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Pathogenesis and Clinical Management of Mesenteric Fibrosis in Small Intestinal Neuroendocine Neoplasms: a Systematic Review

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Pathogenesis and Clinical Management of Mesenteric Fibrosis in Small Intestinal Neuroendocine Neoplasms: a Systematic Review Journal of Clinical Medicine Review Pathogenesis and Clinical Management of Mesenteric Fibrosis in Small Intestinal Neuroendocine Neoplasms: A Systematic Review 1, , 2, 3 2 Anna Koumarianou * y , Krystallenia I. Alexandraki y , Göran Wallin , Gregory Kaltsas and Kosmas Daskalakis 2,3 1 Hematology Oncology Unit, Fourth Department of Internal Medicine, Attikon University General Hospital, National and Kapodistrian University of Athens, 12462 Athens, Greece 2 1st Department of Propaedeutic Internal Medicine, Endocrine Unit, National and Kapodistrian, University of Athens, 11527 Athens, Greece; [email protected] (K.I.A.); [email protected] (G.K.); [email protected] (K.D.) 3 Department of Surgery, Faculty of Medicine and Health, Örebro University, 701 85 Örebro, Sweden; [email protected] * Correspondence: [email protected]; Tel.: +30-21-0583-1687 Denotes equal contribution. y Received: 12 May 2020; Accepted: 4 June 2020; Published: 8 June 2020 Abstract: Mesenteric fibrosis (MF) constitutes an underrecognized sequela in patients with small intestinal neuroendocrine neoplasms (SI-NENs), often complicating the disease clinical course. The aim of the present systematic review, carried out by Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology, is to provide an update in evolving aspects of MF pathogenesis and its clinical management in SI-NENs. Complex and dynamic interactions are present in the microenvironment of tumor deposits in the mesentery. Serotonin, as well as the signaling pathways of certain growth factors play a pivotal, yet not fully elucidated role in the pathogenesis of MF. Clinically, MF often results in significant morbidity by causing either acute complications, such as intestinal obstruction and/or acute ischemia or more chronic conditions involving abdominal pain, venous stasis, malabsorption and malnutrition. Surgical resection in patients with locoregional disease only or symptomatic distant stage disease, as well as palliative minimally invasive interventions in advanced inoperable cases seem clinically meaningful, whereas currently available systemic and/or targeted treatments do not unequivocally affect the development of MF in SI-NENs. Increased awareness and improved understanding of the molecular pathogenesis of MF in SI-NENs may provide better diagnostic and predictive tools for its timely recognition and intervention and also facilitates the development of agents targeting MF. Keywords: neuroendocrine tumors; small intestine; mesenteric fibrosis; serotonin; TGF; FGF; PDGF; VEGF; CTGF 1. Introduction Small intestinal neuroendocrine neoplasms (SI-NENs) comprise a rare tumor entity with rising incidence, but overall favorable survival outcomes despite frequent presentation at distant stage disease [1]. They originate in enterochromafin (EC) cells, usually in the terminal ileum and less commonly in the jejunum. The primary tumor is typically submucosal and < 1cm in size, whereas in up to 50% of patients multifocal tumors can be found arising independently in the small intestine [2,3]. Mesenteric lymph node (LN) metastases are commonly present at diagnosis and tend to grow conspicuously large and often induce mesenteric fibrosis (MF) in the surrounding tissue of the mesentery. J. Clin. Med. 2020, 9, 1777; doi:10.3390/jcm9061777 www.mdpi.com/journal/jcm J. Clin. Med. 2019, 8, x FOR PEER REVIEW 2 of 21 conspicuously large and often induce mesenteric fibrosis (MF) in the surrounding tissue of the mesentery. The release of various amines, peptides and growth factors (GFs) may induce hormonal symptoms that constitute the carcinoid syndrome (CS), but also fibrosis in cellular systems leading to MF and carcinoid heart disease (CHD) [4,5]. In addition, neuroendocrine neoplasm (NEN) cells overexpressJ. Clin. a Med. plethora2020, 9, 1777 of proangiogenic molecules that promote both recruitment and2 of 21proliferation of endothelial cell precursors becoming highly vascularized neoplasms [6]. LocoregionalThe release LN ofmetastases various amines, together peptides with and the growth acco factorsmpanying (GFs) may MF induce may occur hormonal in up symptoms to 50% of SI-NENs with encasementthat constitute of the the superior carcinoid mese syndromenteric (CS), vessels but also at different fibrosis in levels cellular in systems the mesentery leading to MF[7,8]. and Locoregional carcinoid heart disease (CHD) [4,5]. In addition, neuroendocrine neoplasm (NEN) cells overexpress a resectiveplethora surgery of proangiogenicwhen feasible molecules constitutes that promote the main both recruitmentstay of treatment and proliferation