the aforementioned indicator. Specifically, the sensitivity analysis was conducted by excluding each study sequentially to determine the stability of the meta-assay results.
Data Analysis
The meta-analysis was executed by inbound all the relevant outcome variables in the Review Manager (Version 5.4, Copenhagen: The Nordic Cochrane Center, The Cochrane Collaboration, 2014). All the studies included in the assay had continuous outcome variables while the test units and methods were dissimilar. Therefore, standardized mean divergence (SMD) was chosen as the result calibration index. Heterogeneity between studies was tested using the I (Kacin and Strazar, 2011) statistic. Heterogeneity was considered absent betwixt studies when the I (Kacin and Strazar, 2011) is less than 40%. Therefore, a stock-still-result model tin be used for analysis. Conversely, heterogeneity is present betwixt studies if I (Kacin and Strazar, 2011) is equal to or greater than 40% and a random effect model must be used for analysis. Sub-group assay was further performed to decide the heterogeneity. The level of statistical significance was adjusted to P < 0.05. Co-ordinate to the Cohen's guideline (Cohen, 1992), the effect size was explained as: 0.2 is a minor effect, 0.five is a medium effect and 0.viii is a large effect.
Results
Eligibility of Studies
A full of ten cross-sectional studies evaluating the effects of BFR training on angiogenesis-related factors in skeletal musculus amidst salubrious adults were included in this review. The bones information in the included studies is shown in Tabular array 1. Ethical approvals were obtained from the various institutions in which the studies were conducted. The level of agreement betwixt the two principal investigators was high with a Cohen kappa coefficient of 0.884. A total of 74 men and 3 women participated in the studies, corresponding to the overall sample size in the BFR and CON groups. Seven studies focused on PGC-1α and VEGF. HIF-1α were reported in six articles while only three studies evaluated VEGFR-two and eNOS. Vi of the articles employed resistance exercises, whereas aerobic exercises were used in the remaining four studies. Overall, the BFR pressure ranged from 50 to 220 mmHg.
Table 1. Overview of the included studies.
Sensitivity Assay
3 steps were performed for the sensitivity analysis: changing the analysis model, outcome size option, and exclusion of individual studies. VEGF and PGC-1α indices were not significantly affected subsequently the sensitivity test and the outcomes were stable. In contrast, the HIF-1α was highly sensitive and characterized by unstable results.
Quality Assessment
Based on the NIH scale, nine of the 10 studies included in this review (Ameln et al., 2005; Drummond et al., 2008; Norrbom et al., 2011; Larkin et al., 2012; Taylor et al., 2016; Christiansen et al., 2018; Ferguson et al., 2018; Preobrazenski et al., 2020; Barjaste et al., 2021) recorded an overall quality rating of "Skilful" and only one report (Norrbom et al., 2004) had an overall quality rating of "Fair" as shown in Table 2.
Table ii. Depiction of the risk of bias assessment.
Quantitative Synthesis
Vascular Endothelial Growth Factor and Vascular Endothelial Growth Cistron Receptor-2
Figure 2A shows the six studies (Ameln et al., 2005; Larkin et al., 2012; Taylor et al., 2016; Ferguson et al., 2018; Preobrazenski et al., 2020; Barjaste et al., 2021) that evaluated the effects of BFR on VEGF, whereas the iii studies (Larkin et al., 2012; Taylor et al., 2016; Ferguson et al., 2018) reporting the effects of BFR on VEGFR-2 mRNA are presented in Effigy 2B. The meta-analysis revealed that BFR grouping (northward = 58) improved VEGF more significantly (P < 0.05) compared to the CON group (n = 58) (heterogeneity test, P = 0.09, I2 = 44%; SMD, 0.93 [0.38, 1.48]). VEGF poly peptide (heterogeneity test, P = 0.lxxx, Itwo = 0%; SMD, 0.33 [−0.52, 1.17]), VEGF mRNA AE (heterogeneity exam, P = 0.71, I2 = 0%; SMD, 0.40 [−0.23, i.03]) or VEGF mRNA RE (heterogeneity exam, P = 0.36, I2 = 6%; SMD, ane.66 [0.97, ii.35]) showed greater homogeneity in the sub-group analysis. Also, a significant deviation (P < 0.05) was observed in the VEGFR-ii mRNA betwixt the BFR (due north = 26) and CON (north = 26) groups (heterogeneity exam, P = 0.81, I2 = 0%; SMD, 0.64 [0.08, one.21]).
Figure 2. The wood plot of the effect size for studies assessing the issue of blood menstruum restriction do on the VEGF (A) and VEGFR-2 (B) mRNA.
