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The Clinical Link Between Human Intestinal Microbiota and Systemic Cancer Therapy

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The Clinical Link Between Human Intestinal Microbiota and Systemic Cancer Therapy International Journal of Molecular Sciences Review The Clinical Link between Human Intestinal Microbiota and Systemic Cancer Therapy 1,2, , 1,2, 3,4 2,4 Romy Aarnoutse * y, Janine Ziemons y, John Penders , Sander S. Rensen , Judith de Vos-Geelen 1,5 and Marjolein L. Smidt 1,2 1 GROW-School for Oncology and Developmental Biology, Maastricht University Medical Center+, 6229 ER Maastricht, The Netherlands 2 Department of Surgery, Maastricht University Medical Center+, 6202 AZ Maastricht, The Netherlands 3 Department of Medical Microbiology, Maastricht University Medical Center+, 6202 AZ Maastricht, The Netherlands 4 NUTRIM - School of Nutrition and Translational Research in Metabolism, Maastricht University Medical Center+, 6229 ER Maastricht, The Netherlands 5 Department of Internal Medicine, Division of Medical Oncology, Maastricht University Medical Center+, 6202 AZ Maastricht, The Netherlands * Correspondence: [email protected] or [email protected]; Tel.: +31-(0)6-82019105 These authors contributed equally to this work. y Received: 31 July 2019; Accepted: 22 August 2019; Published: 25 August 2019 Abstract: Clinical interest in the human intestinal microbiota has increased considerably. However, an overview of clinical studies investigating the link between the human intestinal microbiota and systemic cancer therapy is lacking. This systematic review summarizes all clinical studies describing the association between baseline intestinal microbiota and systemic cancer therapy outcome as well as therapy-related changes in intestinal microbiota composition. A systematic literature search was performed and provided 23 articles. There were strong indications for a close association between the intestinal microbiota and outcome of immunotherapy. Furthermore, the development of chemotherapy-induced infectious complications seemed to be associated with the baseline microbiota profile. Both chemotherapy and immunotherapy induced drastic changes in gut microbiota composition with possible consequences for treatment efficacy. Evidence in the field of hormonal therapy was very limited. Large heterogeneity concerning study design, study population, and methods used for analysis limited comparability and generalization of results. For the future, longitudinal studies investigating the predictive ability of baseline intestinal microbiota concerning treatment outcome and complications as well as the potential use of microbiota-modulating strategies in cancer patients are required. More knowledge in this field is likely to be of clinical benefit since modulation of the microbiota might support cancer therapy in the future. Keywords: human intestinal microbiota; systemic cancer therapy; chemotherapy; immunotherapy; hormonal therapy; clinical relevance; baseline microbiota sampling; longitudinal microbiota sampling; 16S rRNA gene sequencing; metagenomic sequencing 1. Introduction The human microbiota is the collection of bacteria, archaea, viruses, and eukaryotic microorganisms that live in and on the human gastrointestinal tract, mucosae, and skin. The microbiome is the collective genome of the microbiota and encodes approximately 100-fold more genes than the human genome itself [1]. The majority of the microbiota resides in the gastrointestinal tract and belongs to the ‘intestinal microbiota’ or ‘gut microbiota’. Int. J. Mol. Sci. 2019, 20, 4145; doi:10.3390/ijms20174145 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 4145 2 of 34 Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 36 It has been established that cross-talk between the gut microbiota and the human host is essential fordysbiosis maintaining has been homeostasis shown to be and associated human health with various [2]. Therefore, metabolic it and is not infl surprisingammatory thatdiseases, microbial such dysbiosisas ulcerative has colitis, been shown obesity, to bediabetes associated mellitus, with and various hypertension metabolic [3–5]. and inflammatory diseases, such as ulcerativeNext colitis,to the obesity,taxonomic diabetes composition mellitus, andof the hypertension gut microbiota, [3–5]. the intra- and inter-individual diversityNext toof thethe taxonomicmicrobial compositioncommunity ofare the considered gut microbiota, to be theof great intra- andimportance inter-individual [3,4,6]. Microbial diversity ofdiversity the microbial can be community quantified are by considered means of to betwo of metrics: great importance α-diversity [3,4 ,6and]. Microbial β-diversity. diversity α-diversity can be quantifieddescribes the by number means of (richness) two metrics: and αdistribution-diversity and(evenness)β-diversity. of taxaα-diversity in a given describes