Near real-time intraoperative brain tumor diagnosis using stimulated Raman histology and deep neural networks.

Journal: Nature medicine
PMID: 31907460

Abstract

Intraoperative diagnosis is essential for providing safe and effective care during cancer surgery. The existing workflow for intraoperative diagnosis based on hematoxylin and eosin staining of processed tissue is time, resource and labor intensive. Moreover, interpretation of intraoperative histologic images is dependent on a contracting, unevenly distributed, pathology workforce. In the present study, we report a parallel workflow that combines stimulated Raman histology (SRH), a label-free optical imaging method and deep convolutional neural networks (CNNs) to predict diagnosis at the bedside in near real-time in an automated fashion. Specifically, our CNNs, trained on over 2.5 million SRH images, predict brain tumor diagnosis in the operating room in under 150 s, an order of magnitude faster than conventional techniques (for example, 20-30 min). In a multicenter, prospective clinical trial (n = 278), we demonstrated that CNN-based diagnosis of SRH images was noninferior to pathologist-based interpretation of conventional histologic images (overall accuracy, 94.6% versus 93.9%). Our CNNs learned a hierarchy of recognizable histologic feature representations to classify the major histopathologic classes of brain tumors. In addition, we implemented a semantic segmentation method to identify tumor-infiltrated diagnostic regions within SRH images. These results demonstrate how intraoperative cancer diagnosis can be streamlined, creating a complementary pathway for tissue diagnosis that is independent of a traditional pathology laboratory.

Authors

  • Todd C Hollon
    Departments of1Neurosurgery.
  • Balaji Pandian
    2School of Medicine, University of Michigan, Ann Arbor, Michigan.
  • Arjun R Adapa
    School of Medicine, University of Michigan, Ann Arbor, MI, USA.
  • Esteban Urias
    School of Medicine, University of Michigan, Ann Arbor, MI, USA.
  • Akshay V Save
    College of Physicians and Surgeons, Columbia University, New York, NY, USA.
  • Siri Sahib S Khalsa
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Daniel G Eichberg
    Department of Neurological Surgery, University of Miami, Miami, FL, USA.
  • Randy S D'Amico
    Neurological Surgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, USA.
  • Zia U Farooq
    Invenio Imaging, Inc., Santa Clara, CA, USA.
  • Spencer Lewis
    School of Medicine, University of Michigan, Ann Arbor, MI, USA.
  • Petros D Petridis
    College of Physicians and Surgeons, Columbia University, New York, NY, USA.
  • Tamara Marie
    Department of Pediatrics Oncology, Columbia University, New York, NY, USA.
  • Ashish H Shah
    Department of Neurological Surgery, University of Miami, Miami, FL, USA.
  • Hugh J L Garton
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Cormac O Maher
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Jason A Heth
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Erin L McKean
    Departments of1Neurosurgery.
  • Stephen E Sullivan
    Departments of1Neurosurgery.
  • Shawn L Hervey-Jumper
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Parag G Patil
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • B Gregory Thompson
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Oren Sagher
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Guy M McKhann
  • Ricardo J Komotar
    Department of Neurological Surgery, University of Miami, Miami, FL, USA.
  • Michael E Ivan
    Department of Neurological Surgery, University of Miami, Miami, FL, USA.
  • Matija Snuderl
    Department of Pathology, New York University, New York, NY, USA.
  • Marc L Otten
    Department of Neurological Surgery, Columbia University, New York, NY, USA.
  • Timothy D Johnson
    Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, MI, USA.
  • Michael B Sisti
    Department of Neurological Surgery, Columbia University, New York, NY, USA.
  • Jeffrey N Bruce
    Department of Neurological Surgery, Columbia University, New York, NY, USA.
  • Karin M Muraszko
    Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA.
  • Jay Trautman
    Invenio Imaging, Inc., Santa Clara, CA, USA.
  • Christian W Freudiger
    Invenio Imaging, Inc., Santa Clara, CA, USA.
  • Peter Canoll
    Department of Pathology & Cell Biology, Columbia University, New York, NY, USA.
  • Honglak Lee
  • Sandra Camelo-Piragua
    Department of Pathology, University of Michigan, Ann Arbor, MI, USA.
  • Daniel A Orringer
    Departments of1Neurosurgery.

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