Hypoxia Inducible Factor 1α
The effects of BFR on HIF-1α was investigated in half dozen studies (Ameln et al., 2005; Drummond et al., 2008; Larkin et al., 2012; Taylor et al., 2016; Ferguson et al., 2018; Preobrazenski et al., 2020) as shown in Figure three. HIF-1α was significantly improved (P < 0.05) in the BFR group compared to the CON group (n = 53) (heterogeneity test, P = 0.67, I2 = 0%; SMD, 0.43 [0.03, 0.82]). A greater homogeneity was detected in the sub-group analysis for HIF-1α mRNA AE (heterogeneity test, P = 0.38, Itwo = 0%; SMD, 0.29 [−0.34, 0.91]) or HIF-1α mRNA RE (heterogeneity test, P = 0.56, I2 = 0%; SMD, 0.51 [0.01, i.02]).
Figure 3. The woods plot of the effect size for studies assessing the effect of blood menses brake exercise on the HIF-1α mRNA.
Peroxisome Proliferator-Activated Receptorγcoactivator-1α
7 studies (Norrbom et al., 2004, 2011; Taylor et al., 2016; Christiansen et al., 2018; Ferguson et al., 2018; Preobrazenski et al., 2020; Barjaste et al., 2021) reported the effects of BFR on PGC-1α (Figure 4). PGC-1α was significantly improved (P < 0.05) in the BFR group (n = 72) than the CON group (northward = 74) (heterogeneity test, P = 0.02, I2 = 54%; SMD, 0.74 [0.21, 1.28]). Likewise, the sub-group analysis demonstrated a greater homogeneity for PGC-1α poly peptide (heterogeneity test, P = 0.23, Itwo = 32%; SMD, −0.07 [−0.92, 0.78]) or PGC-1α mRNA (heterogeneity test, P = 0.12, I2 = 41%; SMD, ane.04 [0.49, 1.59]).
Figure 4. The forest plot of the issue size for studies assessing the effect of claret flow restriction practice on the PGC-1α.
Endothelial Nitric Oxide Synthase
As shown in Figure 5, the effects of BFR on eNOS were evaluated in 3 of the reviewed articles (Larkin et al., 2012; Taylor et al., 2016; Ferguson et al., 2018). The meta-analysis revealed eNOS was more than significantly improved (P < 0.05) in the BFR group (north = 26) compared to the CON group (n = 26) (heterogeneity test, P = 0.88, I2 = 0%; SMD, 0.threescore [0.04, one.17]).
Figure five. The wood plot of the effect size for studies assessing the outcome of blood menstruum restriction exercise on the eNOS mRNA.
Analysis of Publication Bias
A funnel plot was employed in analyzing the publication bias. Using the minimum requirement of the funnel plot, the total sample size of all the 10 studies reflected the publication bias to a sure degree. The feasibility of performing funnel plot analysis using a small sample size has been demonstrated past Lu et al. (2020) in a previous study. Figure 6 depicted the funnel plots of all the symmetrically-distributed indicators, reflecting a minor degree of bias in the studies.
Figure half dozen. Funnel plot of publication bias for the outcome of resistance exercise on the VEGF (A), VEGFR-two (B) and HIF-1α (C).
Discussion
Studies in improving skeletal muscle capillary networks and functions emphasize the high intensity of either aerobic or resistance practice (Prior et al., 2003; Gavin et al., 2007; Larkin et al., 2012). However, high-intensity exercise is restricted to some special populations, including cardiovascular patients and older persons. BFR exercise is a proposed culling for traditional high-intensity practise (Drummond et al., 2008) and it is of import to compare their effects on skeletal musculus capillary growth. Hence, the present meta-assay investigated the expression of VEGF, VEGFR-2, PGC-1α, HIF-1α, and eNOS in healthy adults later both exercise modalities. The results showed that the expression of the above mentioned angiogenic genes was significantly increased in the BFR group compared to the control grouping. However, different practice programs may cause various changes in the mRNA expression of VEGF and HIF-1α. The present results revealed that resistance do can significantly increase the mRNA expression of HIF-1α and VEGF in healthy adults. Conversely, these positive effects were lacking for aerobic do.
It is speculated that this may be caused by different degrees of hypoxia, and the increment of HIF-1 may mainly depend on anaerobic metabolism (Lundby et al., 2009). In exercise with BFR, resistance exercise mainly stimulates the skeletal musculus system, which may lead to lower oxygen consumption than aerobic exercise (Ferrari et al., 2018). The lower oxygen commutation level may be the reason for the higher expression of HIF-1 when resistance do combined with BFR. Furthermore, some show suggests that resistance exercise with BFR may lead to better superposition effect on angiogenesis rather than aerobic exercise (Mueller et al., 2014; Conceicao et al., 2016; Mitchell et al., 2019). Mitchell et al. (2019) indicated that the alter of capillary density afterward four weeks of aerobic training with BFR was like to that without BFR. Briefly, resistance do combined with BFR may have a better outcome on angiogenesis than aerobic exercise.
