Back to Authors

Behfar, Atta

https://orcid.org/0000-0003-3775-5784

Mayo Clinic

Mayo Clinic

Citations 122

From Tissue to Human Regeneration: The Development of a Comprehensive Regenerative Care Clinic for People With Diabetes
Hargraves, Ian , Behfar, Atta , Simha, Vinaya , Donoghue, Chenoa, Renner, Amy Seegmiller , Brito, Juan P. , Hargraves, Ian G, Behfar, Atta , Brito, Juan P , Montori, Víctor M.

Regenerative Medicine | March 16, 2021 | Volume: 16 | Issue: 3 | Pages: 219-228

10.2217/rme-2020-0176 Get It

Impact of Repeat Dosing and Mesh Exposure Chronicity on Exosome-Induced Vaginal Tissue Regeneration in a Porcine Mesh Exposure Model
Kisby, Cassandra K. , Peng, Lillian , Stalboerger, Paul G., Trabuco, Emanuel C. , Behfar, Atta , Occhino, John A. , Peng, Lillian T , Behfar, Atta , Shadrin, Ilya Y.

Female Pelvic Medicine & Reconstructive Surgery | February 26, 2021 | Volume: 27 | Issue: 3 | Pages: 195-201

10.1097/spv.0000000000001017 Get It

Objective The aim of the study was to compare vaginal wound healing after exosome injection in a porcine mesh exposure model with (1) single versus multiple dose regimens and (2) acute versus subacute exposure. Methods Six 80-kg Yorkshire-crossed swine each had 2 polypropylene meshes implanted to create the vaginal mesh exposure model. Animals were divided into 3 groups based on number and timing of exosome injection: (1) single purified exosome product (PEP) injection (acute-single), (2) weekly PEP injections (acute-weekly, 4 total injections), and (3) delayed single injection (subacute-single). Acute and subacute injections occurred 1 and 8 weeks after mesh implantation, respectively. EdU, a thymidine analog, was given twice weekly after the first injection to track tissue regeneration. Euthanasia and tissue analysis occurred 4 weeks after the first injection. ImageJ was used to quantify epithelial thickness, cellular proliferation, and capillary density. Statistical analysis was performed using analysis of variance and post hoc Tukey test. Results Acute-single PEP injection tissues mirrored pilot study results, validating replication of protocol. Within the acute groups, weekly dosing resulted in 1.5× higher epithelial thickness (nonsignificant), 1.8× higher epithelial proliferation ( P < 0.05), and 1.5× higher regenerated capillary density ( P < 0.05) compared with single injection. Regarding chronicity of the exposure, the subacute group showed 1.7× higher epithelial proliferation (nonsignificant) and similar capillary density and epithelial thickness as compared with the acute group. Conclusions Exosome redosing resulted in significantly greater epithelial proliferation with significantly higher regenerated capillary density, leading to a trend toward thicker epithelium. Subacute exposure exhibited similar regeneration to acute exposure despite a delayed injection timeline. These results contribute to a growing body of preclinical research demonstrating utility of exosomes in pelvic floor disorders.
Regenerative Medicine Clinical Readiness
Yamada, Satsuki , Behfar, Atta , Terzic, André , Behfar, Atta , Terzic, Andre

Regenerative Medicine | February 24, 2021 | Volume: 16 | Issue: 3 | Pages: 309-322

10.2217/rme-2020-0178 Get It

Exosome-Induced Vaginal Tissue Regeneration in a Porcine Mesh Exposure Model
Kisby, Cassandra K. , Rolland, Tyler , Stalboerger, Paul G., Trabuco, Emanuel C. , Occhino, John A. , Shadrin, Ilya Y. , Rolland, Tyler J, Rolland, Tyler J , Zhou, Boran , Behfar, Atta

Female Pelvic Medicine & Reconstructive Surgery | January 14, 2021 | Volume: 27 | Issue: 10 | Pages: 609-615

