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Mesenchymal Stromal Cell‐derived Extracellular Vesicles in Preclinical Animal Models of Tumor Growth: Systematic Review and Meta‐analysis

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Abstract

Background

Mesenchymal stromal cell derived extracellular vesicles (MSC-EVs) have been implicated in the regulation of tumor growth. Studies remain preclinical with effects ranging from inhibition of tumor growth to cancer progression. A systematic review and meta-analysis is needed to clarify the effect of MSC-EVs on tumor growth to facilitate potential translation to clinical trials.

Methods

A systematic search of the literature (MEDLINE, Embase, and BIOSIS databases to June 1, 2019) identified all pre-clinical controlled studies investigating the effect of MSC-EVs on tumor growth. Study selection and data extraction were performed in duplicate. Potential risk of bias was assessed using the SYRCLE tool. A random effects meta-analysis of reduction in tumor weight/volume (primary outcome) was performed.

Results

We identified 29 articles and 22 reported data on tumor responses that were included for meta-analysis. Studies were associated with unclear risk of bias in a large proportion of domains in accordance with the SYRCLE tool for determining risk of bias in preclinical studies. A high risk of bias was not identified in any study. MSC-EVs had a mixed response on tumor progression with some studies reporting inhibition of tumor growth and others reporting tumor progression. Overall, MSC-EVs exerted a non-significant reduction in tumor growth compared to controls (standardized mean difference (SMD) -0.80, 95 % CI -1.64 to 0.03, p = 0.06, I2 = 87 %). Some studies reported increased tumor growth which aligned with their stated hypothesis and some interrogated mechanisms in cancer biology. EVs isolated from MSCs that overexpressed anti-tumor RNAs were associated with significant tumor reduction in meta-analysis (SMD − 2.40, 95 % CI -3.36 to -1.44, p < 0.001). Heterogeneity between studies was observed and included aspects of study design such as enrichment of MSC-EVs with specific anti-tumor molecules, tissue source of MSCs, method of EV isolation, characterization of MSCs and EVs, dosage and administration schedules, and tissue type and source of tumor cells studied.

Conclusions

MSC-EVs are associated with mixed effects on tumor growth in animal models of cancer. In studies where anti-tumor RNAs are packaged in EVs, a significant reduction in tumor growth was observed. Reducing heterogeneity in study design may accelerate our understanding of the potential effects of MSC-EVs on cancer. [274 words]

Graphical Abstract

Forest plot of MSC-EV effect on tumor growth accordinggenetic modification of EVs in animal studies identified from a systematicreview of the literature. All cohorts from studies with multiple interventiongroups are presented separately with control groups divided equally among thegroups. M, modified; H, hypoxia

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Funding

AB and was supported by funding from Canadian Blood Services. AT was supported by a Vanier Canada Graduate Scholarship from CIHR and the Canadian Vascular Network Scholar Award. MS was supported by The Ottawa Hospital Foundation. MML is supported by The Ottawa Hospital Anesthesia Alternate Funds Association and holds a University of Ottawa Junior Research Chair in Innovative Translational Research.

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Authors and Affiliations

  1. Clinical Epidemiology, Ottawa Hospital Research Institute, Box 704, 501 Smyth Rd, ON, K1H 8L6, Ottawa, Canada

    Adrian J.M. Bailey, Alvin Tieu, Manika Gupta, Mitchell Slobodian, Risa Shorr, Tim Ramsay, Dean A. Fergusson, Manoj M. Lalu & David S. Allan

  2. Regenerative Medicine Programs, Ottawa Hospital Research Institute, Ottawa, ON, Canada

    Adrian J.M. Bailey, Alvin Tieu, Manoj M. Lalu & David S. Allan

  3. Departments of Medicine, University of Ottawa, Ottawa, ON, Canada

    Adrian J.M. Bailey, Manika Gupta, Tim Ramsay, Rosendo A. Rodriguez, Dean A. Fergusson & David S. Allan

  4. Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada

    Alvin Tieu & Manoj M. Lalu

  5. Medical Library and Learning Services, The Ottawa Hospital, Ottawa, ON, Canada

    Risa Shorr

  6. School of Epidemiology and Public Health, University of Ottawa, Ottawa, ON, Canada

    Tim Ramsay & Dean A. Fergusson

  7. Anesthesiology and Pain Medicine, University of Ottawa, Ottawa, ON, Canada

    Manoj M. Lalu

  8. Biochemistry, Microbiology & Immunology, Faculty of Medicine, University of Ottawa, Ottawa, ON, Canada

    David S. Allan

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  1. Adrian J.M. Bailey
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This article belongs to the Topical Collection: Special Issue on Exosomes and Microvesicles: from Stem Cell Biology to Translation in Human Diseases

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Bailey, A.J., Tieu, A., Gupta, M. et al. Mesenchymal Stromal Cell‐derived Extracellular Vesicles in Preclinical Animal Models of Tumor Growth: Systematic Review and Meta‐analysis. Stem Cell Rev and Rep 18, 993–1006 (2022). https://doi.org/10.1007/s12015-021-10163-5

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