Publications by authors named "Mark L Barr"

53 Publications

Equivalent outcomes with minimally invasive and sternotomy mitral valve repair for degenerative mitral valve disease.

J Card Surg 2021 Aug 28;36(8):2636-2643. Epub 2021 Apr 28.

Department of Surgery, Keck School of Medicine of USC, University of Southern California, Los Angeles, California, USA.

Background: Debate continues in regard to the optimal surgical approach to the mitral valve for degenerative disease.

Methods: Between February 2004 and July 2015, 363 patients underwent mitral valve repair for degenerative mitral valve disease via either sternotomy (sternotomy, n = 109) or small right anterior thoracotomy (minimally invasive, n = 259). Survival, need for mitral valve reoperation, and progression of mitral regurgitation more than two grades were compared between cohorts using time-based statistical methods and inverse probability weighting.

Results: Survival at 1, 5, and 10 years were 99.2, 98.3, and 96.8 for the sternotomy group and 98.1, 94.9, and 94.9 for the minimally invasive group (hazard ratio: 0.39, 95% confidence interval [CI] 0.11-1.30, p = .14). The cumulative incidence of need for mitral valve reoperation with death as a competing outcome at 1, 3, and 5 years were 2.7%, 2.7%, and 2.7% in the sternotomy cohort and 1.5%, 3.3%, and 4.1% for the minimally invasive group (subhazard ratio (SHR) 1.17, 95% CI: 0.33-4.20, p = .81). Cumulative incidence of progression of mitral regurgitation more than two grades with death as a competing outcome at 1, 3, and 5 years were 5.5%, 14.4%, and 44.5% for the sternotomy cohort and 4.2%, 9.7%, and 20.5% for the minimally invasive cohort (SHR: 0.67, 95% CI: 0.28-1.63, p = .38). Inverse probability weighted time-based analyses based on preoperative cohort assignment also demonstrated equivalent outcomes between surgical approaches.

Conclusions: Minimally invasive and sternotomy mitral valve repair in patients with degenerative mitral valve disease is associated with equivalent survival and repair durability.
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http://dx.doi.org/10.1111/jocs.15586DOI Listing
August 2021

Pediatric Living Lung Donor Transplant Candidates: Psychiatric Status of Utilized and Non-Utilized Donors.

J Clin Psychol Med Settings 2021 Apr 21. Epub 2021 Apr 21.

Department of Surgery, University of Southern California, Los Angeles, CA, USA.

Living donor lung (lobar) transplantation has greatly decreased in the past decade due to the success of the lung allocation score (LAS) system, instituted in 2005 by the Organ Procurement and Transplantation Network (OPTN). Between 1993 and 2006, 460 living lung donor transplants were performed in the United States with 369 donations occurring at the University of Southern California and Washington University in St. Louis. These two centers accounted for over 80% of all living donor lung transplants between 1994 and 2006. All potential donors received a psychological/psychiatric evaluation as part of the donor selection process, which is standard practice in the United States, Europe, and Asia. Utilized and non-utilized lung donors were compared in terms of their psychiatric history and present status. Results indicated that 31% (N = 54) of the total sample had a lifetime prevalence of a psychiatric disorder, which is less than that the 46% lifetime rate for the general population (Kessler in Arch Gen Psychiatry 62:593-602, 2005). This study did find that psychiatric history or status was not exclusion factor for transplant surgery in either group. This observation about psychiatric issues in potential living lung donors should be useful to transplant centers who utilize adult live donors of any solid organ type for pediatric recipients and in Japan where live donor lung transplants still represent a significant proportion of lung transplants (Date in J Thorac Dis 8: S631-S636, 2016).
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http://dx.doi.org/10.1007/s10880-021-09777-1DOI Listing
April 2021

Use of a Bluetooth tablet-based technology to improve outcomes in lung transplantation: A pilot study.

Am J Transplant 2020 12 13;20(12):3649-3657. Epub 2020 Jul 13.

Division of Pulmonary and Critical Care Medicine, Department of Medicine, University of Southern California, Los Angeles, California, USA.

The impact of remote patient monitoring platforms to support the postoperative care of solid organ transplant recipients is evolving. In an observational pilot study, 28 lung transplant recipients were enrolled in a novel postdischarge home monitoring program and compared to 28 matched controls during a 2-year period. Primary endpoints included hospital readmissions and total days readmitted. Secondary endpoints were survival and inflation-adjusted hospital readmission charges. In univariate analyses, monitoring was associated with reduced readmissions (incidence rate ratio [IRR]: 0.56; 95% confidence interval [CI]: 0.41-0.76; P < .001), days readmitted (IRR: 0.46; 95% CI: 0.42-0.51; P < .001), and hospital charges (IRR: 0.52; 95% CI: 0.51-0.54; P < .001). Multivariate analyses also showed that remote monitoring was associated with lower incidence of readmission (IRR: 0.38; 95% CI: 0.23-0.63; P < .001), days readmitted (IRR: 0.14; 95% CI: 0.05-0.37; P < .001), and readmission charges (IRR: 0.11; 95% CI: 0.03-0.46; P = .002). There were 2 deaths among monitored patients compared to 6 for controls; however, this difference was not significant. This pilot study in lung transplant recipients suggests that supplementing postdischarge care with remote monitoring may be useful in preventing readmissions, reducing subsequent inpatient days, and controlling hospital charges. A multicenter, randomized control trial should be conducted to validate these findings.
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http://dx.doi.org/10.1111/ajt.16154DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7754459PMC
December 2020

Invited Commentary.

Ann Thorac Surg 2018 04 23;105(4):1157-1159. Epub 2017 Dec 23.

Department of Cardiothoracic Surgery, Keck School of Medicine of USC, University of Southern California, 1520 San Pablo St, Ste 4300, Los Angeles, CA 90033. Electronic address:

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http://dx.doi.org/10.1016/j.athoracsur.2017.12.001DOI Listing
April 2018

Selective Aortic Arch and Root Replacement in Repair of Acute Type A Aortic Dissection.

Ann Thorac Surg 2018 Feb 3;105(2):505-512. Epub 2017 Nov 3.

Department of Surgery, Keck School of Medicine of the University of Southern California, Los Angeles, California. Electronic address:

Background: Controversy exists regarding the optimal extent of repair for type A aortic dissection. Our approach is to replace the ascending aorta, and only replace the aortic root or arch when intimal tears are present in those areas. We examined intermediate outcomes with this approach to acute type A aortic dissection repair.

