Publications by authors named "Benjamin Levi"

245 Publications

A randomized control trial of a child abuse mandated reporter training: Knowledge and attitudes.

Child Abuse Negl 2021 Apr 23;117:105033. Epub 2021 Apr 23.

Pennsylvania State College of Medicine, Hershey, PA, United States.

Background: Despite being well-positioned to identify maltreatment in the children that they provide care for and being legally required to report suspected child maltreatment, early childhood professionals (ECPs) make a limited proportion of reports to child protective services. It is critical to identify evidence-based interventions to improve the reporting practices of this group of mandated reporters allowing for the better protection of children from maltreatment.

Objective: The goal of the present study was to determine if iLookOut, an online child abuse identification and reporting training for ECPs, results in differential gains in knowledge and attitudes towards child abuse and its reporting among ECPs, as compared to an online standard training.

Participants And Setting: Both interventions were completed online by participants recruited from licensed child care programs in Southern Maine from October 2017 to January 2020. Eligibility criteria included being at least 18 years of age, English-speaking, and working as paid or volunteer staff at a licensed child care program taking care of children 5 years of age or younger. Of the 1152 enrolled individuals, 1094 provided complete pre- and post-intervention data.

Methods: A randomized controlled trial comparing iLookOut with an online standard training.

Results: ECPs who completed iLookOut significantly outperformed those who completed Standard mandated reporter training in terms of both knowledge (d=1.09 vs. 0.67) and attitudes (d=0.67 vs. 0.54) relative to pre-test scores.

Conclusions: iLookOut is a promising candidate for widespread use in meeting the need for evidence-based training on child abuse and its reporting.
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http://dx.doi.org/10.1016/j.chiabu.2021.105033DOI Listing
April 2021

High Frequency Spectral Ultrasound Imaging Detects Early Heterotopic Ossification in Rodents.

Stem Cells Dev 2021 May 19;30(9):473-484. Epub 2021 Apr 19.

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Heterotopic ossification (HO) is a devastating condition in which ectopic bone forms inappropriately in soft tissues following traumatic injuries and orthopedic surgeries as a result of aberrant mesenchymal progenitor cell (MPC) differentiation. HO leads to chronic pain, decreased range of motion, and an overall decrease in quality of life. While several treatments have shown promise in animal models, all must be given during early stages of formation. Methods for early determination of whether and where endochondral ossification/soft tissue mineralization (HO anlagen) develop are lacking. At-risk patients are not identified sufficiently early in the process of MPC differentiation and soft tissue endochondral ossification for potential treatments to be effective. Hence, a critical need exists to develop technologies capable of detecting HO anlagen soon after trauma, when treatments are most effective. In this study, we investigate high frequency spectral ultrasound imaging (SUSI) as a noninvasive strategy to identify HO anlagen at early time points after injury. We show that by determining quantitative parameters based on tissue organization and structure, SUSI identifies HO anlagen as early as 1-week postinjury in a mouse model of burn/tenotomy and 3 days postinjury in a rat model of blast/amputation. We analyze single cell RNA sequencing profiles of the MPCs responsible for HO formation and show that the early tissue changes detected by SUSI match chondrogenic and osteogenic gene expression in this population. SUSI identifies sites of soft tissue endochondral ossification at early stages of HO formation so that effective intervention can be targeted when and where it is needed following trauma-induced injury. Furthermore, we characterize the chondrogenic to osteogenic transition that occurs in the MPCs during HO formation and correlate gene expression to SUSI detection of the HO anlagen.
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http://dx.doi.org/10.1089/scd.2021.0011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8106252PMC
May 2021

Novel Lineage-Tracing System to Identify Site-Specific Ectopic Bone Precursor Cells.

Stem Cell Reports 2021 Mar 18;16(3):626-640. Epub 2021 Feb 18.

Center for Organogenesis and Trauma, Department of Surgery, University of Texas Southwestern, 6000 Harry Hines Boulevard, Dallas, TX 75235, USA. Electronic address:

Heterotopic ossification (HO) is a form of pathological cell-fate change of mesenchymal stem/precursor cells (MSCs) that occurs following traumatic injury, limiting range of motion in extremities and causing pain. MSCs have been shown to differentiate to form bone; however, their lineage and aberrant processes after trauma are not well understood. Utilizing a well-established mouse HO model and inducible lineage-tracing mouse (Hoxa11-CreER;ROSA26-LSL-TdTomato), we found that Hoxa11-lineage cells represent HO progenitors specifically in the zeugopod. Bioinformatic single-cell transcriptomic and epigenomic analyses showed Hoxa11-lineage cells are regionally restricted mesenchymal cells that, after injury, gain the potential to undergo differentiation toward chondrocytes, osteoblasts, and adipocytes. This study identifies Hoxa11-lineage cells as zeugopod-specific ectopic bone progenitors and elucidates the fate specification and multipotency that mesenchymal cells acquire after injury. Furthermore, this highlights homeobox patterning genes as useful tools to trace region-specific progenitors and enable location-specific gene deletion.
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http://dx.doi.org/10.1016/j.stemcr.2021.01.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7940250PMC
March 2021

Teamwork at the Bench: Strategies for Collaborative Surgical Science in a Pandemic.

J Surg Res 2021 05 4;261:39-42. Epub 2021 Jan 4.

Center for Basic and Translational Science (CBATS), Michigan Medicine, Ann Arbor, Michigan; Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Texas.

The Center for Basic and Translational Science was formed to address the unique challenges faced by surgeon-scientists. Shortly after its inception, COVID-19 upended research workflows at our institution. We discuss how the collaborative Center for Basic and Translational Science framework was adapted to support laboratories during the pandemic by assisting with ramp-down, promoting mentorship and community building, and maintaining research productivity.
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http://dx.doi.org/10.1016/j.jss.2020.12.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8026522PMC
May 2021

Effect of Advance Care Planning on Surrogate Decision Makers' Preparedness for Decision Making: Results of a Mixed-Methods Randomized Controlled Trial.