10.1097/spv.0000000000001005 Get It

Objectives The purpose of this study was to explore the utility of an injectable purified exosome product derived from human apheresis blood to (1) augment surgical closure of vaginal mesh exposures, and (2) serve as a stand-alone therapy for vaginal mesh exposure. Methods Sixteen polypropylene meshes (1×1–3×3 cm) were implanted in the vaginas of 7 Yorkshire-crossed pigs by urogynecologic surgeons (day 0). On day 7, group 1 underwent surgical intervention via vaginal tissue suture reclosure with (n=2 pigs, n=4 meshes) or without (n=2 pigs, n=4 meshes) exosome injection; group 2 underwent medical intervention with an exosome injection (n=3, n=8 meshes). One animal in group 2 was given oral 2′-deoxy-5-ethynyluridine to track cellular regeneration. Euthansia occurred at 5 weeks. Results Mesh exposures treated with surgical closure alone experienced reexposure of the mesh. Exosome treatment with or without surgical closure resulted in partial to full mesh exposure resolution up to 3×3 cm. Exosome-treated tissues had significantly thicker regenerated epithelial tissue (208 μm exosomes-only and 217 μm surgery+exosomes, versus 80 μm for surgery-only; P < 0.05); evaluation of 2′-deoxy-5-ethynyluridine confirmed de novo regeneration throughout the epithelium and underlying tissues. Capillary density was significantly higher in the surgery+exosomes group ( P = 0.03). Surgery-only tissues had a higher inflammatory and fibrosis response as compared with exosome-treated tissues. Conclusions In this pilot study, exosome treatment augmented healing in the setting of vaginal mesh exposure, reducing the incidence of mesh reexposure after suture closure and decreasing the area of mesh exposure through de novo tissue regeneration after exosome injection only. Further study of varied local tissue conditions and mesh configurations is warranted.
Brachyury engineers cardiac repair competent stem cells
Li, Mark , Yamada, Satsuki , Shi, Ao , Singh, Raman Deep , Rolland, Tyler , Jeon, Ryoung‐Hoon , Shelerud, Lukas, Behfar, Atta , Rolland, Tyler J, Jeon, Ryounghoon, Lopez, Natalia, Behfar, Atta , Jeon, Ryounghoon , Rolland, Tyler J , Lopez, Natalia, Shelerud, Lukas M., Terzic, André

Stem Cells Translational Medicine | October 24, 2020 | Volume: 10 | Issue: 3 | Pages: 385-397

10.1002/sctm.20-0193 Get It

Abstract To optimize the regenerative proficiency of stem cells, a cardiopoietic protein-based cocktail consisting of multiple growth factors has been developed and advanced into clinical trials for treatment of ischemic heart failure. Streamlining the inductors of cardiopoiesis would address the resource intensive nature of the current stem cell enhancement protocol. To this end, the microencapsulated-modified-mRNA (M3RNA) technique was here applied to introduce early cardiogenic genes into human adipose-derived mesenchymal stem cells (AMSCs). A single mesodermal transcription factor, Brachyury, was sufficient to trigger high expression of cardiopoietic markers, Nkx2.5 and Mef2c. Engineered cardiopoietic stem cells (eCP) featured a transcriptome profile distinct from pre-engineered AMSCs. In vitro, eCP demonstrated protective antioxidant capacity with enhanced superoxide dismutase expression and activity; a vasculogenic secretome driving angiogenic tube formation; and macrophage polarizing immunomodulatory properties. In vivo, in a murine model of myocardial infarction, intramyocardial delivery of eCP (600 000 cells per heart) improved cardiac performance and protected against decompensated heart failure. Thus, heart repair competent stem cells, armed with antioxidant, vasculogenic, and immunomodulatory traits, are here engineered through a protein-independent single gene manipulation, expanding the available regenerative toolkit.
Cardiopoietic Stem Cell Therapy in Ischaemic Heart Failure: Long-Term Clinical Outcomes
Behfar, Atta , Sanz‐Ruiz, Ricardo , Sherman, Warren, Heyndrickx, Guy R. , Metra, Marco , Filippatos, Gerasimos , Henry, Timothy D. , Hajjar, Roger J. , Tendera, Michał , Senger, Stefanie , Povsic, Thomas J. , Program, for the CHART, Behfar, Atta , Metra, Marco , Bartúnek, Jozef , Terzic, André , Davison, Beth A. , Wojakowski, Wojciech , Waldman, Scott A. , Teerlink, John R , Gersh, Bernard J. , Cotter, Gad , Wijns, William , Program, for the CHART