Methods: Between March 2005 and October 2016, 195 patients underwent repair of acute type A aortic dissection. Repair was categorized by site of proximal and distal anastomosis and extent of repair. Mean follow-up was 31.0 ± 30.9 months. Kaplan-Meier analysis was used to assess survival. Multiple variable Cox proportional hazards modeling was utilized to identify factors associated with overall mortality.

Results: Overall survival was 85.1%, 83.9%, 79.1%, and 74.4% at 6, 12, 36, and 60 months, respectively. Eight patients required reintervention. The cumulative incidence of aortic reintervention at 1 year with death as a competing outcome was 3.95%. Multiple variable regression analysis identified factors such as age, preoperative renal failure, concomitant thoracic endograft, postoperative myocardial infarction and sepsis, and need for extracorporeal membrane oxygenation as predictive of overall mortality. Neither proximal or distal extent of repair, nor need for reintervention affected overall survival (proximal: hazard ratio 1.63, 95% confidence interval: 0.75 to 3.51, p = 0.22; distal: hazard ratio 1.12, 95% confidence interval: 0.43 to 2.97, p = 0.81; reintervention: hazard ratio 0.03, 95% confidence interval: 0.002 to 0.490, p < 0.01).

Conclusions: A selective approach to root and arch repair in acute type A aortic dissection is safe. If aortic reintervention is needed, survival does not appear to be affected.
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http://dx.doi.org/10.1016/j.athoracsur.2017.07.016DOI Listing
February 2018

Outcomes after mitral valve repair: A single-center 16-year experience.

J Thorac Cardiovasc Surg 2017 09 9;154(3):822-830.e2. Epub 2017 Feb 9.

Department of Surgery, Keck School of Medicine of USC, University of Southern California, Los Angeles, Calif.

Objective: To evaluate outcomes after mitral valve repair.

Methods: Between May 1999 and June 2015, 446 patients underwent mitral valve repair. Isolated mitral valve annuloplasty was excluded. A total of 398 (89%) had degenerative valve disease. Mean follow-up was 5.5 ± 3.8 years. Postoperative echocardiograms were obtained in 334 patients (75%) at a mean of 24.3 ± 13.7 months.

Results: Survival was 97%, 96%, 95%, and 94% at 1, 3, 5, and 10 years. Risk factor analysis showed age >60 years and nondegenerative etiology predict death (hazard ratio, 2.91; 95% confidence interval, 1.06-8.02, P = .038; and hazard ratio, 1.87; 95% confidence interval, 1.16-3.02, P = .010, respectively). Considering competing risks due to mortality, the cumulative incidence of reoperation was 2.8%, 4.2%, 5.1%, and 9.6% at 1, 3, 5, and 10 years. Competing risk proportional hazard survival regression identified nondegenerative etiology and previous cardiac surgery as predictors of reoperation, and posterior repair was protective (all P < .05). Cumulative incidence of progression of mitral regurgitation (2 or more grades) with mortality as a competing risk was 4.7%, 10.5%, 21.0%, and 35.8% at 1, 3, 5, and 10 years. Patients with previous sternotomy, repair or coronary artery bypass grafting, and concurrent tricuspid valve procedure or isolated anterior leaflet repair were more likely to develop progression of mitral regurgitation (all P < .05), and posterior leaflet repair was protective (P = .038). On multivariate analysis diabetes, previous coronary artery bypass grafting and concurrent tricuspid valve intervention predicted MR progression.

Conclusions: Mitral valve repair has excellent outcomes. Our results demonstrate failures appear to occur less in those who undergo posterior leaflet repair.
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http://dx.doi.org/10.1016/j.jtcvs.2017.01.047DOI Listing
September 2017

The Utility of Nurse-Managed Extracorporeal Life Support in an Adult Cardiac Intensive Care Unit.

Ann Thorac Surg 2017 Aug 10;104(2):510-514. Epub 2017 Feb 10.

Division of Cardiothoracic Surgery, Department of Surgery, Keck School of Medicine of the University of Southern California, Los Angeles, California.

Background: The use of extracorporeal life support (ECLS) worldwide has increased exponentially since 2009. The patient requiring ECLS demands an investment of hospital resources, including personnel. Educating bedside nurses to manage ECLS circuits broadens the availability of trained providers.

Methods: Experienced cardiothoracic intensive care unit (CTICU) nurses underwent training to manage ECLS circuits, including volume assessment, treatment of arterial blood gas values, the physiology of ECLS, and recognition of common emergencies. In addition to lectures and a written examination, simulation using water circuits and an ICU model allowed assessment of skills and understanding of concepts. Performance assessments were completed regularly at the bedside, and skills revalidation occurred every 6 months. A sequential cohort of 40 patients was tracked over 1 year.

Results: Despite doubling the census of ECLS patients in 1 year, management by specially trained CTICU nurses has positively affected patient care and outcomes. At a single institution, 40 patients had a median of 6 days (interquartile range, 2 to 226 days) of support in 2014, leading to 767 patient-days of support. Survival to hospital discharge increased to 45% in 2014. Most survivors were weaned from support. Neurologic injury was the most common cause of death, followed by failure to qualify for advanced therapies.

Conclusions: With on-going education and assessment, including crisis training, physiology, and cannulation strategies, CTICU nurses can safely operate ECLS circuits and can increase the availability of appropriately trained providers to accommodate the exponential increase in ECLS occurrences without negatively affecting outcomes and generally at a lower cost.
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http://dx.doi.org/10.1016/j.athoracsur.2016.11.005DOI Listing
August 2017

Assessment of segmental myocardial blood flow and myocardial perfusion reserve by adenosine-stress myocardial arterial spin labeling perfusion imaging.

J Magn Reson Imaging 2017 08 2;46(2):413-420. Epub 2017 Feb 2.

Ming Hsieh Department of Electrical Engineering, University of Southern California, Los Angeles, California, USA.

Purpose: To determine the feasibility of measuring increases in myocardial blood flow (MBF) and myocardial perfusion reserve (MPR) on a per-segment basis using arterial spin labeled (ASL) magnetic resonance imaging (MRI) with adenosine vasodilator stress in normal human myocardium.

