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Structure and Distribution of an Unrecognized Interstitium in Human Tissues Received: 18 May 2017 Petros C www.nature.com/scientificreports OPEN Structure and Distribution of an Unrecognized Interstitium in Human Tissues Received: 18 May 2017 Petros C. Benias1,2, Rebecca G. Wells3,4, Bridget Sackey-Aboagye3, Heather Klavan1, Jason Accepted: 6 March 2018 Reidy5, Darren Buonocore5, Markus Miranda1, Susan Kornacki6, Michael Wayne7, David L. Published: xx xx xxxx Carr-Locke1,8 & Neil D. Theise1,5,6 Confocal laser endomicroscopy (pCLE) provides real-time histologic imaging of human tissues at a depth of 60–70 μm during endoscopy. pCLE of the extrahepatic bile duct after fuorescein injection demonstrated a reticular pattern within fuorescein-flled sinuses that had no known anatomical correlate. Freezing biopsy tissue before fxation preserved the anatomy of this structure, demonstrating that it is part of the submucosa and a previously unappreciated fuid-flled interstitial space, draining to lymph nodes and supported by a complex network of thick collagen bundles. These bundles are intermittently lined on one side by fbroblast-like cells that stain with endothelial markers and vimentin, although there is a highly unusual and extensive unlined interface between the matrix proteins of the bundles and the surrounding fuid. We observed similar structures in numerous tissues that are subject to intermittent or rhythmic compression, including the submucosae of the entire gastrointestinal tract and urinary bladder, the dermis, the peri-bronchial and peri-arterial soft tissues, and fascia. These anatomic structures may be important in cancer metastasis, edema, fbrosis, and mechanical functioning of many or all tissues and organs. In sum, we describe the anatomy and histology of a previously unrecognized, though widespread, macroscopic, fuid-flled space within and between tissues, a novel expansion and specifcation of the concept of the human interstitium. Te interstitial space is the primary source of lymph and is a major fuid compartment in the body. While the anatomy and composition of the interstitial space between cells is increasingly understood, the existence, loca- tion, and structure of larger inter- and intra-tissue spaces is described only vaguely in the literature. Tis is par- ticularly important in reference to “third spacing” (interstitial fuid build-up) and when considering overall interstitial fuid fow and volume, which have not been well studied1. Advances in in vivo microscopy ofer the potential to identify new, functionally-relevant anatomical struc- tures in humans. Lymphatic vessels in the brain, for example, were recently identifed for the frst time using in vivo multiphoton microscopy imaging through a thinned skull preparation2. Probe-based Confocal Laser Endomicroscopy (pCLE) is an in vivo imaging technology that provides real-time histologic assessment of tissue structures during endoscopy, generally afer intravenous injection of fuorescein. We and others have observed that, in the extrahepatic bile ducts and pancreatic ducts, pCLE at the fxed focal length of 60–70 μm shows a submucosal “reticular pattern” (Fig. 1A,B) consisting of 20 μm wide dark branching bands surrounding large, 1Department of Medicine, Division of Digestive Diseases, Mount Sinai Beth Israel Medical Center, Icahn School of Medicine at Mount Sinai, New York, New York, 10003, USA. 2Department of Medicine, Division of Gastroenterology, Zucker School of Medicine at Hofstra/Northwell, 500 Hofstra Blvd, Hempstead, NY 11549, USA. 3Department of Medicine, Division of Gastroenterology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA. 4Department of Bioengineering and Center for Engineering MechanoBiology, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA. 5Department of Pathology, Mount Sinai Beth Israel Medical Center, Icahn School of Medicine at Mount Sinai, New York, New York, 10003, USA. 6Department of Pathology, New York University School of Medicine, New York, New York, 10016, USA. 7Department of Surgery, Mount Sinai Beth Israel Medical Center, Icahn School of Medicine at Mount Sinai, New York, New York, 10003, USA. 8The Center for Advanced Digestive Care, Weill Cornell Medicine, New York Presbyterian Hospital, 1305 York Avenue, 4th Floor, New York, New York, 10021, USA. Petros C. Benias and Rebecca G. Wells contributed equally to this work. David L. Carr-Locke and Neil D. Theise jointly supervised this work. Correspondence and requests for materials should be addressed to N.D.T. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:4947 | DOI:10.1038/s41598-018-23062-6 1 www.nature.com/scientificreports/ Figure 1. Identifcation of bile duct reticular pattern and demonstration of submucosal space. (A,B) pCLE of bile duct afer fuorescein injection shows a reticular pattern at a depth of 60–70 μm. Scale bar, 20 μm. (C–E) Bile duct tissue removed at the time of Whipple surgery was frozen and ex vivo pCLE performed, demonstrating persistence of the reticular pattern. Scale bar, 20 μm. (F) Unstained frozen tissue of submucosa of a bile duct imaged by fuorescent microscopy, showing the reticular pattern in this layer of bile duct wall. Te “bright” spaces are now dark (fuoresceinated fuid drained in processing and the tissue structures remained stained with residual fuorescein). (G) Masson trichrome of fresh-frozen bile duct shows that the dark bands are collagen bundles (blue) (lef). Te upper right shows Masson trichrome of a normally processed/fxed bile duct from the same patient, with collapse of spaces and apparent adherence of collagen bundles to each other. Lower right shows the fxed specimen stained with H&E; the thin spaces between collagen layers (arrows) refect normally fuid-flled spaces that are almost completely collapsed. (H) Frozen (top) and fxed (bottom) bile ducts immunostained with antibodies against CD34 (lef, brown) and D2-40 (right, brown) show cells lining the collagen bundles; note that bundles ofen seem to have a lining cell on one side, but not the other (20×, DAB, hematoxylin). (I) Schematic of the fuid-flled space supported by a network of collagen bundles lined on one side with cells. Illustration by Jill Gregory. Printed with permission from Mount Sinai Health System, licenced under CC-BY-ND. (https://creativecommons.org/licenses/by-nd/4.0/legalcode). fuorescein-flled polygonal spaces3. Tese have no obvious correlate to known structures. Although endoscopists have suggested that this network represents capillaries or lymphangioles3, neither structure can explain the retic- ular pattern of dark bands and bright, fuid-flled spaces. We hypothesized that this pattern refects an extension of the intercellular interstitial space. We carried out an in-depth study using pCLE and histology of the human extrahepatic bile duct in order to identify the microan- atomic correlates of the reticular pattern. We report here the existence of a novel interstitial (i.e. pre-lymphatic) space defned by a complex lattice of thick collagen bundles. We observed similar structures when we extended our study to include the dermis, peri-arterial stroma, submucosa of the viscera (gastrointestinal tract, urinary bladder), bronchial tree of the lungs, and fascial planes of the musculoskeletal system and adipose tissue, and as a result propose a large-scale revision of the macro- and microanatomy of the human interstitium. Results Samples were obtained from surgical specimens of bile ducts resected during twelve pancreatico-biliary surgeries. Several minutes prior to vascular ligation and resection of the surgical specimen, patients were infused intravas- cularly with fuorescein with direct in situ visualization by pCLE of the reticular pattern (Fig. 1A,B). Te site was resected and then immediately scanned again with pCLE ex vivo, confrming that the reticular pattern and the fu- orescein were still intact afer resection (data not shown). Te specimens were then embedded in frozen section medium, rapidly frozen using an aerosol-based freezing spray, and re-imaged (Fig. 1C,D,E). Serial frozen sections were cut perpendicular to the viewing angle of the pCLE exactly en face to the lumen surface, marking sections every 5 μm until a depth of 60–70 μm was reached. We also performed serial sections of tissue in a cross-sectional plane. Tese sections were visualized under routine fuorescence microscopy (Fig. 1F), showing that the reticular pattern correlated with thick, fuorescein-stained bundles (seen on pCLE as black bands). Te absence of fuores- cence between these bundles in the fnal slides is due to the process of frozen section slide preparation (air drying, fxation and washing) causing the fuid to drain from the fnal slide. Parallel frozen sections were stained with Masson’s trichrome stain, confrming the presence of collagenous bands separating open, formerly fuid-flled spaces (Fig. 1G, lef). Tese structures co-localized with the com- pacted biliary submucosa normally seen in biopsy and resection specimens (Fig. 1G, right, from the same patient as sample on lef). Tis suggests that the previously described dense structure of the submucosa represents an artifact due to loss of fuid during tissue excision and fxation, causing normally-separated collagen bundles to collapse and adhere to each other. We observed that the reticular pattern appeared within 30 seconds of intravas- cular infusion of fuorescein, approximately the same time point at which lymph nodes are visualized, but later SCIENTIFIC REPORTS | (2018) 8:4947 | DOI:10.1038/s41598-018-23062-6
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