J Palliat Med 2020 Dec 29. Epub 2020 Dec 29.

College of Medicine, Penn State University, Hershey, Pennsylvania, USA.

Advance care planning (ACP) is intended to help patients and their spokespersons prepare for end-of-life decision making, yet little is known about what factors influence the extent to which spokespersons feel prepared for that role. To examine spokespersons' perceived preparedness for surrogate decision making after engaging in ACP. Mixed methods experimental design with qualitative thematic analysis and data transformation (creating categorical data from rich qualitative data) of interviews collected during a randomized controlled trial (2012-2017). Two tertiary care medical centers (Hershey, PA and Boston, MA). Of 285 dyads (patients with advanced illness and their spokespersons) enrolled in the trial, 200 spokesperson interviews were purposively sampled and 198 included in the analyses. Interviews with spokespersons (four weeks post-intervention) explored spokespersons' perceived preparedness for surrogate decision making, occurrence of ACP conversations, and spokespersons' intentions regarding future surrogate decisions. Data transformation was used to categorize participants' responses into three categories: , , or . Themes and categories were compared across arms. About 72.72% of spokespersons (144/198) reported being and 27.28% (54/198) reported being or with no differences in preparedness across study arms. Occurrence of post-intervention ACP conversations did not influence perceived preparedness; however, spokespersons who used an ACP decision aid reported more conversations. Four themes emerged to explain spokespersons' perceived preparedness: (1) perceptions about ACP; (2) level of comfort with uncertainty; (3) relational issues; and (4) personal characteristics. Regarding future intentions, it emerged that spokespersons believed their knowledge of patient wishes, as well as other personal, relational, situational, and emotional factors would influence their surrogate decisions. Factors extrinsic to specific ACP interventions influence how prepared spokespersons feel to act as spokespersons. Understanding these factors is important for understanding how to improve concordance between patients' stated end-of-life wishes and surrogate decisions. NCT02429479.
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http://dx.doi.org/10.1089/jpm.2020.0238DOI Listing
December 2020

Mesenchymal VEGFA induces aberrant differentiation in heterotopic ossification.

Bone Res 2019 Dec 10;7(1):36. Epub 2019 Dec 10.

Department of Surgery, University of Michigan, Ann Arbor, MI, 48109, USA.

Heterotopic ossification (HO) is a debilitating condition characterized by the pathologic formation of ectopic bone. HO occurs commonly following orthopedic surgeries, burns, and neurologic injuries. While surgical excision may provide palliation, the procedure is often burdened with significant intra-operative blood loss due to a more robust contribution of blood supply to the pathologic bone than to native bone. Based on these clinical observations, we set out to examine the role of vascular signaling in HO. Vascular endothelial growth factor A (VEGFA) has previously been shown to be a crucial pro-angiogenic and pro-osteogenic cue during normal bone development and homeostasis. Our findings, using a validated mouse model of HO, demonstrate that HO lesions are highly vascular, and that VEGFA is critical to ectopic bone formation, despite lacking a contribution of endothelial cells within the developing anlagen.
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http://dx.doi.org/10.1038/s41413-019-0075-6DOI Listing
December 2019

BMP Ligand Trap ALK3-Fc Attenuates Osteogenesis and Heterotopic Ossification in Blast-Related Lower Extremity Trauma.

Stem Cells Dev 2021 Jan 24;30(2):91-105. Epub 2020 Dec 24.

Regenerative Medicine Department, Naval Medical Research Center, Silver Spring, Maryland, USA.

Traumatic heterotopic ossification (tHO) commonly develops in wounded service members who sustain high-energy and blast-related traumatic amputations. Currently, no safe and effective preventive measures have been identified for this patient population. Bone morphogenetic protein (BMP) signaling blockade has previously been shown to reduce ectopic bone formation in genetic models of HO. In this study, we demonstrate the efficacy of small-molecule inhibition with LDN193189 (ALK2/ALK3 inhibition), LDN212854 (ALK2-biased inhibition), and BMP ligand trap ALK3-Fc at inhibiting early and late osteogenic differentiation of tissue-resident mesenchymal progenitor cells (MPCs) harvested from mice subjected to burn/tenotomy, a well-characterized trauma-induced model of HO. Using an established rat tHO model of blast-related extremity trauma and methicillin-resistant infection, a significant decrease in ectopic bone volume was observed by micro-computed tomography imaging following treatment with LDN193189, LDN212854, and ALK3-Fc. The efficacy of LDN193189 and LDN212854 in this model was associated with weight loss (17%-19%) within the first two postoperative weeks, and in the case of LDN193189, delayed wound healing and metastatic infection was observed, while ALK3-Fc was well tolerated. At day 14 following injury, RNA-Seq and quantitative reverse transcriptase-polymerase chain reaction analysis revealed that ALK3-Fc enhanced the expression of skeletal muscle structural genes and myogenic transcriptional factors while inhibiting the expression of inflammatory genes. Tissue-resident MPCs harvested from rats treated with ALK3-Fc exhibited reduced osteogenic differentiation, proliferation, and self-renewal capacity and diminished expression of genes associated with endochondral ossification and SMAD-dependent signaling pathways. Together, these results confirm the contribution of BMP signaling in osteogenic differentiation and ectopic bone formation and that a selective ligand-trap approach such as ALK3-Fc may be an effective and tolerable prophylactic strategy for tHO.
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http://dx.doi.org/10.1089/scd.2020.0162DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7826435PMC
January 2021

The role of neutrophil extracellular traps and TLR signaling in skeletal muscle ischemia reperfusion injury.

FASEB J 2020 12 22;34(12):15753-15770. Epub 2020 Oct 22.

Department of Surgery, University of Michigan, Ann Arbor, MI, USA.