Materials And Methods: Myocardial ASL scans at rest and during adenosine infusion were incorporated into a routine 3T MR adenosine-induced vasodilator stress protocol and were performed in 10 healthy human volunteers. Myocardial ASL was performed using single-gated flow-sensitive alternating inversion recovery (FAIR) tagging and balanced steady-state free precession (bSSFP) imaging at 3T. A T -prep blood oxygen level-dependent (BOLD) SSFP sequence was used to concurrently assess segmental myocardial oxygenation with BOLD signal intensity (SI) percent change in the same subjects.

Results: There was a statistically significant difference between MBF measured by ASL at rest (1.75 ± 0.86 ml/g/min) compared to adenosine stress (4.58 ± 2.14 ml/g/min) for all wall segments (P < 0.0001), yielding a per-segment MPR of 3.02 ± 1.51. When wall segments were divided into specific segmental myocardial perfusion territories (ie, anteroseptal, anterior, anterolateral, inferolateral, inferior, and inferoseptal), the differences between rest and stress regional MBF for each territory remained consistently statistically significant (P < 0.001) after correcting for multiple comparisons.

Conclusion: This study demonstrates the feasibility of measuring MBF and MPR on a segmental basis by single-gated cardiac ASL in normal volunteers. Second, this study demonstrates the feasibility of performing the ASL sequence and T -prepared SSFP BOLD imaging during a single adenosine infusion.

Level Of Evidence: 2 Technical Efficacy: Stage 1 J. MAGN. RESON. IMAGING 2017;46:413-420.
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http://dx.doi.org/10.1002/jmri.25604DOI Listing
August 2017

Double-gated myocardial ASL perfusion imaging is robust to heart rate variation.

Magn Reson Med 2017 05 30;77(5):1975-1980. Epub 2016 May 30.

Ming Hsieh Department of Electrical Engineering, University of Southern California, Los Angeles, California, USA.

Purpose: Cardiac motion is a dominant source of physiological noise (PN) in myocardial arterial spin labeled (ASL) perfusion imaging. This study investigates the sensitivity to heart rate variation (HRV) of double-gated myocardial ASL compared with the more widely used single-gated method.

Methods: Double-gating and single-gating were performed on 10 healthy volunteers (n = 10, 3F/7M; age, 23-34 years) and eight heart transplant recipients (n = 8, 1F/7M; age, 26-76 years) at rest in the randomized order. Myocardial blood flow (MBF), PN, temporal signal-to-noise ratio (SNR), and HRV were measured.

Results: HRV ranged from 0.2 to 7.8 bpm. Double-gating PN did not depend on HRV, while single-gating PN increased with HRV. Over all subjects, double-gating provided a significant reduction in global PN (from 0.20 ± 0.15 to 0.11 ± 0.03 mL/g/min; P = 0.01) and per-segment PN (from 0.33 ± 0.23 to 0.21 ± 0.12 mL/g/min; P < 0.001), with significant increases in global temporal SNR (from 11 ± 8 to 18 ± 8; P = 0.02) and per-segment temporal SNR (from 7 ± 4 to 11 ± 12; P < 0.001) without significant difference in measured MBF.

Conclusion: Single-gated myocardial ASL suffers from reduced temporal SNR, while double-gated myocardial ASL provides consistent temporal SNR independent of HRV. Magn Reson Med 77:1975-1980, 2017. © 2016 International Society for Magnetic Resonance in Medicine.
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http://dx.doi.org/10.1002/mrm.26282DOI Listing
May 2017

A comparison of aortic valve replacement via an anterior right minithoracotomy with standard sternotomy: a propensity score analysis of 492 patients.

Eur J Cardiothorac Surg 2016 Feb 6;49(2):456-63. Epub 2015 Mar 6.

Department of Surgery, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, USA.

Objectives: Right anterior minithoracotomy with central arterial cannulation is our preferred technique of minimally invasive aortic valve replacement (AVR). We compared perioperative outcomes with this technique to those via sternotomy.

Methods: Between March 1999 and December 2013, 492 patients underwent isolated AVR via either sternotomy (SAVR, n = 198) or minimally invasive right anterior thoracotomy (MIAVR, n = 294) in our institution. Univariate comparisons between groups were made to evaluate overall outcomes and adverse events. To control treatment selection bias, propensity scores were constructed from core patient characteristics. A propensity score-stratified analysis of outcome and adverse events was then performed.

Results: Overall mortality was 2.5 and 1.0% in the SAVR and MIAVR groups, respectively. Hospital and ICU stays were shorter, there was less intraoperative blood product usage, and fewer wound infections in the MIAVR group. There were no differences in other adverse events, including strokes. The composite end-point of alive and adverse event-free was significantly more common in the MIAVR group (83 vs 74%, P = 0.002). After adjusting for the propensity score, hospital and ICU stays remained shorter and intraoperative blood product usage remained less in the MIAVR group. There was no difference in mortality, stroke or other adverse events between groups.

Conclusion: Minimally invasive AVR via an anterior right thoracotomy with predominately central cannulation can be performed with morbidity and mortality similar to that of a sternotomy approach. There appear to be advantages to this minimally invasive approach when compared with sternotomy in terms of less intraoperative blood product usage, lower wound infection rates and decreased hospital stays. If mortality and the occurrence of adverse events are taken together, MIAVR may be associated with better outcomes. As minimally invasive AVR becomes more common, further long-term follow-up is needed and a prospective multicentre randomized trial would be warranted.
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http://dx.doi.org/10.1093/ejcts/ezv038DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4711701PMC
February 2016

Outcomes after pregnancy in living lobar lung transplantation.

Transplantation 2014 Oct;98(7):692-4

Pregnancy after lung transplantation has been described, but pregnancy after living donor lobar lung transplantation (LDLT) has not been reported. The aim of this study was to evaluate outcomes after pregnancy with LDLT and discuss current recommendations regarding pregnancy and lung transplantation. A total of four LDLT patients and five pregnancies were identified, all from our institution. No patient has developed worsening pulmonary function or acute or chronic rejection. The complications of pulmonary hypertension and rejection may be overestimated in this population, and recommendations for preventive sterilization at transplantation or abortion at the time of conception are likely unwarranted and unnecessary.
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http://dx.doi.org/10.1097/TP.0000000000000363DOI Listing
October 2014

Oscillatory shear stress induces mitochondrial superoxide production: implication of NADPH oxidase and c-Jun NH2-terminal kinase signaling.