Interestingly, the included studies presented contradicting outcomes in the expression of VEGF (Larkin et al., 2012) and PGC-1α (Ferguson et al., 2018) protein from mRNA. The authors attributed the discrepancies to the limitations of sampling time as information technology might have several days after exercise for some proteins to exist translated (Gustafsson et al., 2005; Perry et al., 2010). In contrast, Barjaste et al. (2021) reported that VEGF, HIF-1α, and PGC-1α poly peptide expression were significantly increased at 3-h post-BFR-walking. This finding corroborates an brute-based study, which reported an increase in PGC-1α protein level in BFR-low intensity aerobic grooming (Bahreinipour et al., 2018). This might exist explained by the different exercise modes adopted in the studies, reflecting diverse metabolic stress and mechanical tension between them. For instance, it was found the expression of HIF-1α, VEGF and PGC-1α proteins (Conceicao et al., 2016) was improve stimulated past low-intensity BFR walking compared to depression-intensity BFR cycling (Barjaste et al., 2021).
1 of the primal pro-angiogenic factors during exercise training is VEGF (Hellsten and Hoier, 2014) and its mRNA expression increases after a unmarried bout of exercise (Gustafsson et al., 1999). This event was reported past Larkin et al. (2012) equally the nigh notable transcriptional change among other angiogenic genes in response to the reduced blood flow and oxygen delivery in exercised skeletal musculus during BFR. The primary receptor of VEGF (VEGFR-2) mediates the VEGF-induced angiogenesis (Milkiewicz et al., 2005; Ferguson et al., 2018). Results from this meta-analysis indicated that VEGFR-2 mRNA increased subsequently BFR-practice, which may result from the increased VEGF bounden (Ferguson et al., 2018) and the number of endothelial cells (Gustafsson et al., 2007) induced by BFR-do. Additionally, VEGF expression would exist promoted by activating some of its key regulating factors (HIF-1α, PGC-1α, and eNOS) when BFR is combined with do, thereby eliciting an increased local muscular ischemia or hypoxia, shear-stress, and mechanical stress (Shweiki et al., 1992; Stein et al., 1995; St-Pierre et al., 2003; Bloor, 2005; Jager et al., 2007; Arany et al., 2008; Hawley et al., 2014; Paula et al., 2020).
HIF-1α is an important angiogenic regulator of hypoxia and metabolic stress (Semenza, 2006; Taylor et al., 2016). While skeletal musculus PO2 is reduced past exercise, exercise-dependent reduction in oxygen tension might facilitate up-regulation of HIF-1α expression in skeletal muscles. The levels of HIF-1α is increased significantly afterward BFR-exercise compared to non-BFR exercise (Larkin et al., 2012; Taylor et al., 2016; Barjaste et al., 2021). This reflects a higher degree of hypoxia, followed by increased activation of VEGF, which is the downstream factor of the HIF-1α pathway. This is in line with the nowadays pooled data meta-analysis simply contradicts the findings from the assay of some included studies. Ameln et al. (2005) constitute no pregnant differences between BRF and non-BFR conditions in HIF-1α protein levels although the lactate levels indicated a lower oxygen tension during BFR-exercise. The caste of hypoxia may be already low enough to stimulate HIF-1α expression at 50 to 60% of the maximum work rate during non-BFR do. Hence, the intensity of exercise protocols may also play an important role in activating the HIF-1α by BFR-do. Other possible reasons that may likely account for the negative results include field of study variability, exercise modes and sampling time (Drummond et al., 2008; Ferguson et al., 2018; Preobrazenski et al., 2020). Given these negative results, the enhanced angiogenesis induced by BFR more likely depends on the PGC-1α pathway.
PGC-1α has recently emerged equally an inducer of angiogenesis in skeletal muscle, which strongly induces VEGF expression (Jung and Kim, 2014) in response to ischaemia (Arany et al., 2008). Therefore, increased oxidative stress (Kemp et al., 2003; Yu et al., 2008; Zhong et al., 2011) and cobweb type-dependent AMPK signaling (Norrbom et al., 2011; Christiansen et al., 2018; Preobrazenski et al., 2020) may be associated with augmentation of BFR in exercise-induced PGC-1 mRNA. Four out of five studies including PGC-1α mRNA measurement showed a higher expression of the poly peptide during BFR-practise (Norrbom et al., 2011; Christiansen et al., 2018; Ferguson et al., 2018; Preobrazenski et al., 2020), which is consistent with the electric current pooled information meta-analysis. Nevertheless, one study reported no differences between the two exercise modalities, which might be due to dissimilar exercise and BFR modes adopted (Taylor et al., 2016). Christiansen et al. (2018) constitute that musculus hypoxia was non a cardinal gene for BFR upon comparing the effects of BFR and systemic hypoxia (∼3,250 m) on PGC-1α. Similarly, a previous written report discovered that moderate-intensity cycling at simulated altitude (iii,000 m) did not bear upon the PGC-1α mRNA in the skeletal muscle (Slivka et al., 2014). In addition, the alterations in the expression of PGC-1α poly peptide might be influenced by the intensities of do with BFR (Bahreinipour et al., 2018; Ferguson et al., 2018; Barjaste et al., 2021). Moreover, this protein may also be affected by the sampling time because the increase in protein concentrations or levels may delay for hours or days afterward the exercise (Baar et al., 2002).