Ischemia reperfusion (IR) injury results in devastating skeletal muscle fibrosis. Here, we recapitulate this injury with a mouse model of hindlimb IR injury which leads to skeletal muscle fibrosis. Injury resulted in extensive immune infiltration with robust neutrophil extracellular trap (NET) formation in the skeletal muscle, however, direct targeting of NETs via the peptidylarginine deiminase 4 (PAD4) mechanism was insufficient to reduce muscle fibrosis. Circulating levels of IL-10 and TNFα were significantly elevated post injury, indicating toll-like receptor (TLR) signaling may be involved in muscle injury. Administration of hydroxychloroquine (HCQ), a small molecule inhibitor of TLR7/8/9, following injury reduced NET formation, IL-10, and TNFα levels and ultimately mitigated muscle fibrosis and improved myofiber regeneration following IR injury. HCQ treatment decreased fibroadipogenic progenitor cell proliferation and partially inhibited ERK1/2 phosphorylation in the injured tissue, suggesting it may act through a combination of TLR7/8/9 and ERK signaling mechanisms. We demonstrate that treatment with FDA-approved HCQ leads to decreased muscle fibrosis and increased myofiber regeneration following IR injury, suggesting short-term HCQ treatment may be a viable treatment to prevent muscle fibrosis in ischemia reperfusion and traumatic extremity injury.
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http://dx.doi.org/10.1096/fj.202000994RRDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8054227PMC
December 2020

COGNITIVE MAPPING FOR ILOOKOUT FOR CHILD ABUSE: AN ONLINE TRAINING PROGRAM FOR EARLY CHILDHOOD PROFESSIONALS.

Online J Distance Educ Elearn 2020 Apr;8(2):80-89

Penn State University.

This article delineates the theory and framework for an innovative child abuse training program for mandated reporters called ''. is an online learning delivery system that utilizes mastery learning and self-determination theory in the Core Training program, along with spaced retrieval and retrieval practice in a follow-up micro-learning program that reinforces learning from the Core Training. A cognitive mapping model provides the structure for documenting and organizing the learning content in both the Core training and the follow-up micro-learning program. The article provides a conceptual framework for designing and implementing effective and efficient online learning programs.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7511090PMC
April 2020

Low Skepticism and Positive Attitudes About Advance Care Planning Among African Americans: a National, Mixed Methods Cohort Study.

J Gen Intern Med 2021 Mar 18;36(3):705-712. Epub 2020 Sep 18.

Department of Humanities, Penn State Milton S. Hershey Medical Center, Penn State College of Medicine, Hershey, PA, USA.

Background: African Americans have low engagement in advance care planning (ACP). This has been attributed to healthcare distrust and skepticism about ACP. A better understanding of these attitudes is needed to address health disparities related to end-of-life care.

Objective: To explore the ACP-related values and beliefs of diverse African American communities across the USA and then the perceived value of an inexpensive end-of-life conversational game.

Design: Prospective, convergent, mixed methods cohort study involving fifteen underserved, African American communities across the USA.

Participants: Of the 428 who attended events at purposively sampled sites, 90% consented to the research; 37% participated in one of 15 focus groups (n = 141).

Intervention: An end-of-life conversation game, played in groups of 4-6.

Main Measures: The validated, 7-item ACP values and beliefs questionnaire (scaled 7 = least skeptical, 49 = most skeptical) was administered pre-game. Post-game focus groups explored perceptions about ACP and the intervention.

Key Results: Participants had positive attitudes (low skepticism) about ACP with a median score of 12.00 (7.00, 20.00). Values and beliefs did not significantly differ by geographical region; however, rural areas were observed to be slightly more skeptical than urban areas (median score 14.00 vs. 11.00, p = 0.002). Themes from focus groups converged with survey data showing participants valued the ACP process and consider further engagement in ACP to be worthwhile. Subthemes emphasized the need for and value of ACP.

Conclusions: Skepticism about ACP may contribute to low rates of ACP engagement in underserved African American communities. The positive attitudes uncovered in our study either negate previous findings or suggest reduced skepticism.

Trial Registration: This study has been registered at clinicaltrials.gov ( NCT03456921 ).
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http://dx.doi.org/10.1007/s11606-020-06224-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947044PMC
March 2021

Mechanisms of bone development and repair.

Nat Rev Mol Cell Biol 2020 11 8;21(11):696-711. Epub 2020 Sep 8.

Division of Plastic and Reconstructive Surgery, Department of Surgery, Stanford University School of Medicine, Stanford, CA, USA.

Bone development occurs through a series of synchronous events that result in the formation of the body scaffold. The repair potential of bone and its surrounding microenvironment - including inflammatory, endothelial and Schwann cells - persists throughout adulthood, enabling restoration of tissue to its homeostatic functional state. The isolation of a single skeletal stem cell population through cell surface markers and the development of single-cell technologies are enabling precise elucidation of cellular activity and fate during bone repair by providing key insights into the mechanisms that maintain and regenerate bone during homeostasis and repair. Increased understanding of bone development, as well as normal and aberrant bone repair, has important therapeutic implications for the treatment of bone disease and ageing-related degeneration.
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http://dx.doi.org/10.1038/s41580-020-00279-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7699981PMC
November 2020

Articular cartilage regeneration by activated skeletal stem cells.

Nat Med 2020 10 17;26(10):1583-1592. Epub 2020 Aug 17.

Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine, Stanford, CA, USA.

Osteoarthritis (OA) is a degenerative disease resulting in irreversible, progressive destruction of articular cartilage. The etiology of OA is complex and involves a variety of factors, including genetic predisposition, acute injury and chronic inflammation. Here we investigate the ability of resident skeletal stem-cell (SSC) populations to regenerate cartilage in relation to age, a possible contributor to the development of osteoarthritis. We demonstrate that aging is associated with progressive loss of SSCs and diminished chondrogenesis in the joints of both mice and humans. However, a local expansion of SSCs could still be triggered in the chondral surface of adult limb joints in mice by stimulating a regenerative response using microfracture (MF) surgery. Although MF-activated SSCs tended to form fibrous tissues, localized co-delivery of BMP2 and soluble VEGFR1 (sVEGFR1), a VEGF receptor antagonist, in a hydrogel skewed differentiation of MF-activated SSCs toward articular cartilage. These data indicate that following MF, a resident stem-cell population can be induced to generate cartilage for treatment of localized chondral disease in OA.
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http://dx.doi.org/10.1038/s41591-020-1013-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7704061PMC
October 2020

Immobilization after injury alters extracellular matrix and stem cell fate.

