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 inPain (Amsterdam) Vol. 161; no. 11; pp. 2592 - 2602
Main Authors Salvo, Elizabeth, Campana, Wendy M., Scheff, Nicole N., Nguyen, Tu Huu, Jeong, Se-hee, Wall, Ian, Wu, Angie K., Zhang, Susanna, Kim, Hyesung, Bhattacharya, Aditi, Janal, Malvin N., Liu, Cheng, Albertson, Donna G., Schmidt, Brian L., Dolan, John C., Schmidt, Robert E., Boada, M. Danilo, Ye, Yi
Format Journal Article
LanguageEnglish
Published 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.
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
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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
URI https://ovidsp.ovid.com/ovidweb.cgi?T=JS&NEWS=n&CSC=Y&PAGE=fulltext&D=ovft&AN=00006396-202011000-00016
https://www.ncbi.nlm.nih.gov/pubmed/32658150
https://www.proquest.com/docview/2423515832
https://pubmed.ncbi.nlm.nih.gov/PMC7572698
Volume 161
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