ESC Heart Failure | October 23, 2020 | Volume: 7 | Issue: 6 | Pages: 3345-3354

10.1002/ehf2.13031 Get It

Abstract Aims This study aims to explore long-term clinical outcomes of cardiopoiesis-guided stem cell therapy for ischaemic heart failure assessed in the Congestive Heart Failure Cardiopoietic Regenerative Therapy (CHART-1) trial. Methods and results CHART-1 is a multinational, randomized, and double-blind trial conducted in 39 centres in heart failure patients (n = 315) on standard-of-care therapy. The ‘active’ group received cardiopoietic stem cells delivered intramyocardially using a retention-enhanced catheter. The ‘control’ group underwent patient-level sham procedure. Patients were followed up to 104 weeks. In the entire study population, results of the primary hierarchical composite outcome were maintained neutral at Week 52 [Mann–Whitney estimator 0.52, 95% confidence interval (CI) 0.45–0.59, P = 0.51]. Landmark analyses suggested late clinical benefit in patients with significant left ventricular enlargement receiving adequate dosing. Specifically, beyond 100 days of follow-up, patients with left ventricular end-diastolic volume of 200–370 mL treated with ≤19 injections of cardiopoietic stem cells showed reduced risk of death or cardiovascular hospitalization (hazard ratio 0.38, 95% CI 0.16–0.91, P = 0.031) and cardiovascular death or heart failure hospitalization (hazard ratio 0.28, 95% CI 0.09–0.94, P = 0.040). Cardiopoietic stem cell therapy was well tolerated long term with no difference in safety readouts compared with sham at 2 years. Conclusions Longitudinal follow-up documents that cardiopoietic stem cell therapy is overall safe, and post hoc analyses suggest benefit in an ischaemic heart failure subpopulation defined by advanced left ventricular enlargement on tolerable stem cell dosing. The long-term clinical follow-up thus offers guidance for future targeted trials.
Injectable conductive hydrogel restores conduction through ablated myocardium
Zyl, Martin van , Pedrotty, Dawn , Kuzmenko, Volodymyr , Sämfors, Sanna, Livia, Christopher , Vaidya, Vaibhav R. , Sugrue, Alan , Behfar, Atta , Asirvatham, Samuel J. , Gatenholm, Paul , Kapa, Suraj , van Zyl, Martin , Livia, Christopher , Vaidya, Vaibhav , Sugrue, Alan , Asirvatham, Samuel J , Gatenholm, Paul , Kapa, Suraj , Behfar, Atta , Karabulut, Erdem , McLeod, Christopher J.

Journal of Cardiovascular Electrophysiology | September 23, 2020 | Volume: 31 | Issue: 12 | Pages: 3293-3301

10.1111/jce.14762 Get It

AbstractIntroductionTherapies for substrate‐related arrhythmias include ablation or drugs targeted at altering conductive properties or disruption of slow zones in heterogeneous myocardium. Conductive compounds such as carbon nanotubes may provide a novel personalizable therapy for arrhythmia treatment by allowing tissue homogenization.MethodsA nanocellulose carbon nanotube‐conductive hydrogel was developed to have conduction properties similar to normal myocardium. Ex vivo perfused canine hearts were studied. Electroanatomic activation mapping of the epicardial surface was performed at baseline, after radiofrequency ablation, and after uniform needle injections of the conductive hydrogel through the injured tissue. Gross histology was used to assess distribution of conductive hydrogel in the tissue.ResultsThe conductive hydrogel viscosity was optimized to decrease with increasing shear rate to allow expression through a syringe. The direct current conductivity under aqueous conduction was 4.3 × 10−1 S/cm. In four canine hearts, when compared with the homogeneous baseline conduction, isochronal maps demonstrated sequential myocardial activation with a shift in direction of activation to surround the edges of the ablated region. After injection of the conductive hydrogel, isochrones demonstrated conduction through the ablated tissue with activation restored through the ablated tissue. Gross specimen examination demonstrated retention of the hydrogel within the tissue.ConclusionsThis proof‐of‐concept study demonstrates that conductive hydrogel can be injected into acutely disrupted myocardium to restore conduction. Future experiments should focus on evaluating long‐term retention and biocompatibility of the hydrogel through in vivo experimentation.
A novel engineered purified exosome product patch for tendon healing: An explant in an ex vivo model
Shi, Guidong , Wang, Zhanwen , Thoreson, Andrew R. , Jacobson, Daniel S. , Amadio, Peter C. , Behfar, Atta , Moran, Steven L. , Zhao, Chunfeng , Wang, Yicun , Zhao, Chunfeng , Behfar, Atta , Wang, Yicun , Shi, Guidong

Journal of Orthopaedic Research | September 16, 2020 | Volume: 39 | Issue: 8 | Pages: 1825-1837