Antioxid Redox Signal 2011 Sep 14;15(5):1379-88. Epub 2011 Apr 14.

Department of Biomedical Engineering and Cardiovascular Medicine, University of Southern California, Los Angeles, California 90089, USA.

Fluid shear stress is intimately linked with vascular oxidative stress and atherosclerosis. We posited that atherogenic oscillatory shear stress (OSS) induced mitochondrial superoxide (mtO2•-) production via NADPH oxidase and c-Jun NH(2)-terminal kinase (JNK-1 and JNK-2) signaling. In bovine aortic endothelial cells, OSS (±3 dyn/cm2) induced JNK activation, which peaked at 1 h, accompanied by an increase in fluorescein isothiocyanate-conjugated JNK fluorescent and MitoSOX Red (specific for mtO2•- production) intensities. Pretreatment with apocynin (NADPH oxidase inhibitor) or N-acetyl cysteine (antioxidant) significantly attenuated OSS-induced JNK activation. Apocynin further reduced OSS-mediated dihydroethidium and MitoSOX Red intensities specific for cytosolic O2•- and mtO2•- production, respectively. As a corollary, transfecting bovine aortic endothelial cells with JNK siRNA (siJNK) and pretreating with SP600125 (JNK inhibitor) significantly attenuated OSS-mediated mtO2•- production. Immunohistochemistry on explants of human coronary arteries further revealed prominent phosphorylated JNK staining in OSS-exposed regions. These findings indicate that OSS induces mtO2•- production via NADPH oxidase and JNK activation relevant for vascular oxidative stress.
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http://dx.doi.org/10.1089/ars.2010.3645DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3144427PMC
September 2011

Alveolar inflammation in cystic fibrosis.

J Cyst Fibros 2010 May 29;9(3):217-27. Epub 2010 Mar 29.

Institute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, Germany.

Background: In infected lungs of the cystic fibrosis (CF) patients, opportunistic pathogens and mutated cystic fibrosis transmembrane conductance regulator protein (CFTR) contribute to chronic airway inflammation that is characterized by neutrophil/macrophage infiltration, cytokine release and ceramide accumulation. We sought to investigate CF lung inflammation in the alveoli.

Methods: Lung tissue from 14 CF patients and four healthy individuals was analyzed for numbers of effector cells, elastin and collagen concentrations, inflammatory markers and density of Pseudomonas aeruginosa. Additionally, desmosine and isodesmosine concentrations were determined in 52 urine specimens from CF patients to estimate the burden of elastase activities in respiratory secretions.

Results: Elastin concentration was significantly decreased and collagen significantly increased in CF alveolar tissues as compared to age-matched, healthy individuals. Elastin split products were significantly increased in urine samples from patients with CF and correlated inversely with age, indicating local tissue remodelling due to elastin degradation by unopposed proteolytic enzymes. Alveolar inflammation was also characterized by a significant cell infiltration of neutrophils, macrophages and T cells, extensive nuclear factor-kappaB and insulin-like growth factor-1 activation in various cell types and increased intercellular adhesion molecule-1 expression, and increased numbers of myofibroblasts. Additionally, ceramide accumulated in type II alveolar epithelial cells, lacking CFTR. P. aeruginosa organisms were rarely present in inflamed alveoli.

Conclusions: Chronic inflammation and remodeling is present in alveolar tissues of the CF lung and needs to be addressed by anti-inflammatory therapies.
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http://dx.doi.org/10.1016/j.jcf.2010.03.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2883667PMC
May 2010

Lung transplantation for cystic fibrosis.

Proc Am Thorac Soc 2009 Dec;6(8):619-33

Department of Mathematics, University of Utah, Salt Lake City, Utah 84112, USA.

Lung transplantation is a complex, high-risk, potentially life-saving therapy for the end-stage lung disease of cystic fibrosis (CF). The decision to pursue transplantation involves comparing the likelihood of survival with and without transplantation as well as assessing the effect of wait-listing and transplantation on the patient's quality of life. Although recent population-based analyses of the US lung allocation system for the CF population have raised controversies about the survival benefits of transplantation, studies from the United Kingdom and Canada have suggested a definite survival advantage for those receiving transplants. In response to these and other controversies, leaders in transplantation and CF met together in Lansdowne, Virginia, to consider the state of the art in lung transplantation for CF in an international context, focusing on advances in surgical technique, measurement of outcomes, use of prognostic criteria, variations in local control over listing, and prioritization among the United States, Canada, the United Kingdom, and The Netherlands, patient adherence before and after transplantation and other issues in the broader context of lung transplantation. Finally, the conference members carefully considered how efforts to improve outcomes for lung transplantation for CF lung disease might best be studied. This Roundtable seeks to communicate the substance of our discussions.
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http://dx.doi.org/10.1513/pats.2009008-088TLDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2797068PMC
December 2009

CT-guided tube pericardiostomy: a safe and effective technique in the management of postsurgical pericardial effusion.

AJR Am J Roentgenol 2009 Oct;193(4):W314-20

Department of Radiology, University of Southern California Keck School of Medicine, University Hospital, Los Angeles, CA 90033, USA.

Objective: The purpose of this study was to analyze the efficacy and examine the competitive cost of CT-guided tube pericardiostomy in the management of symptomatic postsurgical pericardial effusion.

Materials And Methods: Over a 4-year period, 36 patients with symptomatic pericardial effusion were treated with CT-guided percutaneous placement of an indwelling pericardial catheter, for a total of 39 CT-guided tube pericardiostomy procedures. Thirty-three patients (92%) had undergone major cardiothoracic surgery, and three patients (8%) had undergone minimally invasive procedures. The medical records were retrospectively reviewed for clinical presentation, surgical history, imaging studies performed, procedural details, fluid characterization, and outcome. Charge comparison was performed with the American Medical Association Current Procedural Terminology codes and information acquired from the billing department at our facility.