J Clin Invest 2020 10;130(10):5444-5460

Section of Plastic Surgery, Department of Surgery.

Cells sense the extracellular environment and mechanical stimuli and translate these signals into intracellular responses through mechanotransduction, which alters cell maintenance, proliferation, and differentiation. Here we use a mouse model of trauma-induced heterotopic ossification (HO) to examine how cell-extrinsic forces impact mesenchymal progenitor cell (MPC) fate. After injury, single-cell (sc) RNA sequencing of the injury site reveals an early increase in MPC genes associated with pathways of cell adhesion and ECM-receptor interactions, and MPC trajectories to cartilage and bone. Immunostaining uncovers active mechanotransduction after injury with increased focal adhesion kinase signaling and nuclear translocation of transcriptional coactivator TAZ, inhibition of which mitigates HO. Similarly, joint immobilization decreases mechanotransductive signaling, and completely inhibits HO. Joint immobilization decreases collagen alignment and increases adipogenesis. Further, scRNA sequencing of the HO site after injury with or without immobilization identifies gene signatures in mobile MPCs correlating with osteogenesis, and signatures from immobile MPCs with adipogenesis. scATAC-seq in these same MPCs confirm that in mobile MPCs, chromatin regions around osteogenic genes are open, whereas in immobile MPCs, regions around adipogenic genes are open. Together these data suggest that joint immobilization after injury results in decreased ECM alignment, altered MPC mechanotransduction, and changes in genomic architecture favoring adipogenesis over osteogenesis, resulting in decreased formation of HO.
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http://dx.doi.org/10.1172/JCI136142DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7524473PMC
October 2020

Surrogate Decision Maker Stress in Advance Care Planning Conversations: A Mixed-Methods Analysis From a Randomized Controlled Trial.

J Pain Symptom Manage 2020 12 6;60(6):1117-1126. Epub 2020 Jul 6.

Department of Humanities, Penn State College of Medicine, Penn State Milton S. Hershey Medical Center, Hershey, Pennsylvania, USA; Department of Medicine, Penn State College of Medicine, Penn State Milton S. Hershey Medical Center, Hershey, Pennsylvania, USA; Public Health Sciences at Penn State College of Medicine, Penn State Milton S. Hershey Medical Center, Hershey, Pennsylvania, USA.

Context: Spokespersons serving as surrogate decision makers for their loved ones report high levels of stress. Despite known benefits, advance care planning (ACP) conversations often do not occur. More information is needed to understand spokesperson stress during ACP.

Objectives: To explore if and how spokespersons perceive stress related to ACP conversations; compare factors related to stress; and assess whether ACP intervention impacted stress.

Methods: Secondary and mixed-methods analysis with data transformation of semistructured interviews occurring during a 2 × 2 factorial (four armed) randomized controlled trial that compared standard online ACP to a comprehensive online ACP decision aid. Tools were completed by patients with advanced illness (n = 285) alone or with their spokesperson (n = 285). About 200 spokesperson interviews were purposively sampled from each of the four arms (50 per arm).

Results: ACP conversations were reported as stressful by 54.41% (74 of 136) and nonstressful by 45.59% (62 of 136). Five themes impacting spokesperson stress were the nature of the relationship with their loved one; self-described personality and belief systems; knowledge and experience with illness and ACP conversations; attitude toward ACP conversations; and social support in caregiving and decision making. No significant differences in stress were associated with arm assignment.

Conclusion: Identifying what factors impact spokesperson stress in ACP conversations can be used to help design ACP interventions to more appropriately address the needs and concerns of spokespersons.
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http://dx.doi.org/10.1016/j.jpainsymman.2020.07.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8109394PMC
December 2020

Small molecule inhibition of non-canonical (TAK1-mediated) BMP signaling results in reduced chondrogenic ossification and heterotopic ossification in a rat model of blast-associated combat-related lower limb trauma.

Bone 2020 10 2;139:115517. Epub 2020 Jul 2.

Regenerative Medicine Department, Naval Medical Research Center, Silver Spring, MD, United States of America; Department of Surgery, Uniformed Services University of the Health Sciences, Bethesda, MD, United States of America. Electronic address:

Heterotopic ossification (HO) is defined as ectopic bone formation around joints and in soft tissues following trauma, particularly blast-related extremity injuries, thermal injuries, central nerve injuries, or orthopaedic surgeries, leading to increased pain and diminished quality of life. Current treatment options include pharmacotherapy with non-steroidal anti-inflammatory drugs, radiotherapy, and surgical excision, but these treatments have limited efficacy and have associated complication profiles. In contrast, small molecule inhibitors have been shown to have higher specificity and less systemic cytotoxicity. Previous studies have shown that bone morphogenetic protein (BMP) signaling and downstream non-canonical (SMAD-independent) BMP signaling mediated induction of TGF-β activated kinase-1 (TAK1) contributes to HO. In the current study, small molecule inhibition of TAK1, NG-25, was evaluated for its efficacy in limiting ectopic bone formation following a rat blast-associated lower limb trauma and a murine burn tenotomy injury model. A significant decrease in total HO volume in the rat blast injury model was observed by microCT imaging with no systemic complications following NG-25 therapy. Furthermore, tissue-resident mesenchymal progenitor cells (MPCs) harvested from rats treated with NG-25 demonstrated decreased proliferation, limited osteogenic differentiation capacity, and reduced gene expression of Tac1, Col10a1, Ibsp, Smad3, and Sox2 (P < 0.05). Single cell RNA-sequencing of murine cells harvested from the injury site in a burn tenotomy injury model showed increased expression of these genes in MPCs during stages of chondrogenic differentiation. Additional in vitro cell cultures of murine tissue-resident MPCs and osteochondrogenic progenitors (OCPs) treated with NG-25 demonstrated reduced chondrogenic differentiation by 10.2-fold (P < 0.001) and 133.3-fold (P < 0.001), respectively, as well as associated reduction in chondrogenic gene expression. Induction of HO in Tak1 knockout mice demonstrated a 7.1-fold (P < 0.001) and 2.7-fold reduction (P < 0.001) in chondrogenic differentiation of murine MPCs and OCPs, respectively, with reduced chondrogenic gene expression. Together, our in vivo models and in vitro cell culture studies demonstrate the importance of TAK1 signaling in chondrogenic differentiation and HO formation and suggest that small molecule inhibition of TAK1 is a promising therapy to limit the formation and progression of HO.
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http://dx.doi.org/10.1016/j.bone.2020.115517DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7945876PMC
October 2020