The bounden of VEGF to VEGFR-two activates a signaling pour leading to NO product (Larkin et al., 2012). Furthermore, the production of NO is direct induced past the eNOS activity, which is controlled by either shear-stress dependent or contained VEGF expression (Larkin et al., 2012). Therefore, the increased eNOS mRNA expression afterwards BFR-exercise (Ferguson et al., 2018) might event from the shear stimulus caused by BFR, as well as mechanical pinch by skeletal muscle contraction. In contrast, Larkin et al. (2012) and Taylor et al. (2016) indicated that musculus expression of eNOS was not increased by the combination of BFR with acute low-intensity practice. These inconsistent results may be due to variations in sampling time, as the peak expression of eNOS may announced before VEGF and VEGFR-2 (Milkiewicz et al., 2005; Ferguson et al., 2018).
Report Limitations
About of the studies included in this review reflected a small sample size and only 10 manufactures met the inclusion criteria. This reflects the lack of large sample size literature on this subject. Secondly, differences in muscle fiber types may explain the differences in the expression patterns of angiogenic factors, merely at that place is a lack of straight evidence. Only ii indirect evidences showed that there was no departure in the expression of AMPK (Christiansen et al., 2018) and PGC-1α (Norrbom et al., 2004) after exercise with blood flow restriction compared without blood flow brake. Additionally, the changes of angiogenesis related factors in skeletal muscle can not really represent the actual angiogenesis. Capillary-to-fiber ratio is an constructive alphabetize to reflect vascular density, notwithstanding the relationship betwixt blood menses brake training intervention and capillary-to-fiber ratio is not clear. This limits our further explanation and verification of the effect of claret menstruation brake training. In hereafter enquiry, nosotros tin can further explore the effect of blood period restriction training on vascular density and its human relationship with angiogenesis related factors. Furthermore, the majority of studies focused on male person samples while simply three females were included. This might be attributed to the fact that women are more reluctant to accept musculus biopsy. Moreover, the forms of BFR used in various studies vary greatly, including cuff, raised limb and pressure level sleeping accommodation. This may atomic number 82 to differences in the actual pressure practical and some errors may occur in horizontal comparison. Finally, most studies focused on mRNA expression and only a few considered protein alterations. Future studies should further explore the effect of BFR training on the expression of angiogenesis-related proteins, especially after a few days of exercise.
Conclusion
This study revealed that exercise with BFR elicited more VEGF, VEGFR-two, HIF-1α, PGC-1α, and eNOS mRNA expression than exercise without BFR, but not VEGF and PGC-1α protein expression. Given that the combination of resistance practice and BFR was more conducive to improving VEGF and HIF-1α mRNA expression compared to aerobic exercise. Therefore, BFR grooming may be more conducive to improve vascular function, the protocol should be considered when developing sports-based training programs. Results cannot be extrapolated to all individuals. Hereafter studies should include samples from other populations to determine viable training programs.
Information Availability Argument
The original contributions presented in the study are included in the commodity/supplementary material, farther inquiries can be directed to the corresponding writer/s.
Author Contributions
LW conceptualized and designed the study, collected and organized the information, and drafted the initial manuscript. ShuL collected and organized the information, reviewed the included articles, and conducted the analyses. ShiL and WY collected and organized the data and reviewed the included articles. WL and HQ conceptualized and designed the written report and critically reviewed and revised the manuscript. TL conceptualized and designed the written report, coordinated and supervised data collection, and critically reviewed and revised the manuscript. All authors read and approved the concluding manuscript.
Funding
This piece of work was supported by the Zhejiang Provincial Natural Science Foundation of Red china (LY19C110002).
Conflict of Interest
The authors declare that the research was conducted in the absence of whatsoever commercial or financial relationships that could be construed as a potential conflict of interest.
The handling editor alleged a shared affiliation with several of the authors LW, HQ, TL, and WL at time of review.
Publisher's Annotation
All claims expressed in this article are solely those of the authors and practise not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this commodity, or claim that may exist made past its manufacturer, is not guaranteed or endorsed by the publisher.
Footnotes
- ^ https://www.nhlbi.nih.gov/wellness-topics/report-quality-cess-tools
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Appendix
Appendix A. Search strategy.
Source: https://www.frontiersin.org/articles/10.3389/fphys.2022.814965/full
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