Results: All 39 CT-guided tube pericardiostomy procedures were performed successfully without clinically significant complications. After 33 of the 39 procedures (85%), symptoms did not recur after the catheter was removed. Three of 36 patients (8%) had a recurrence of pericardial effusion. Comparison of procedure charges showed an 89% saving over intraoperative pericardial window procedures and no significant difference compared with ultrasound-guided tube pericardiostomy. Eight patients (21% of procedures) needed pleural drainage procedures, all of which were performed in the CT suite immediately after the tube pericardiostomy procedure.

Conclusion: CT-guided tube pericardiostomy is a safe and effective alternative to surgical drainage in the care of patients with clinically significant pericardial effusion after cardiothoracic surgery and has the additional benefit of substantial cost savings.
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http://dx.doi.org/10.2214/AJR.08.1834DOI Listing
October 2009

Extracorporeal photopheresis: past, present, and future.

J Am Acad Dermatol 2009 Oct 7;61(4):652-65. Epub 2009 Aug 7.

Department of Dermatology, Medical University of Vienna, Vienna, Austria.

Extracorporeal photopheresis (ECP) is a leukapheresis-based therapy that uses 8-methoxypsoralen and ultraviolet A irradiation. Used alone or in combination with biological agents, ECP is an established and effective therapy for advanced cutaneous T-cell lymphoma. ECP has also shown promising efficacy in a number of other severe and difficult-to-treat conditions, including systemic sclerosis, graft-versus-host disease, prevention and treatment of rejection in solid organ transplantation, and Crohn disease. Furthermore, the use of ECP in some of these conditions may allow a significant reduction in the use of systemic steroids and other immunosuppressants, reducing long-term morbidity and mortality. The accumulated experience shows ECP to be well tolerated, with no clinically significant side effects. Progress is also being made in the search for understanding of the mechanisms of action of ECP, which will ultimately facilitate improvements in the use of this therapy.
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http://dx.doi.org/10.1016/j.jaad.2009.02.039DOI Listing
October 2009

Genetic modulation of CD44 expression by intragraft fibroblasts.

J Biochem 2008 Nov 6;144(5):571-80. Epub 2008 Sep 6.

Department of Surgery, Comprehensive Transplant Center, Cedars-Sinai Medical Center, Los Angeles, CA, USA.

This study investigated the genetic composition and the functional implication of CD44 species expressed by intragraft fibroblasts. An LEW-to-F344 heart transplant model of chronic rejection was used. Intragraft fibroblasts recovered from the chronically rejecting allografts displayed a 4.5-fold increase in expression of CD44 mRNA when compared with that of the fibroblasts isolated from non-rejecting heart allografts (P < 0.01). The intragraft fibroblasts preferentially expressed CD44 variant isoforms containing v1 exon transcript. Automated nucleotide sequence analysis revealed that the majority (90.12%) of the CD44 v1 isoforms expressed by the rejecting graft fibroblasts were encoded by a mutated CD44 mRNA, which contained two point mutations and a codon deletion in the v1 coding region. Histochemistry demonstrated a massive deposition of extracellular HA in the rejecting heart allografts. Hyaluronic acid (HA) was able to promote in vitro fibroblast adhesion, migration in a CD44-dependent manner, and survival in a serum-free culture condition. The study concludes that up-regulation of CD44 v1 isoforms expressed by the intragraft fibroblasts is associated with an increase in the deposition of extracellular HA, the principal ligand for CD44, in the allografts, suggesting that CD44-HA interaction plays an important role in regulating fibroblast recruitment and growth in allografts developing chronic rejection.
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http://dx.doi.org/10.1093/jb/mvn106DOI Listing
November 2008

Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis.

Nat Med 2008 Apr 30;14(4):382-91. Epub 2008 Mar 30.

Department of Molecular Biology, Hufelandstrasse 55, University of Duisburg-Essen, 45122 Essen, Germany.

Microbial lung infections are the major cause of morbidity and mortality in the hereditary metabolic disorder cystic fibrosis, yet the molecular mechanisms leading from the mutation of cystic fibrosis transmembrane conductance regulator (CFTR) to lung infection are still unclear. Here, we show that ceramide age-dependently accumulates in the respiratory tract of uninfected Cftr-deficient mice owing to an alkalinization of intracellular vesicles in Cftr-deficient cells. This change in pH results in an imbalance between acid sphingomyelinase (Asm) cleavage of sphingomyelin to ceramide and acid ceramidase consumption of ceramide, resulting in the higher levels of ceramide. The accumulation of ceramide causes Cftr-deficient mice to suffer from constitutive age-dependent pulmonary inflammation, death of respiratory epithelial cells, deposits of DNA in bronchi and high susceptibility to severe Pseudomonas aeruginosa infections. Partial genetic deficiency of Asm in Cftr(-/-)Smpd1(+/-) mice or pharmacological treatment of Cftr-deficient mice with the Asm blocker amitriptyline normalizes pulmonary ceramide and prevents all pathological findings, including susceptibility to infection. These data suggest inhibition of Asm as a new treatment strategy for cystic fibrosis.
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http://dx.doi.org/10.1038/nm1748DOI Listing
April 2008

Outcomes after lung retransplantation in the modern era.

Am J Respir Crit Care Med 2008 Jan 27;177(1):114-20. Epub 2007 Sep 27.

Department of Medicine, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA.

Rationale: Characteristics of and survival estimates for recipients of lung retransplantation in the modern era are unknown.

Objectives: To compare lung retransplant patients in the modern era with historical retransplant patients, to compare retransplant patients with initial transplant patients in the modern era, and to determine the predictors of the risk of death after lung retransplantation.

Methods: We performed a retrospective cohort study of patients who underwent lung retransplantation between January 2001 and May 2006 in the United States (modern retransplant cohort). The characteristics and survival of this cohort were compared with those of patients who underwent first lung retransplantation between January 1990 and December 2000 (historical retransplant cohort) and patients who underwent initial lung transplantation between January 2001 and May 2006 (modern initial transplant cohort).

Measurements And Main Results: Modern retransplant recipients (n = 205) had a lower risk of death compared with that of the historical retransplant cohort (n = 184) (hazard ratio, 0.7; 95% confidence interval, 0.5-0.9; P = 0.006). However, modern retransplant recipients had a higher risk of death than that of patients who underwent initial lung transplantation (n = 5,657) (hazard ratio, 1.3; 95% confidence interval, 1.2-1.5; P = 0.001), which appeared to be explained by a higher prevalence of certain comorbidities. Retransplantation at less than 30 days after the initial transplant procedure was associated with worse survival.