Activin A does not drive post-traumatic heterotopic ossification.

Bone 2020 09 15;138:115473. Epub 2020 Jun 15.

Department of Surgery, University of Michigan, Ann Arbor, MI, United States of America; Division of Plastic Surgery, Department of Surgery, University of Michigan Health System, 1500 E Medical Center Drive, SPC 5340, Ann Arbor, MI 48109-5340, United States of America. Electronic address:

Heterotopic ossification (HO), the formation of ectopic bone in soft tissues, has been extensively studied in its two primary forms: post-traumatic HO (tHO) typically found in patients who have experienced musculoskeletal or neurogenic injury and in fibrodysplasia ossificans progressiva (FOP), where it is genetically driven. Given that in both diseases HO arises via endochondral ossification, the molecular mechanisms behind both diseases have been postulated to be manifestations of similar pathways including those activated by BMP/TGFβ superfamily ligands. A significant step towards understanding the molecular mechanism by which HO arises in FOP was the discovery that FOP causing ACVR1 variants trigger HO in response to activin A, a ligand that does not activate signaling from wild type ACVR1, and that is not inherently osteogenic in wild type settings. The physiological significance of this finding was demonstrated by showing that activin A neutralizing antibodies stop HO in two different genetically accurate mouse models of FOP. In order to explore the role of activin A in tHO, we performed single cell RNA sequencing and compared the expression of activin A as well as other BMP pathway genes in tHO and FOP HO. We show that activin A is expressed in response to injury in both settings, but by different types of cells. Given that wild type ACVR1 does not transduce signal when engaged by activin A, we hypothesized that inhibition of activin A will not block tHO. Nonetheless, as activin A was expressed in tHO lesions, we tested its inhibition and compared it with inhibition of BMPs. We show here that anti-activin A does not block tHO, whereas agents such as antibodies that neutralize ACVR1 or ALK3-Fc (which blocks osteogenic BMPs) are beneficial, though not completely curative. These results demonstrate that inhibition of activin A should not be considered as a therapeutic strategy for ameliorating tHO.
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http://dx.doi.org/10.1016/j.bone.2020.115473DOI Listing
September 2020

Perivascular Fibro-Adipogenic Progenitor Tracing during Post-Traumatic Osteoarthritis.

Am J Pathol 2020 09 10;190(9):1909-1920. Epub 2020 Jun 10.

Department of Pathology, Johns Hopkins University, Baltimore, Maryland; Department of Orthopaedic Surgery and the Orthopaedic Hospital Research Center, UCLA and Orthopaedic Hospital, Los Angeles, California. Electronic address:

Perivascular mural cells surround capillaries and microvessels and have diverse regenerative or fibrotic functions after tissue injury. Subsynovial fibrosis is a well-known pathologic feature of osteoarthritis, yet transgenic animals for use in visualizing perivascular cell contribution to fibrosis during arthritic changes have not been developed. Here, inducible Pdgfra-CreER reporter mice were subjected to joint-destabilization surgery to induce arthritic changes, and cell lineage was traced over an 8-week period with a focus on the joint-associated fat pad. Results showed that, at baseline, inducible Pdgfra reporter activity highlighted adventitial and, to a lesser extent, pericytic cells within the infrapatellar fat pad. Joint-destabilization surgery was associated with marked fibrosis of the infrapatellar fat pad, accompanied by an expansion of perivascular Pdgfra-expressing cellular descendants, many of which adopted α-smooth muscle actin expression. Gene expression analysis of microdissected infrapatellar fat pad confirmed enrichment in membrane-bound green fluorescent protein/Pdgfra-expressing cells, along with a gene signature that corresponded with injury-associated fibro-adipogenic progenitors. Our results highlight dynamic changes in joint-associated perivascular fibro-adipogenic progenitors during osteoarthritis.
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http://dx.doi.org/10.1016/j.ajpath.2020.05.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456743PMC
September 2020

Endogenous CCN family member WISP1 inhibits trauma-induced heterotopic ossification.

JCI Insight 2020 07 9;5(13). Epub 2020 Jul 9.

Department of Pathology, Johns Hopkins University, Baltimore, Maryland, USA.

Heterotopic ossification (HO) is defined as abnormal differentiation of local stromal cells of mesenchymal origin, resulting in pathologic cartilage and bone matrix deposition. Cyr61, CTGF, Nov (CCN) family members are matricellular proteins that have diverse regulatory functions on cell proliferation and differentiation, including the regulation of chondrogenesis. However, little is known regarding CCN family member expression or function in HO. Here, a combination of bulk and single-cell RNA sequencing defined the dynamic temporospatial pattern of CCN family member induction within a mouse model of trauma-induced HO. Among CCN family proteins, Wisp1 (also known as Ccn4) was most upregulated during the evolution of HO, and Wisp1 expression corresponded with chondrogenic gene profile. Immunohistochemistry confirmed WISP1 expression across traumatic and genetic HO mouse models as well as in human HO samples. Transgenic Wisp1LacZ/LacZ knockin animals showed an increase in endochondral ossification in HO after trauma. Finally, the transcriptome of Wisp1-null tenocytes revealed enrichment in signaling pathways, such as the STAT3 and PCP signaling pathways, that may explain increased HO in the context of Wisp1 deficiency. In sum, CCN family members, and in particular Wisp1, are spatiotemporally associated with and negatively regulate trauma-induced HO formation.
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http://dx.doi.org/10.1172/jci.insight.135432DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7406255PMC
July 2020

The Impact of Medical Scribes on Relative Value Units in a Pediatric Primary Care Practice.

