IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28678-x.html
   My bibliography  Save this article

Circulating microbial content in myeloid malignancy patients is associated with disease subtypes and patient outcomes

Author

Listed:
  • Jakob Woerner

    (Case Western Reserve University)

  • Yidi Huang

    (Case Western Reserve University)

  • Stephan Hutter

    (Munich Leukemia Laboratory)

  • Carmelo Gurnari

    (Cleveland Clinic Foundation)

  • Jesús María Hernández Sánchez

    (Centro de Investigación del Cáncer)

  • Janet Wang

    (Case Western Reserve University)

  • Yimin Huang

    (Case Western Reserve University)

  • Daniel Schnabel

    (Case Western Reserve University)

  • Michael Aaby

    (Case Western Reserve University)

  • Wanying Xu

    (Case Western Reserve University)

  • Vedant Thorat

    (Case Western Reserve University)

  • Dongxu Jiang

    (Cleveland Clinic Foundation)

  • Babal K. Jha

    (Cleveland Clinic Foundation)

  • Mehmet Koyuturk

    (Case Western Reserve University)

  • Jaroslaw P. Maciejewski

    (Cleveland Clinic Foundation)

  • Torsten Haferlach

    (Munich Leukemia Laboratory)

  • Thomas LaFramboise

    (Case Western Reserve University)

Abstract

Although recent work has described the microbiome in solid tumors, microbial content in hematological malignancies is not well-characterized. Here we analyze existing deep DNA sequence data from the blood and bone marrow of 1870 patients with myeloid malignancies, along with healthy controls, for bacterial, fungal, and viral content. After strict quality filtering, we find evidence for dysbiosis in disease cases, and distinct microbial signatures among disease subtypes. We also find that microbial content is associated with host gene mutations and with myeloblast cell percentages. In patients with low-risk myelodysplastic syndrome, we provide evidence that Epstein-Barr virus status refines risk stratification into more precise categories than the current standard. Motivated by these observations, we construct machine-learning classifiers that can discriminate among disease subtypes based solely on bacterial content. Our study highlights the association between the circulating microbiome and patient outcome, and its relationship with disease subtype.