sample [7]. the Common number (richness)indices to anddescribe distribution α-diversity (evenness) are the Shannon of taxa in index, a given Simpson sample index, [7]. Common and the Chao indices 1 index to describe [7]. β- αdiversity-diversity defines are the the Shannon number index, of taxa Simpson shared index, between and thedifferent Chao 1samples index [7and]. β -diversitycan be seen defines as a the(dis)similarity number of taxascore shared [7]. Generally, between dia healthyfferent samples state is andcharacterized can be seen by asa aspecies-rich, (dis)similarity diverse, score and [7]. Generally,stable microbiota, a healthy which state fulfills is characterized various and by complex a species-rich, metabolic diverse, roles [8]. and stable microbiota, which fulfillsIn various recent andyears, complex increasing metabolic evidence roles shows [8]. that the gut microbiota has an important role in carcinogenesisIn recent years, and the increasing pathophysiology evidence of shows human that cancer. the gut For microbiota instance, infection has an important with Helicobacter role in carcinogenesispylori is considered and theto stimulate pathophysiology the development of human of gastric cancer. carcinoma For instance, by producing infection with virulenceHelicobacter factors pyloriand enhancingis considered chronic to stimulate inflammation the development and subsequent of gastric carcinogenesis carcinoma by [9]. producing Similarly, virulence abundance factors of andFusobacterium enhancing nucleatum chronicinflammation has been found and to subsequentbe increased carcinogenesis in colorectal cancer [9]. Similarly, and it is suggested abundance that of Fusobacteriumthis bacterial nucleatumspecies mighthas beenbe involved found to in be intestinal increased tumorigenesis in colorectal cancerand modulation and it is suggested of the tumor that thismicroenvironment bacterial species [10,11]. might be involved in intestinal tumorigenesis and modulation of the tumor microenvironmentInterestingly, the [10, 11involvement]. of the gut microbiota is not limited to gastrointestinal cancers. It has beenInterestingly, suggested the that involvement gut bacteria of theaffect gut the microbiota development is not limitedof breast to cancer gastrointestinal through modulation cancers. It has of beenestrogen suggested metabolism that gut [12,13]. bacteria aInff ectline the with development this, it ofhas breast been cancer demonstrated through modulation that gut ofmicrobiota estrogen metabolismcomposition, [12 as,13 well]. In as line several with this,functional it has beenfeatur demonstratedes, differ between that gutpostme microbiotanopausal composition, breast cancer as wellpatients as several and healthy functional controls features, [14]. diFurthermore,ffer between Ra postmenopausaljagopala et al. breast(2016) cancerdemonstrated patients that and patients healthy controlswith leukemia [14]. Furthermore, already had Rajagopala reduced microbial et al. (2016) divers demonstratedity and dysbiosis that patients at the withtime leukemiaof diagnosis already and hadcould reduced be distinguished microbial diversityfrom healthy and controls dysbiosis based at the on time their of microbiota diagnosis profiles and could [15]. be distinguished fromWhile healthy there controls are strong based indications on their microbiota for the role profiles of the [15 gut]. microbiota in carcinogenesis, evidence concerningWhile thereits role are strongin the indicationscontext of forcancer the roletreatment of the gutis scarce. microbiota Currently, in carcinogenesis, most of the evidence results concerningconcerning its interactions role in the contextbetween of cancerthe gut treatment microbio ista scarce. and cancer Currently, therapy most oforiginate the results from concerning in-vitro interactionsstudies using between culturing the methods gut microbiota [16–18]. andA comprehens cancer therapyive overview originate of from clinical in-vitro studies studies in this using field culturingof research methods is lacking. [16 –18]. A comprehensive overview of clinical studies in this field of research is lacking.This systematic review summarizes clinical studies investigating the influence of the intestinal microbiotaThis systematic on systemic review cancer summarizes therapy as clinical well as studies the influence investigating of systemic the influence cancerof therapy the intestinal on the microbiotaintestinal microbiota on systemic (Figure cancer 1). therapy We focused as well on as thechemotherapy, influence of immunoth systemic cancererapy, therapyand hormonal on the intestinaltherapy. microbiotaIn addition, (Figure Table1 ).A2 We in focused Appendix on chemotherapy,B provides an immunotherapy, overview of important and hormonal terms therapy.used in Inmicrobiota addition, research. Table A2 Byin Appendixproviding Ba providescomprehensive
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