Acad Pediatr 2021 04 20;21(3):542-547. Epub 2020 May 20.

Department of Pediatrics, Penn State College of Medicine (BH Levi, P Jhaveri, D Abdulahad, and BN Fogel), Hershey, Pa; Penn State College of Medicine (P Jhaveri), Hershey, Pa.

Objective: Our study assessed the impact of adding medical scribes to an academic pediatric primary practice by measuring the relationship between work relative value units (wRVUs) and use of the medical scribe.

Methods: This is a retrospective comparative study on the effect of medical scribes on average wRVUs per patient encounter. wRVUs were abstracted from procedure codes in the billing system.

Results: Six clinicians performed 2277 patient visits included in the study over 2 different time periods during 2017 and 2018. The first period was without the use of medical scribes and the second period included scribes. Average clinician wRVU production per visit increased by 7.68% (P < .001) with medical scribes over the previous period without them.

Conclusions: This study shows that scribes contribute to improving the wRVU per visit in a primary pediatric practice. This finding is consistent with other research showing that scribes help increase volume and improve wRVUs for specialists who perform complex procedures.
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http://dx.doi.org/10.1016/j.acap.2020.05.009DOI Listing
April 2021

Association of Participation in an End-of-Life Conversation Game With Advance Care Planning Behavior and Perspectives Among African American Individuals.

JAMA Netw Open 2020 05 1;3(5):e204315. Epub 2020 May 1.

Department of Medicine, Penn State Milton S. Hershey Medical Center, Penn State College of Medicine, Hershey, Pennsylvania.

Importance: Less than 25% of African American individuals have completed advance directives and are thus vulnerable to poor end-of-life care. Low-cost interventions are needed to increase engagement in advance care planning (ACP).

Objectives: To investigate whether an end-of-life conversation game motivates African American attendees to engage in ACP and to assess whether the game is well received and endorsed.

Exposures: Attendance at an end-of-life conversation game (Hello) played in groups of 4 to 6 participants for 60 minutes.

Design, Setting, And Participants: Prospective, mixed-methods cohort study conducted from 2018 to 2019 with a 3- to 11-month follow-up interview. Game events were held in 53 community venues across the US; 15 were purposively sampled for onsite research procedures. Of 428 attendees at purposively sampled sites, 386 (90%) consented to research procedures (6 attendees were removed from analysis for protocol deviation). Of 367 attendees who provided accurate contact information, 232 (63%) were contacted, and 220 were included in follow-up analyses.

Main Outcomes And Measures: The primary outcome was advance directive completion rates after the intervention. Secondary outcomes included rates of other ACP behaviors, ACP engagement, conversation satisfaction and realism, and participants' Net Promoter Score (a measure of endorsement). Follow-up telephone interviews explored the game experience and relevant ACP behaviors of attendees.

Results: Of 380 individuals who participated (mean [SD] age, 62.2 [13.8] years; 304 were female [80%], and 348 were [92%] African American), none withdrew because of an adverse event. After the intervention, 91 of 220 attendees (41%) completed a new advance directive; 176 of 220 attendees (80%) discussed end-of-life wishes with loved ones, and 214 of 219 attendees (98%) completed at least 1 ACP behavior. There was a moderate increase in the self-efficacy domain on the ACP Engagement Survey (mean [SD] change from before to after the game, 0.54 [0.98]; P < .001). The mean (SD) conversation satisfaction score was 6.21 (0.93) (range, 1-7, with 7 being highest satisfaction), and the overall Net Promoter Score was 57.89 (range, -100 to 100, with 100 being highest endorsement). Interviews revealed 5 themes about the game: (1) it was a useful forum for ACP; (2) it provided new information and perspective; (3) it was emotionally beneficial; (4) it increased appreciation for ACP; and (5) it empowered and motivated participants to perform ACP. Mixed-methods integration showed convergence across data sets.

Conclusions And Relevance: Among a nationwide sample of African American individuals, the end-of-life conversation game appeared to be well received and was associated with high rates of ACP behavior. This low-cost and scalable tool may help reduce health disparities associated with end-of-life care.
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http://dx.doi.org/10.1001/jamanetworkopen.2020.4315DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7210487PMC
May 2020

Tuning Macrophage Phenotype to Mitigate Skeletal Muscle Fibrosis.

J Immunol 2020 04 11;204(8):2203-2215. Epub 2020 Mar 11.

Department of Surgery, University of Michigan, Ann Arbor, MI 48109;

Myeloid cells are critical to the development of fibrosis following muscle injury; however, the mechanism of their role in fibrosis formation remains unclear. In this study, we demonstrate that myeloid cell-derived TGF-β1 signaling is increased in a profibrotic ischemia reperfusion and cardiotoxin muscle injury model. We found that myeloid-specific deletion of abrogates the fibrotic response in this injury model and reduces fibro/adipogenic progenitor cell proliferation while simultaneously enhancing muscle regeneration, which is abrogated by adaptive transfer of normal macrophages. Similarly, a murine TGFBRII-Fc ligand trap administered after injury significantly reduced muscle fibrosis and improved muscle regeneration. This study ultimately demonstrates that infiltrating myeloid cell TGF-β1 is responsible for the development of traumatic muscle fibrosis, and its blockade offers a promising therapeutic target for preventing muscle fibrosis after ischemic injury.
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http://dx.doi.org/10.4049/jimmunol.1900814DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8080967PMC
April 2020

Self-reported baseline phenotypes from the International Fibrodysplasia Ossificans Progressiva (FOP) Association Global Registry.

