Peripheral nerve injury and sensitization underlie pain associated with oral cancer perineural invasion
Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater spontaneous pain and mechanical allodynia compared with patients without PNI, suggesting that unique mechanisms drive PNI-induced pain. We studied t...
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Published in | Pain (Amsterdam) Vol. 161; no. 11; pp. 2592 - 2602 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Wolters Kluwer
01.11.2020
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Abstract | Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater spontaneous pain and mechanical allodynia compared with patients without PNI, suggesting that unique mechanisms drive PNI-induced pain. We studied the impact of PNI on peripheral nerve physiology and anatomy using a murine sciatic nerve PNI model. Mice with PNI exhibited spontaneous nociception and mechanical allodynia. Perineural invasion induced afterdischarge in A high-threshold mechanoreceptors (HTMRs), mechanical sensitization (ie, decreased mechanical thresholds) in both A and C HTMRs, and mechanical desensitization in low-threshold mechanoreceptors. Perineural invasion resulted in nerve damage, including axon loss, myelin damage, and axon degeneration. Electrophysiological evidence of nerve injury included decreased conduction velocity, and increased percentage of both mechanically insensitive and electrically unexcitable neurons. We conclude that PNI-induced pain is driven by nerve injury and peripheral sensitization in HTMRs. |
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AbstractList | Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater spontaneous pain and mechanical allodynia compared with patients without PNI, suggesting that unique mechanisms drive PNI-induced pain. We studied the impact of PNI on peripheral nerve physiology and anatomy using a murine sciatic nerve PNI model. Mice with PNI exhibited spontaneous nociception and mechanical allodynia. Perineural invasion induced afterdischarge in A high-threshold mechanoreceptors (HTMRs), mechanical sensitization (ie, decreased mechanical thresholds) in both A and C HTMRs, and mechanical desensitization in low-threshold mechanoreceptors. Perineural invasion resulted in nerve damage, including axon loss, myelin damage, and axon degeneration. Electrophysiological evidence of nerve injury included decreased conduction velocity, and increased percentage of both mechanically insensitive and electrically unexcitable neurons. We conclude that PNI-induced pain is driven by nerve injury and peripheral sensitization in HTMRs. Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater spontaneous pain and mechanical allodynia compared with patients without PNI, suggesting that unique mechanisms drive PNI-induced pain. We studied the impact of PNI on peripheral nerve physiology and anatomy using a murine sciatic nerve PNI model. Mice with PNI exhibited spontaneous nociception and mechanical allodynia. Perineural invasion induced afterdischarge in A high-threshold mechanoreceptors (HTMRs), mechanical sensitization (ie, decreased mechanical thresholds) in both A and C HTMRs, and mechanical desensitization in low-threshold mechanoreceptors. Perineural invasion resulted in nerve damage, including axon loss, myelin damage, and axon degeneration. Electrophysiological evidence of nerve injury included decreased conduction velocity, and increased percentage of both mechanically insensitive and electrically unexcitable neurons. We conclude that PNI-induced pain is driven by nerve injury and peripheral sensitization in HTMRs.Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater spontaneous pain and mechanical allodynia compared with patients without PNI, suggesting that unique mechanisms drive PNI-induced pain. We studied the impact of PNI on peripheral nerve physiology and anatomy using a murine sciatic nerve PNI model. Mice with PNI exhibited spontaneous nociception and mechanical allodynia. Perineural invasion induced afterdischarge in A high-threshold mechanoreceptors (HTMRs), mechanical sensitization (ie, decreased mechanical thresholds) in both A and C HTMRs, and mechanical desensitization in low-threshold mechanoreceptors. Perineural invasion resulted in nerve damage, including axon loss, myelin damage, and axon degeneration. Electrophysiological evidence of nerve injury included decreased conduction velocity, and increased percentage of both mechanically insensitive and electrically unexcitable neurons. We conclude that PNI-induced pain is driven by nerve injury and peripheral sensitization in HTMRs. |
Author | Wall, Ian Kim, Hyesung Bhattacharya, Aditi Nguyen, Tu Huu Janal, Malvin N. Salvo, Elizabeth Dolan, John C. Ye, Yi Campana, Wendy M. Jeong, Se-hee Albertson, Donna G. Wu, Angie K. Zhang, Susanna Liu, Cheng Schmidt, Brian L. Schmidt, Robert E. Boada, M. Danilo Scheff, Nicole N. |
AuthorAffiliation | Department of Pathology, New York University Langone Medical Center, New York, NY, United States Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, United States Bluestone Center for Clinical Research, New York University College of Dentistry, New York, NY, United States Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, United States Department of Epidemiology and Health Promotion, New York University College of Dentistry, New York, NY, United States D.D.S. program, New York University College of Dentistry, New York, NY, United States |
AuthorAffiliation_xml | – name: Department of Epidemiology and Health Promotion, New York University College of Dentistry, New York, NY, United States – name: Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, United States – name: D.D.S. program, New York University College of Dentistry, New York, NY, United States – name: Bluestone Center for Clinical Research, New York University College of Dentistry, New York, NY, United States – name: Department of Pathology, New York University Langone Medical Center, New York, NY, United States – name: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, United States – name: 4 San Diego Veterans Health System, San Diego, CA 92161, USA – name: 5 New York University College of Dentistry, New York, NY, 10010, USA – name: 3 Department of Anesthesiology, School of Medicine, University of California, San Diego, CA 92093-0629, USA – name: 1 Bluestone Center for Clinical Research, New York University College of Dentistry, New York, NY, 10010, USA – name: 8 Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 7 Department of Pathology, New York University Langone Medical Center, New York, NY, 10010, USA – name: 9 Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, 27157-1009, USA – name: 2 Department of Oral and Maxillofacial Surgery, New York University College of Dentistry, New York, NY, 10010, USA – name: 6 Department of Epidemiology and Health Promotion, New York University College of Dentistry, New York, NY, 10010, USA |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Correspondence: Yi Ye, MS, PhD, Bluestone Center for Clinical Research, New York University College of Dentistry, 421 First Avenue, 233W, New York, New York 10010, yy22@nyu.edu, Tel: 212-998-9285, Fax: 212-995-4843 |
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Snippet | Cancer invading into nerves, termed perineural invasion (PNI), is associated with pain. Here, we show that oral cancer patients with PNI report greater... |
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SubjectTerms | Animals Cancer Pain - etiology Female Male Mice Mouth Neoplasms - complications Neoplasm Invasiveness Peripheral Nerve Injuries - etiology Peripheral Nerves Sciatic Nerve |
Title | Peripheral nerve injury and sensitization underlie pain associated with oral cancer perineural invasion |
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