Conclusions: Outcomes after lung retransplantation have improved; however, retransplantation continues to pose an increased risk of death compared with the initial transplant procedure. Retransplantation early after the initial transplant poses a particularly high mortality risk.
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http://dx.doi.org/10.1164/rccm.200707-1132OCDOI Listing
January 2008

Hemodynamics influences vascular peroxynitrite formation: Implication for low-density lipoprotein apo-B-100 nitration.

Free Radic Biol Med 2007 Feb 21;42(4):519-29. Epub 2006 Nov 21.

Department of Biomedical Engineering and Cardiovascular Medicine, University of Southern California, Los Angeles, CA 90081, USA.

Hemodynamics, specifically, fluid shear stress, modulates the focal nature of atherogenesis. Superoxide anion (O2(-.)) reacts with nitric oxide (.NO) at a rapid diffusion-limited rate to form peroxynitrite (O2(-.) + .NO-->ONOO(-)). Immunohistostaining of human coronary arterial bifurcations or curvatures, where OSS develops, revealed the presence of nitrotyrosine staining, a fingerprint of peroxynitrite; whereas in straight segments, where PSS occurs, nitrotyrosine was absent. We examined vascular nitrative stress in models of oscillatory (OSS) and pulsatile shear stress (PSS). Bovine aortic endothelial cells (BAEC) were exposed to fluid shear stress that simulates arterial blood flow: (1) PSS at a mean shear stress (tau(ave)) of 23 dyn cm(-2) and a temporal gradient (partial differential(tau)/partial differential(t)) at 71 dyn cm(-2) s(-1), and (2) OSS at tau(ave) = 0.02 dyn cm(- 2) and partial differential(tau)/partial differential(t) = +/- 3.0 dyn cm(-2) s(-1) at a frequency of 1 Hz. OSS significantly up-regulated one of the NADPH oxidase subunits (NOx4) expression accompanied with an increase in O2(-.) production. In contrast, PSS up-regulated eNOS expression accompanied with .NO production (total NO(2)(-) and NO(3)(-)). To demonstrate that O2(-.) and .NO are implicated in ONOO(-) formation, we added low-density lipoprotein cholesterol (LDL) to the medium in which BAEC were exposed to the above flow conditions. The medium was analyzed for LDL apo-B-100 nitrotyrosine by liquid chromatography electrospray ionization tandem mass spectrometry (LC/ESI/MS/MS). OSS induced higher levels of 3-nitrotyrosine, dityrosine, and o-hydroxyphenylalanine compared with PSS. In the presence of ONOO(-), specific apo-B-100 tyrosine residues underwent nitration in the alpha and beta helices: alpha-1 (Tyr(144)), alpha-2 (Tyr(2524)), beta-2 (Tyr(3295)), alpha-3 (Tyr(4116)), and beta-2 (Tyr(4211)). Hence, the characteristics of shear stress in the arterial bifurcations influenced the relative production of O2(-.) and .NO with an implication for ONOO(-) formation as evidenced by LDL protein nitration.
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http://dx.doi.org/10.1016/j.freeradbiomed.2006.11.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2561143PMC
February 2007

Rat chemokine CXCL11: structure, tissue distribution, function and expression in cardiac transplantation models.

Mol Cell Biochem 2007 Feb 31;296(1-2):1-9. Epub 2007 Jan 31.

Cardiothoracic Surgery, The Saban Research Institute of Childrens Hospital Los Angeles, The Keck School of Medicine, University of Southern California, Los Angeles, CA 90027, USA.

CXCL11 is thought to play a critical role in allograft rejection. To clarify the role of CXCL11 in the rat transplantation model, we cloned CXCL11 cDNA from rat liver tissue and used it to study CXCL11 structure, function and expression. The rat CXCL11 gene encodes a protein of 100 amino acids and spans approximately a 2.8 kb DNA segment containing 4 exons in the protein coding region. Tissue distribution of rat CXCL11 was analyzed by quantitative RT-PCR and showed that rat CXCL11 mRNA is expressed in various tissues and, in particular, at high levels in the spleen and lymph nodes. COS-1 cells were transfected with a plasmid vector encoding rat CXCL11 and used to study CXCL11 effects on cell migration and internalization of CXCR3, the CXCL11 receptor. The recombinant CXCL11 showed chemotactic properties and induced CXCR3 internalization in CD4(+) T cells. Expression of CXCL11 mRNA also was measured in rat acute (ACI to LEW) and chronic (LEW to F344) heart transplant rejection models. CXCL11 mRNA expression in allografts increased in both models, compared with controls, and was primarily observed in infiltrating macrophages and donor endothelial cells. These results indicate that, like the other CXCR3 chemokines, rat CXCL11 seems to have a role in the homing of CD4(+) T cells in both acute and chronic rejection models of heart allotransplantation.
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http://dx.doi.org/10.1007/s11010-005-9010-9DOI Listing
February 2007

Multicenter retrospective analysis of cardiovascular risk factors affecting long-term outcome of de novo cardiac transplant recipients.

J Heart Lung Transplant 2006 Sep 18;25(9):1063-9. Epub 2006 Jul 18.

University of California at Los Angeles, Los Angeles, California 90095, USA.

Background: Previous risk factor studies in cardiac transplant patients have analyzed pre-transplant risk factors as they relate to outcomes. This study is the first in-depth multicenter assessment of ongoing post-transplant risk factors in heart transplant patients and their impact on 5-year outcomes.

Methods: We reviewed 280 heart transplant patients who survived > 1 year for the impact of post-transplant risk factors (hyperlipidemia, hypertension, diabetes, body mass index [BMI] and renal dysfunction: 8 to 18 possible measurements over 5 years) on outcomes, including death, cardiac allograft vasculopathy (CAV) and non-fatal major adverse cardiac events (NF-MACE).

Results: Upon multivariate Cox regression analysis, significant findings were high total-cholesterol for NF-MACE (relative risk [RR] = 4.34, confidence interval [CI] 1.35 to 13.98, p = 0.01), presence of diabetes for NF-MACE (RR = 3.96, CI 1.24 to 12.65, p = 0.02) and high serum creatinine for graft death (RR = 1.59, CI 1.35 to 1.87, p < 0.001). No covariates were found to be significant for CAV. Other significant risk factors by univariate Cox regression models with time-dependent covariates included BMI > or = 33 for graft death.