Bone 2020 05 13;134:115274. Epub 2020 Feb 13.

Departments of Orthopaedic Surgery and Medicine, The Center for Research in FOP & Related Disorders, The Perelman School of Medicine, The University of Pennsylvania, Philadelphia, PA, United States. Electronic address:

A global, patient-reported registry has been established to characterize the course of disease and track clinical outcomes in patients with fibrodysplasia ossificans progressiva (FOP), an ultra-rare genetic condition of progressive heterotopic ossification (HO) that results in ankylosis of joints and renders most affected individuals immobile by the second decade of life. Here, we present baseline phenotypes on 299 patients (median age 21 years; range 0.1 to 78 years) from 54 countries based on aggregate data from the International FOP Association (IFOPA) Global Registry (the "FOP Registry"). The mean current age of the patients is 23.7 years (range, 0.1 to 78 years). Baseline characteristics are presented for FOP diagnosis, HO, flare-ups and precedent events, system-based prevalent symptomatology, encounters with medical and dental care providers, Patient Reported Outcomes Measurement Information System (PROMIS) Global Health Scale scores, physical function, as well as the use of aids, assistive devices, and adaptations. Correlations of PROMIS Global Health scores with HO burden and physical function are calculated. Associations of joint mobility with PROMIS Global Health scores, physical function, and use of aids, assistive devices, and adaptations are summarized. Overall, the FOP Registry database contains a broad sample of the global FOP patient population, providing a useful tool for expanding knowledge of FOP, designing clinical trials and facilitating evidence-based decisions about the optimal monitoring and management of affected individuals.
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http://dx.doi.org/10.1016/j.bone.2020.115274DOI Listing
May 2020

Regulation of heterotopic ossification by monocytes in a mouse model of aberrant wound healing.

Nat Commun 2020 02 5;11(1):722. Epub 2020 Feb 5.

Section of Plastic Surgery, Department of Surgery, University of Michigan, Ann Arbor, MI, 48109, USA.

Heterotopic ossification (HO) is an aberrant regenerative process with ectopic bone induction in response to musculoskeletal trauma, in which mesenchymal stem cells (MSC) differentiate into osteochondrogenic cells instead of myocytes or tenocytes. Despite frequent cases of hospitalized musculoskeletal trauma, the inflammatory responses and cell population dynamics that regulate subsequent wound healing and tissue regeneration are still unclear. Here we examine, using a mouse model of trauma-induced HO, the local microenvironment of the initial post-injury inflammatory response. Single cell transcriptome analyses identify distinct monocyte/macrophage populations at the injury site, with their dynamic changes over time elucidated using trajectory analyses. Mechanistically, transforming growth factor beta-1 (TGFβ1)-producing monocytes/macrophages are associated with HO and aberrant chondrogenic progenitor cell differentiation, while CD47-activating peptides that reduce systemic macrophage TGFβ levels and help ameliorate HO. Our data thus implicate CD47 activation as a therapeutic approach for modulating monocyte/macrophage phenotypes, MSC differentiation and HO formation during wound healing.
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http://dx.doi.org/10.1038/s41467-019-14172-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7002453PMC
February 2020

Generalizing findings from a randomized controlled trial to a real-world study of the iLookOut, an online education program to improve early childhood care and education providers' knowledge and attitudes about reporting child maltreatment.

PLoS One 2020 8;15(1):e0227398. Epub 2020 Jan 8.

Departments of Humanities & Pediatrics, Penn State College of Medicine, Hershey, Pennsylvania, United States of America.

In recent years, real-world studies (RWS) are gaining increasing interests, because they can generate more realistic and generalizable results than randomized controlled clinical trials (RCT). In 2017, we published a RCT in 741 early childhood care and education providers (CCPs). It is the Phase I of our iLookOut for Child Abuse project (iLookOut), an online, interactive learning module about reporting suspected child maltreatment. That study demonstrated that in a RCT setting, the iLookOut is efficient at improving CCPs' knowledge of and attitudes towards child maltreatment reporting. However, the generalizability of that RCT's results in a RWS setting remains unknown. To address this question, we design and conduct this large RWS in 11,065 CCPs, which is the Phase II of the iLookOut. We hypothesize replication of the earlier RCT findings, i.e., the iLookOut can improve CCPs' knowledge of and attitudes toward child maltreatment reporting in a real world setting. In addition, this RWS also explores whether demographic factors affect CCPs' performance. Results of this RWS confirmed the generalizability of the previous RCT's results in a real world setting. It yielded similar effect sizes for knowledge and attitudes as were found in the earlier RCT. Cohen's d for knowledge improvement was 0.95 in that RCT, 0.96 in this RWS; Cohen's d for attitude improvement was 0.98 in that RCT, 0.80 in this RWS. Also, we found several significant differences in knowledge and attitude improvement with regard to age, race, education, and employment status. In conclusion, iLookOut improves knowledge and attitudes of CCPs about child maltreatment prevention and reporting in a real-world setting. The generalizability of the initial RCT findings to this RWS provides strong evidence that the iLookout will be effective in other real world settings. It can be a useful model for other interventions aimed at preventing child maltreatment. Clinical trial registration for the original RCT: NCT02225301 (ClinicalTrials.gov Identifier).
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0227398PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6948728PMC
May 2020

Mesenchymal VEGFA induces aberrant differentiation in heterotopic ossification.

Bone Res 2019 10;7:36. Epub 2019 Dec 10.

1Department of Surgery, University of Michigan, Ann Arbor, MI 48109 USA.