10.1002/jor.24859 Get It

AbstractReducing tendon failure after repair remains a challenge due to its poor intrinsic healing ability. The purpose of this study is to investigate the effect of a novel tissue‐engineered purified exosome product (PEP) patch on tendon healing in a canine ex vivo model. Lacerated flexor digitorum profundus (FDP) tendons from three canines' paws underwent simulated repair with Tisseel patch alone or biopotentiated with PEP. For the ex vivo model, FDP tendons were randomly divided into three groups: FDP tendon repair alone group (Control), Tisseel patch alone group, and the Tisseel plus PEP (TEPEP) patch group. Following 4 weeks of tissue culture, the failure load, stiffness, histology, and gene expression of the healing tendon were evaluated. Transmission electron microscopy revealed that in exosomes of PEP the diameters ranged from 93.70 to 124.65 nm, and the patch release test showed this TEPEP patch could stably release the extracellular vesicle over 2 weeks. The failure strength of the tendon in the TEPEP patch group was significantly higher than that of the Control group and Tisseel alone group. The results of histology showed that the TEPEP patch group had the smallest healing gap and the largest number of fibroblasts on the surface of the injured tendon. Quantitative reverse transcription polymerase chain reaction showed that TEPEP patch increased the expression of collagen type III, matrix metallopeptidase 2 (MMP2), MMP3, MMP14, and reduced the expression of transforming growth factor β1, interleukin 6. This study shows that the TEPEP patch could promote tendon repair by reducing gap formation and inflammatory response, increasing the activity of endogenous cells, and formation of type III collagen.
Percutaneous Axillary Intra-aortic Balloon Pump Insertion Technique as Bridge to Advanced Heart Failure Therapy
Rosenbaum, Andrew , Jain, C. Charles , Shadrin, Ilya Y. , Hajj, Stephanie C. El , Sabbagh, Abdallah El , Behfar, Atta , Rosenbaum, Andrew N , Behfar, Atta , Hajj, Stephanie C. El

ASAIO Journal | September 6, 2020 | Volume: 67 | Issue: 4 | Pages: e81-e85

10.1097/mat.0000000000001259 Get It

In patients with advanced heart failure (HF), temporary mechanical circulator support (TMCS) is used to improve hemodynamics, via left ventricular unloading, and end-organ function as a bridge to definitive therapy. While listed for cardiac transplantation, use of TMCS may be prolonged, preventing adequate mobility. Here, we describe the technique for placement of a percutaneous axillary intra-aortic balloon pump (IABP) using single-site arterial access to facilitate ambulation and subsequent safe removal without surgery or a closure device. Retrospective review of the experience with this approach at a single institution between September 2017 and February 2020 documented feasibility and safety. Baseline demographics, hemodynamic data, and clinical outcomes were collected. Thirty-eight patients had a total of 56 IABPs placed. There were no significant access site or cerebrovascular complications. One fifth of IABPs (21.4%) had balloon failure or migration, requiring placement of a new device, though no patients had significant complications from balloon failure. The majority (81.6%) of patients in the cohort on axillary IABP support were ambulatory and ultimately received the intended therapy (63.2% transplant, 13.2% durable left ventricular assist device, 5.3% other cardiac surgery). Percutaneous, axillary IABP is feasible and associated with an acceptable complication rate as a bridge to definitive therapy.
Inadequate left ventricular unloading during ramp is associated with hospitalization or death during left ventricular assist device support
Rosenbaum, Andrew , Stulak, John M., Clavell, Alfredo L. , Behfar, Atta , Rosenbaum, Andrew N , Behfar, Atta

Artificial Organs | August 6, 2020 | Volume: 45 | Issue: 2 | Pages: 115-123

10.1111/aor.13792 Get It

AbstractA combined right and left‐sided heart catheterization (RHC/LHC) protocol was recently reported to optimize patients supported by left ventricular assist device (LVAD). Using this platform, we sought to evaluate the prognostic significance of several hemodynamic indices, including left ventricular end‐diastolic pressure (LVEDP) and transaortic gradient (peak aortic pressure ‐ peak left ventricular pressure in systole, TAG). We evaluated all patients undergoing RHC/LHC at our institution from 2015 through 2018, and comprehensive clinical data were obtained. Primary end points were (1) a composite outcome that included hospitalization or death and (2) 1‐year overall survival after catheterization. Forty‐two patients were included in the analysis. Optimization resulted in normalization of hemodynamic parameters; all variables were significantly improved from baseline (P ≤ .05). On univariate modeling, final LVEDP was associated with the primary end point (hazard ratio [HR], 1.2 per 1‐mm Hg increase; 95% CI, 1.1‐1.3; P = .002). After adjusting for LVAD speed, TAG, and cardiac index in a multivariate model, the association between LVEDP and the composite end point remained significant (HR, 1.2 per 1‐mm Hg increase; 95% CI, 1.1‐1.4; P = .001). In the setting of LVAD support, inadequate LV unloading was a significant marker of poor outcomes with time, suggesting that LVEDP is a central prognostic marker in this population.