Conclusions: Post-transplant risk factors of hypercholesterolemia and diabetes are associated with NF-MACE, whereas high serum creatinine and BMI > or = 33 are associated with graft death. Risk factor modification, including direct therapy to minimize risk factors, should be considered.
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http://dx.doi.org/10.1016/j.healun.2006.05.001DOI Listing
September 2006

Transfer of regulatory T cells generated ex vivo modifies graft rejection through induction of tolerogenic CD4+CD25+ cells in the recipient.

Int Immunol 2006 Feb 13;18(2):279-89. Epub 2006 Jan 13.

Division of Rheumatology and Immunology, Department of Medicine, 2011 Zonal Avenue, HMR 711.

Certain CD4+CD25+ T cells can induce and maintain T-cell non-responsiveness to donor alloantigens and have therapeutic potential in solid organ transplantation. Peripheral CD4+CD25- cells alloactivated with IL-2 and transforming growth factor beta (TGF-beta) ex vivo express the transcription factor FoxP3, and become potent antigen-specific CD4+CD25- suppressor cells. Here we report that the transfer of TGF-beta-induced regulatory CD4+ and CD8+ T cells (Tregs) co-incident with transplantation of a histoincompatible heart resulted in extended allograft survival. To account for this result, we injected non-transplanted mice with a single dose of CD4+ and CD8+ Tregs and transferred donor cells every 2 weeks to mimic the continuous stimulation of a transplant. We observed increased splenic CD4+CD25+ cells that were of recipient origin. These cells rendered the animals non-responsive to donor alloantigens by an antigen-specific and cytokine-dependent mechanism of action. Both the increased number of CD4+CD25+ cells and their tolerogenic effect were dependent on continued donor antigen boosting. Thus, Tregs generated ex vivo can act like a vaccine that generates host suppressor cells with the potential to protect MHC-mismatched organ grafts from rejection.
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http://dx.doi.org/10.1093/intimm/dxh368DOI Listing
February 2006

Contribution of mesenchymal progenitor cells to tissue repair in rat cardiac allografts undergoing chronic rejection.

J Heart Lung Transplant 2005 Dec 15;24(12):2160-9. Epub 2005 Sep 15.

Comprehensive Transplant Center, Department of Surgery, Cedars-Sinai Medical Center, Los Angeles, California 90048, USA.

Background: Mesenchymal progenitor cells (MPC) have recently been demonstrated to actively migrate into cardiac allografts during chronic rejection. This study examines the role of MPC in tissue repair of heart allografts in a rat model of chronic rejection.

Methods: The potential of a rat MPC line (Ap8c3) to differentiate to myofibroblasts and cardiomyocytes was studied in differentiation cultures. Ap8c3 cells tagged with an enhanced green fluorescent protein (eGFP) reporter gene were engrafted into Fischer 344 (F344) recipients of Lewis (LEW) cardiac allografts. Development of intragraft MPC into scar-forming fibroblasts and cardiomyocytes was studied using immunohistochemistry.

Results: Ap8c3 cells contain fibroblast progenitors (FP) positive for P07 antibody. Transforming growth factor (TGF)-beta stimulation promoted FP to terminally differentiate into myofibroblasts, which express alpha-smooth muscle actin (alphaSMA). In cardiac differentiation culture, Ap8c3 cells were induced by 5-azatiditin (5-aza) to form tropomyosin+ myotubes, and to express mRNA encoding for cardiac troponin I (TnI) and alpha-myosin heavy chain (alphaMHC). Transfusion of eGFP+ Ap8c3 cells to F344 recipients resulted in migration of eGFP(+) cells into LEW heart allografts, as well as homing of the eGFP+ MPC to bone marrow. The majority of eGFP+ cells in the heart allografts appeared to be vimentin-expressing fibroblasts. Foci of eGFP+ myocardium were also detected in all heart allografts, with eGFP+ cardiomyocytes representing 4.8 +/- 1.2% of the allografted eGFP+ cells.

Conclusions: The data suggest that rat MPC participate in tissue repair in heart allografts by giving rise to scar-forming myofibroblasts and cardiomyocytes.
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http://dx.doi.org/10.1016/j.healun.2005.05.017DOI Listing
December 2005

Transforming growth factor-beta/interleukin-2-induced regulatory CD4+ T cells prolong cardiac allograft survival in rats.

J Heart Lung Transplant 2005 Dec 2;24(12):2153-9. Epub 2005 Nov 2.

Department of Cardiothoracic Surgery, University of Southern California, Children's Hospital Los Angeles, Los Angeles, California 90027, USA.

Background: Treatment of naive CD4+ T cells in vitro with transforming growth factor-beta (TGF-beta) or TGF-beta/interleukin-2 (IL-2), combined with stimulation in a mixed lymphoid culture (MLC), has been shown to generate CD4+ CD25+ regulatory T cells. However, little is known about the effect of these regulatory T cells on cardiac allograft survival in vivo.

Methods: CD4+ CD25+ T cells were generated from Lewis (LEW) rat spleen through a primary MLC with TGF-beta (10 ng/ml) or TGF-beta/IL-2 (10 U/ml). The effect of adoptive transfer of the CD4+ CD25+ T cells (5.0 x 10(7)) was evaluated using an animal model of ACI rat cardiac allograft survival in LEW recipients.

Results: The MLC with TGF-beta or TGF-beta/IL-2 generated CD4+ CD25+ regulatory T cells, which suppressed the cytotoxic activity of LEW spleen T cells against irradiated ACI spleen cells in vitro. Adoptive transfer of the CD4+ CD25+ regulatory T cells intravenously to naive syngeneic recipients significantly prolonged the ACI cardiac allograft survival (N = 6, 13.5 +/- 3.4 days) compared with the control group (N = 6, 5.0 +/- 0.6 days).

Conclusions: Intravenous administration of CD4+ CD25+ regulatory T cells, successfully generated by TGF-beta/IL-2 treatment, had a significant effect on cardiac allograft survival in this rat model. Adoptive transfer of regulatory T cells may represent a novel approach for preventing allograft rejection.
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http://dx.doi.org/10.1016/j.healun.2005.07.007DOI Listing
December 2005

Pleural space problems after living lobar transplantation.