Heterotopic ossification (HO) is a debilitating condition characterized by the pathologic formation of ectopic bone. HO occurs commonly following orthopedic surgeries, burns, and neurologic injuries. While surgical excision may provide palliation, the procedure is often burdened with significant intra-operative blood loss due to a more robust contribution of blood supply to the pathologic bone than to native bone. Based on these clinical observations, we set out to examine the role of vascular signaling in HO. Vascular endothelial growth factor A (VEGFA) has previously been shown to be a crucial pro-angiogenic and pro-osteogenic cue during normal bone development and homeostasis. Our findings, using a validated mouse model of HO, demonstrate that HO lesions are highly vascular, and that VEGFA is critical to ectopic bone formation, despite lacking a contribution of endothelial cells within the developing anlagen.
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http://dx.doi.org/10.1038/s41413-019-0075-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6904752PMC
December 2019

Patients With Advanced Cancer Choose Less Aggressive Medical Treatment on Vignettes After Using a Computer-Based Decision Aid.

Am J Hosp Palliat Care 2020 Jul 13;37(7):537-541. Epub 2019 Dec 13.

Department of Humanities, Penn State College of Medicine, Hershey, PA, USA.

Background: Although patients often prefer less rather than more treatment at the end of life, in the absence of contrary instructions, the medical profession's de facto position is to treat aggressively. It is unknown whether a computer-based decision aid can affect treatment choices.

Methods: Secondary analysis of a single-center, single-blind randomized controlled trial of an advance care planning (ACP) intervention among 200 patients with stage IV cancer. Participants were randomized to intervention (, a values-neutral, educational, computer-based decision aid) or control (standard living will + brochure). After reading a hypothetical clinical vignette, participants were asked whether they would want 11 medical/surgical treatments in that situation (dialysis, cardiopulmonary resuscitation [CPR], ventilator, feeding tube, etc). The median number of treatments wanted by participants was compared between groups, and logistic regression was used to compare between-group likelihood of not wanting each specific treatment.

Results: The median number of treatments wanted was 1 in the intervention group versus 5 in the control ( < .001). For 6 of 11 treatments, the intervention group was significantly less likely than control to want aggressive treatment. Most notably, compared to control, intervention participants were less likely to want CPR (odds ratio [OR] = 0.31), short-term mechanical ventilation (OR = 0.34), short-term dialysis (OR = 0.38), surgery (OR = 0.37), and transfusion (OR = 0.21).

Conclusions: Individuals using an educational ACP decision aid were less likely to want aggressive medical treatment than those completing standard living wills. These findings have implications not only for how to respect patient's wishes but also potentially for reducing costs at the end of life.
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http://dx.doi.org/10.1177/1049909119892596DOI Listing
July 2020

Cellular Plasticity in Musculoskeletal Development, Regeneration, and Disease.

J Orthop Res 2020 04 25;38(4):708-718. Epub 2019 Nov 25.

Department of Orthopaedics, Icahn School of Medicine at Mount Sinai, New York, New York.

In this review, we highlight themes from a recent workshop focused on "Plasticity of Cell Fate in Musculoskeletal Tissues" held at the Orthopaedic Research Society's 2019 annual meeting. Experts in the field provided examples of mesenchymal cell plasticity during normal musculoskeletal development, regeneration, and disease. A thorough understanding of the biology underpinning mesenchymal cell plasticity may offer a roadmap for promoting regeneration while attenuating pathologic differentiation. © 2019 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 38:708-718, 2020.
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http://dx.doi.org/10.1002/jor.24523DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7213644PMC
April 2020

Disruption of Neutrophil Extracellular Traps (NETs) Links Mechanical Strain to Post-traumatic Inflammation.

Front Immunol 2019 24;10:2148. Epub 2019 Oct 24.

Department of Surgery, University of Michigan Medical School, Ann Arbor, MI, United States.

Inflammation after trauma is both critical to normal wound healing and may be highly detrimental when prolonged or unchecked with the potential to impair physiologic healing and promote pathology. Mechanical strain after trauma is associated with impaired wound healing and increased inflammation. The exact mechanisms behind this are not fully elucidated. Neutrophil extracellular traps (NETs), a component of the neutrophil response to trauma, are implicated in a range of pro-inflammatory conditions. In the current study, we evaluated their role in linking movement and inflammation. We found that a link exists between the disruption and amplification of NETs which harbors the potential to regulate the wound's response to mechanical strain, while leaving the initial inflammatory signal necessary for physiologic wound healing intact.
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http://dx.doi.org/10.3389/fimmu.2019.02148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6821718PMC
October 2020

Short-wave infrared light imaging measures tissue moisture and distinguishes superficial from deep burns.

Wound Repair Regen 2020 03 4;28(2):185-193. Epub 2019 Dec 4.

Department of Surgery, University of Michigan, Ann Arbor, Michigan.

Existing clinical approaches and tools to measure burn tissue destruction are limited resulting in misdiagnosis of injury depth in over 40% of cases. Thus, our objective in this study was to characterize the ability of short-wave infrared (SWIR) imaging to detect moisture levels as a surrogate for tissue viability with resolution to differentiate between burns of various depths. To accomplish our aim, we constructed an imaging system consisting of a broad-band Tungsten light source; 1,200-, 1,650-, 1,940-, and 2,250-nm wavelength filters; and a specialized SWIR camera. We initially used agar slabs to provide a baseline spectrum for SWIR light imaging and demonstrated the differential absorbance at the multiple wavelengths, with 1,940 nm being the highest absorbed wavelength. These spectral bands were then demonstrated to detect levels of moisture in inorganic and in vivo mice models. The multiwavelength SWIR imaging approach was used to diagnose depth of burns using an in vivo porcine burn model. Healthy and injured skin regions were imaged 72 hours after short (20 seconds) and long (60 seconds) burn application, and biopsies were extracted from those regions for histologic analysis. Burn depth analysis based on collagen coagulation histology confirmed the formation of superficial and deep burns. SWIR multispectral reflectance imaging showed enhanced intensity levels in long burned regions, which correlated with histology and distinguished between superficial and deep burns. This SWIR imaging method represents a novel, real-time method to objectively distinguishing superficial from deep burns.
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http://dx.doi.org/10.1111/wrr.12779DOI Listing
March 2020