Suggested Citation

  • Jakob Woerner & Yidi Huang & Stephan Hutter & Carmelo Gurnari & Jesús María Hernández Sánchez & Janet Wang & Yimin Huang & Daniel Schnabel & Michael Aaby & Wanying Xu & Vedant Thorat & Dongxu Jiang & , 2022. "Circulating microbial content in myeloid malignancy patients is associated with disease subtypes and patient outcomes," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28678-x
    DOI: 10.1038/s41467-022-28678-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28678-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-28678-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Dmitry Kobak & Philipp Berens, 2019. "The art of using t-SNE for single-cell transcriptomics," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    2. Gregory D. Poore & Evguenia Kopylova & Qiyun Zhu & Carolina Carpenter & Serena Fraraccio & Stephen Wandro & Tomasz Kosciolek & Stefan Janssen & Jessica Metcalf & Se Jin Song & Jad Kanbar & Sandrine Mi, 2020. "Microbiome analyses of blood and tissues suggest cancer diagnostic approach," Nature, Nature, vol. 579(7800), pages 567-574, March.
    3. Marlies Meisel & Reinhard Hinterleitner & Alain Pacis & Li Chen & Zachary M. Earley & Toufic Mayassi & Joseph F. Pierre & Jordan D. Ernest & Heather J. Galipeau & Nikolaus Thuille & Romain Bouziat & M, 2018. "Microbial signals drive pre-leukaemic myeloproliferation in a Tet2-deficient host," Nature, Nature, vol. 557(7706), pages 580-584, May.
    4. Catherine A. Lozupone & Jesse I. Stombaugh & Jeffrey I. Gordon & Janet K. Jansson & Rob Knight, 2012. "Diversity, stability and resilience of the human gut microbiota," Nature, Nature, vol. 489(7415), pages 220-230, September.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jos A. Bosch & Max Nieuwdorp & Aeilko H. Zwinderman & Mélanie Deschasaux & Djawad Radjabzadeh & Robert Kraaij & Mark Davids & Susanne R. Rooij & Anja Lok, 2022. "The gut microbiota and depressive symptoms across ethnic groups," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. J. McClatchy & R. Strogantsev & E. Wolfe & H. Y. Lin & M. Mohammadhosseini & B. A. Davis & C. Eden & D. Goldman & W. H. Fleming & P. Conley & G. Wu & L. Cimmino & H. Mohammed & A. Agarwal, 2023. "Clonal hematopoiesis related TET2 loss-of-function impedes IL1β-mediated epigenetic reprogramming in hematopoietic stem and progenitor cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Kiran Konain & Sadia & Turfa Nadeem & Adeed Khan & Warda Iqbal & Arsalan & Amir Javed & Ruby Khan & Kainat Jamil & Kainat Jamil, 2018. "Importance of Probiotics in Gastrointestinal Tract," Journal of Asian Scientific Research, Asian Economic and Social Society, vol. 8(3), pages 128-143, March.
    4. Leandro C. Hermida & E. Michael Gertz & Eytan Ruppin, 2022. "Predicting cancer prognosis and drug response from the tumor microbiome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Khalilullah Mayar & David G. Carmichael & Xuesong Shen, 2022. "Resilience and Systems—A Review," Sustainability, MDPI, vol. 14(14), pages 1-22, July.
    6. Bazeia, D. & Bongestab, M. & de Oliveira, B.F. & Szolnoki, A., 2021. "Effects of a pestilent species on the stability of cyclically dominant species," Chaos, Solitons & Fractals, Elsevier, vol. 151(C).
    7. Rong Ma & Eric D. Sun & James Zou, 2023. "A spectral method for assessing and combining multiple data visualizations," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Yunmin Yang & Binbin Chu & Jiayi Cheng & Jiali Tang & Bin Song & Houyu Wang & Yao He, 2022. "Bacteria eat nanoprobes for aggregation-enhanced imaging and killing diverse microorganisms," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Monika & Manoj Kumar Verma & Vasim Ahmed & Nar Singh Chauhan, 2017. "Human Gut Microbiome: an Imperative Element for Human Survival," Current Trends in Biomedical Engineering & Biosciences, Juniper Publishers Inc., vol. 6(1), pages 14-15, July.
    10. Kaiwen Wang & Yuqiu Yang & Fangjiang Wu & Bing Song & Xinlei Wang & Tao Wang, 2023. "Comparative analysis of dimension reduction methods for cytometry by time-of-flight data," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. L. Mathur & B. Szalai & N. H. Du & R. Utharala & M. Ballinger & J. J. M. Landry & M. Ryckelynck & V. Benes & J. Saez-Rodriguez & C. A. Merten, 2022. "Combi-seq for multiplexed transcriptome-based profiling of drug combinations using deterministic barcoding in single-cell droplets," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Debanjan Mukherjee & Ângelo Ferreira Chora & Jean-Christophe Lone & Ricardo S. Ramiro & Birte Blankenhaus & Karine Serre & Mário Ramirez & Isabel Gordo & Marc Veldhoen & Patrick Varga-Weisz & Maria M., 2022. "Host lung microbiota promotes malaria-associated acute respiratory distress syndrome," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Candice R. Gurbatri & Georgette A. Radford & Laura Vrbanac & Jongwon Im & Elaine M. Thomas & Courtney Coker & Samuel R. Taylor & YoungUk Jang & Ayelet Sivan & Kyu Rhee & Anas A. Saleh & Tiffany Chien , 2024. "Engineering tumor-colonizing E. coli Nissle 1917 for detection and treatment of colorectal neoplasia," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    14. Zhiyuan Yuan & Yisi Li & Minglei Shi & Fan Yang & Juntao Gao & Jianhua Yao & Michael Q. Zhang, 2022. "SOTIP is a versatile method for microenvironment modeling with spatial omics data," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    15. Todd D. Terhune & Richard C. Deth, 2018. "Aluminum Adjuvant-Containing Vaccines in the Context of the Hygiene Hypothesis: A Risk Factor for Eosinophilia and Allergy in a Genetically Susceptible Subpopulation?," IJERPH, MDPI, vol. 15(5), pages 1-16, May.
    16. Sarah L Hagerty & Kent E Hutchison & Christopher A Lowry & Angela D Bryan, 2020. "An empirically derived method for measuring human gut microbiome alpha diversity: Demonstrated utility in predicting health-related outcomes among a human clinical sample," PLOS ONE, Public Library of Science, vol. 15(3), pages 1-21, March.
    17. Ziyan Huang & Myung Chung & Kentaro Tao & Akiyuki Watarai & Mu-Yun Wang & Hiroh Ito & Teruhiro Okuyama, 2023. "Ventromedial prefrontal neurons represent self-states shaped by vicarious fear in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Lingjing Jiang & Niina Haiminen & Anna‐Paola Carrieri & Shi Huang & Yoshiki Vázquez‐Baeza & Laxmi Parida & Ho‐Cheol Kim & Austin D. Swafford & Rob Knight & Loki Natarajan, 2022. "Utilizing stability criteria in choosing feature selection methods yields reproducible results in microbiome data," Biometrics, The International Biometric Society, vol. 78(3), pages 1155-1167, September.
    19. Oscar Lorenzo & Marta Crespo-Yanguas & Tianyu Hang & Jairo Lumpuy-Castillo & Artur M. Hernández & Carolina Llavero & MLuisa García-Alonso & Jaime Ruiz-Tovar, 2020. "Addition of Probiotics to Anti-Obesity Therapy by Percutaneous Electrical Stimulation of Dermatome T6. A Pilot Study," IJERPH, MDPI, vol. 17(19), pages 1-14, October.
    20. Lena Takayasu & Wataru Suda & Eiichiro Watanabe & Shinji Fukuda & Kageyasu Takanashi & Hiroshi Ohno & Misako Takayasu & Hideki Takayasu & Masahira Hattori, 2017. "A 3-dimensional mathematical model of microbial proliferation that generates the characteristic cumulative relative abundance distributions in gut microbiomes," PLOS ONE, Public Library of Science, vol. 12(8), pages 1-20, August.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28678-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.