in patients of endothelial with MF-related symptoms.cell precursorsAlthough becoming advances highly in systemic vascularized and neoplasms liver-targeted [6]. treatment of SI-NENs have been made, alleviating hormonalLocoregional symptoms LN metastases and together prolonging with the progression-free accompanying MF may(PFS) occur and in upoverall to 50% survival of (OS), effectiveSI-NENs treatment with options encasement targeting of the superior MF are mesenteric not full vesselsy elucidated. at different As levels improved in the mesentery insight [ 7in,8 ].the complex Locoregional resective surgery when feasible constitutes the mainstay of treatment in patients with pathogenesisMF-related of MF symptoms. is key to Although the development advances in of systemic new therapies, and liver-targeted we have treatment reviewed of SI-NENs evolving aspects of tumorhave microenvironment been made, alleviating (TME), hormonal mediators symptoms and prolonging signaling progression-free pathways involved (PFS) and overallin the molecular pathogenesissurvival of (OS), MF einffective SI-NENs, treatment in order options to targeting refine MF the are management not fully elucidated. of patients As improved suffering insight from fibrotic complications.in the complex pathogenesis of MF is key to the development of new therapies, we have reviewed evolving aspects of tumor microenvironment (TME), mediators and signaling pathways involved in the molecular pathogenesis of MF in SI-NENs, in order to refine the management of patients suffering 2. Experimentalfrom fibrotic Section complications. We 2.performed Experimental a Sectionsystematic review of the literature available on PubMed, Cochrane Library, Embase, WebWe of performed Science a and systematic SCOPUS review databases of the literature about available MF in on SI-NENs PubMed, until Cochrane March Library, 15th, 2020, as specifiedEmbase, in the Web“Search of Science Strategy and SCOPUS Supplement” databases (Table about MFS1). in Articles SI-NENs were until Marchindependently 15th, 2020, asevaluated by two of thespecified authors in the (K.D. “Search and Strategy K.I.A.) Supplement” for the releva (Tablence S1). to Articles the planned were independently scope of evaluatedthe review. by Reference lists of keytwo publications of the authors (K.D.were and also K.I.A.) reviewed for the relevancefor eligibility. to the planned We followed scope of Preferred the review. ReferenceReporting Items for lists of key publications were also reviewed for eligibility. We followed Preferred Reporting Items for SystematicSystematic Reviews Reviews and andMeta-Analyses Meta-Analyses (PRISMA) guidelines guidelines for reporting for reporting [9]. The literature[9]. Thesearch literature search and the selectionand the selection of included of included studies studies are are presentedpresented in thein the PRISMA PRISMA flow diagram flow diagram (Figure1). (Figure 1). Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow Figure 1.diagram Preferred of study Reporting selection. Abbreviations: Items for Systematic ENETS; European Reviews Neuroendocrine and Meta-Analyses Tumor Society; NENs: (PRISMA) flow diagramNeuroendocrine of study selection. Neoplasms. Abbreviations: ENETS; European Neuroendocrine Tumor Society; NENs: Neuroendocrine Neoplasms. 3. Results 3.1. Pathogenesis of Mesenteric Fibrosis (MF) In SI-NENs, MF represents an abnormal repair process, mimicking the mechanism operating in certain types of connective tissue disorder, associated with serious complications during the course J. Clin. Med. 2020, 9, 1777 3 of 21 3. Results 3.1. Pathogenesis of Mesenteric Fibrosis (MF) In SI-NENs, MF represents an abnormal repair process, mimicking the mechanism operating in certain types of connective tissue disorder, associated with serious complications during the course of the disease [10,11]. Serotonin and vasoactive substances were the first effectors to be implicated in the pathogenesis of CS and into its more severe complications, the MF or CHD, representing the fibrotic-related sequelae of CS. There is currently evidence that CHD pathophysiology is mostly based on circulating effectors, specifically on high serotonin levels as depicted by the high urine level of 5-hydroxyindoleacetic acid (5-HIAA), whereas MF seems to be caused by a complex network of autocrine and paracrine mediators produced by neoplastic cells and TME elements [11]. TME represents an important functional unit comprising a cluster of endothelial and inflammatory cells and mesenchymal stroma elements with fibroblasts. This network of cells is interconnected and interacting, leading to tumor growth and development of fibrosis, possibly through epigenetic changes of tumor cells [6,12,13]. TME has been recently depicted as a dynamic milieu where an injury with fragmentation of extracellular matrix elements results in chemo-attractant
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