J Heart Lung Transplant 2005 Dec 28;24(12):2086-90. Epub 2005 Sep 28.

Department of Cardiothoracic Surgery, University of Southern California Keck School of Medicine, Los Angeles, California 90003, USA.

Background: We reviewed our experience with adult living lobar lung transplant (LL) recipients to assess whether size and shape mismatch of the donor organ to the recipient pre-disposes to the development of pleural space problems (PSP).

Methods: Eighty-seven LL were performed on 84 adult recipients from 1993 through 2003. Seventy-six patients had cystic fibrosis. Patient records were examined for PSP, defined as air leak or bronchopleural fistula for more than 7 days; pneumothorax, loculated pleural effusions, or empyema in 68 patients for which complete data were available.

Results: There were 24 PSP identified for an overall incidence of 35%. The most common PSP was air leak/bronchopleural fistula, accounting for 38% of PSP. The second most common PSP was loculated pleural effusion (21% of PSP). Empyema was uncommon (2 patients, 3% of total patients) in our series of patients despite the large population of cystic fibrosis patients. In 4 of these patients, computed tomography-guided drainage was used for loculated effusions after chest tube removal. Three LL patients underwent surgery for persistent air leak and required muscle flap repair. One of these required subsequent omental transfer. Two LL patients required decortication for empyema. Many patients with PSP could be managed without further surgical intervention (14/24 patients). Donor-recipient height mismatch was not significantly different between PSP and non-PSP patients (p = 0.53).

Conclusions: The incidence of PSP in LL recipients is similar to that reported in the literature on cadaveric transplant recipients. The relatively small lobe in the potentially contaminated chest cavity of cystic fibrosis recipients does not significantly pre-dispose to development of empyema despite immunosuppression. Many PSP can be managed non-operatively, although early aggressive intervention for large air leaks and judicious chest tube management are essential for a good outcome.
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http://dx.doi.org/10.1016/j.healun.2005.06.013DOI Listing
December 2005

The role of the hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix.

Stem Cells 2006 Apr 23;24(4):928-35. Epub 2005 Nov 23.

Comprehensive Transplant Center, Department of Surgery, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Los Angeles, California 90048, USA.

In a previous investigation, we demonstrated that mesenchymal stem cells (MSCs) actively migrated to cardiac allografts and contributed to graft fibrosis and, to a lesser extent, to myocardial regeneration. The cellular/molecular mechanism responsible for MSC migration, however, is poorly understood. This paper examines the role of CD44-hyaluronan interaction in MSC migration, using a rat MSC line Ap8c3 and mouse CD44-/- or CD44+/+ bone marrow stromal cells (BMSCs). Platelet-derived growth factor (PDGF) stimulation of MSC Ap8c3 cells significantly increased the levels of cell surface CD44 detected by flow cytometry. The CD44 standard isoform was predominantly expressed by Ap8c3 cells, accounting for 90% of the CD44 mRNA determined by quantitative real-time polymerase chain reaction. Mouse CD44-/- BMSCs bonded inefficiently to hyaluronic acid (HA), whereas CD44+/+ BMSC and MSC Ap8c3 adhered strongly to HA. Adhesions of MSC Ap8c3 cells to HA were suppressed by anti-CD44 antibody and by CD44 small interfering RNA (siRNA). HA coating of the migration chamber significantly promoted passage of CD44+/+ BMSC or Ap8c3 cells, but not CD44-/- BMSCs, through the insert membranes (p < .01). Migration of MSC Ap8c3 was significantly inhibited by anti-CD44 antibodies (p < .01) and to a lesser extent by CD44 siRNA (p = .05). The data indicate that MSC Ap8c3 cells, in response to PDGF stimulation, express high levels of CD44 standard (CD44s) isoform, which facilitates cell migration through interaction with extracellular HA. Such a migratory mechanism could be critical for recruitment of MSCs into wound sites for the proposition of tissue regeneration, as well as for migration of fibroblast progenitors to allografts in the development of graft fibrosis.
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http://dx.doi.org/10.1634/stemcells.2005-0186DOI Listing
April 2006

The ethics of living donor lung transplantation.

Thorac Surg Clin 2005 Nov;15(4):519-25

Department of Cardiothoracic Surgery, University of Southern California, Los Angeles, CA 90027, USA.

A constant awareness of the risk to the living donors must be maintained with any living donor organ transplantation program, and comprehensive short- and long-term follow-up should be strongly encouraged to maintain the viability of these potentially life-saving procedures. There has been no perioperative or long-term mortality following lobectomy for living lobar lung transplantation, and perioperative risks associated with donor lobectomy seem to be similar to those seen with standard lung resections. These risks might increase, however, if the procedure is offered on an occasional basis and not within a well-established program. The long-term outcomes and functional effects of lobar donation raise important questions that are unanswered. This has proved difficult to follow closely, because of the fact that many donors live far from the transplant medical center and are reluctant to return for routine follow-up evaluation. The death of a recipient can further exacerbate this situation, because there is reluctance to insist on further routine examinations for a grieving donor. Prospective donors must be informed of the morbidity associated with lobectomy and the potential for mortality, and for potential negative recipient outcomes in regard to life expectancy and quality of life after transplantation. Although cadaveric transplantation must be considered because of the risk to the donors, living lobar lung transplantation should continue to be used under properly selected circumstances. The results reported by the authors' group and others are important if this procedure is to be considered as an option at more pulmonary transplant centers in view of the institutional, regional, and international differences in the philosophic and ethical acceptance of the use of living organ donors for transplantation. The integration of ethical discussion into topics that are relevant and of interest to thoracic surgeons, such as living lung donation, is a recent and welcome event. Many of the clinical situations that thoracic surgeons deal with on a daily basis have important and complex ethical implications, and there has been little training to deal effectively with these issues. This is changing as invited discussions on ethically compelling topics are finding their way into journals and the programs of national meetings. What may be of more importance, however, is the development of an ethics curriculum for those training in the specialty. The core curriculum recommended by the Thoracic Surgical Directors Association (which represents the leadership of the 89 approved residency training programs in the United States) has one lecture pertaining to ethics out of the several hundred offerings in its requisite curriculum. It is hoped that this will change in the near future.
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http://dx.doi.org/10.1016/j.thorsurg.2005.06.003DOI Listing
November 2005
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