The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.
The Vagus Nerve is One Route of Transneural Invasion for Intranasally Inoculated Influenza A Virus in Mice
Open accessAbstract
Intranasally inoculated neurotropic influenza viruses in mice infect not only the respiratory tract but also the central nervous system (CNS), mainly the brain stem. 26 , 34 Previous studies suggested that the route of invasion of virus into the CNS was via the peripheral nervous system, especially the vagus nerve. To evaluate the transvagal transmission of the virus, we intranasally inoculated unilaterally vagectomized mice with a virulent influenza virus (strain 24a5b) and examined the distribution of the viral protein and genome by immunohistochemistry and in situ hybridization over time. An asymmetric distribution of viral antigens was observed between vagal (nodose) ganglia: viral antigen was detected in the vagal ganglion of the vagectomized side 2 days later than in the vagal ganglion of the intact side. The virus was apparently transported from the respiratory mucosa to the CNS directly and decussately via the vagus nerve and centrifugally to the vagal ganglion of the vagectomized side. The results of this study, thus, demonstrate that neurotropic influenza virus travels to the CNS mainly via the vagus nerve.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“CNS viral invasion can occur through vagus nerve mediated trans-synaptic route, through intranasal inoculation of the influenza virus [177].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [177]
In the citing paper
“Partially (ipsilaterally) vagotomized animals inoculated with the virus showed viral presence in the root ganglia, bilaterally.”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [177]
In the citing paper
“Trans-synaptic routes have been reported in different coronaviruses (CoVs), such as HEV67 [175, 176] and in the avian bronchitis virus [177, 178].”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [177]
In the citing paper
“The virus reached the ganglion contralateral to the de-afferentation first, suggesting a less effective transport after vagus nerve injury.”
From Cognitive decline following acute viral infections: literature review and projections for post-COVID-19 (2022) · cites this paper as [177]
Citations
Cites
Yuen, K., Chan, P., Peiris, M. J. S., Tsang, D., Que, T., Shortridge, K. F., Cheung, P., To, W., Ho, E., Sung, R. Y. T., et al. (1998) · The Lancet · doi:10.1016/s0140-6736(98)01182-9 · Cited by 1,054
Kalia, M., & Mesulam, M. M. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901930211 · Cited by 846
ENCEPHALOPATHY AND FATTY DEGENERATION OF THE VISCERA A DISEASE ENTITY IN CHILDHOOD
Reye, R. D. K., Morgan, G., & Baral, J. (1963) · The Lancet · doi:10.1016/s0140-6736(63)90554-3 · Cited by 823
Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus
Sodeik, B., Ebersold, M. W., & Helenius, A. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.5.1007 · Cited by 687
Cox, N. J., & Subbarao, K. (1999) · The Lancet · doi:10.1016/s0140-6736(99)01241-6 · Cited by 593
Mizuguchi, M., Abe, J., Mikkaichi, K., Noma, S., Yoshida, K., Yamanaka, T., & Kamoshita, S. (1995) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.58.5.555 · Cited by 460
Lu, X., Tumpey, T. M., Morken, T., Zaki, S. R., Cox, N. J., & Katz, J. M. (1999) · Journal of Virology · doi:10.1128/jvi.73.7.5903-5911.1999 · Cited by 371
Pathogenesis of Avian Influenza A (H5N1) Viruses in Ferrets
Zitzow, L. A., Rowe, T., Morken, T., Shieh, W., Zaki, S. R., & Katz, J. M. (2002) · Journal of Virology · doi:10.1128/jvi.76.9.4420-4429.2002 · Cited by 354
Card, J. P., Rinaman, L., Schwaber, J. S., Miselis, R. R., Whealy, M. E., Robbins, A. K., & Enquist, L. W. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-06-01974.1990 · Cited by 325
Interaction of the Rabies Virus P Protein with the LC8 Dynein Light Chain
Raux, H., Flamand, A., & Blondel, D. (2000) · Journal of Virology · doi:10.1128/jvi.74.21.10212-10216.2000 · Cited by 297
Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons
Smith, G. A., Gross, S. P., & Enquist, L. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061029798 · Cited by 273
Gao, P., Watanabe, S., Ito, T., Goto, H., Wells, K., McGregor, M. W., Cooley, A. J., & Kawaoka, Y. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.3184-3189.1999 · Cited by 270
Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis
Leopold, P. L., Kreitzer, G., Miyazawa, N., Rempel, S., Pfister, K. K., Rodriguez-Boulan, E., & Crystal, R. G. (2000) · Human Gene Therapy · doi:10.1089/10430340050016238 · Cited by 254
1918 INFLUENZA, ENCEPHALITIS LETHARGICA, PARKINSONISM
Ravenholt, R. T., & Foege, W. (1982) · The Lancet · doi:10.1016/s0140-6736(82)90820-0 · Cited by 248
HAEMORRHAGIC SHOCK AND ENCEPHALOPATHY: A NEW SYNDROME WITH A HIGH MORTALITY IN YOUNG CHILDREN
Levin, M., Kay, J. D., Gould, J. D., Hjelm, M., Pincott, J. R., Dinwiddie, R., & Matthew, D. J. (1983) · The Lancet · doi:10.1016/s0140-6736(83)90057-0 · Cited by 226
Ito, T., Goto, H., Yamamoto, E., Tanaka, H., Takeuchi, M., Kuwayama, M., Kawaoka, Y., & Otsuki, K. (2001) · Journal of Virology · doi:10.1128/jvi.75.9.4439-4443.2001 · Cited by 178
Park, C. H., Ishinaka, M., Takada, A., Kida, H., Kimura, T., Ochiai, K., & Umemura, T. (2002) · Archives of Virology · doi:10.1007/s00705-001-0750-x · Cited by 164
Self-citationGubareva, L. V., McCullers, J. A., Bethell, R. C., & Webster, R. G. (1998) · The Journal of Infectious Diseases · doi:10.1086/314515 · Cited by 149
Hadziefendic, S., & Haxhiu, M. A. (1999) · Journal of the Autonomic Nervous System · doi:10.1016/s0165-1838(99)00020-x · Cited by 122
The substantia nigra is a major target for neurovirulent influenza A virus.
Takahashi, M., Yamada, T., Nakajima, S., Nakajima, K., Yamamoto, T., & Okada, H. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.181.6.2161 · Cited by 120
Retrograde Transport of Intact Poliovirus Through the Axon via the Fast Transport System
Ohka, S., Yang, W., Terada, E., Iwasaki, K., & Nomoto, A. (1998) · Virology · doi:10.1006/viro.1998.9360 · Cited by 116
Morrison, L. A., Sidman, R. L., & Fields, B. N. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.9.3852 · Cited by 115
Postencephalitic parkinsonism – a review
Casals, J., Elizan, T. S., & Yahr, M. D. (1998) · Journal of Neural Transmission · doi:10.1007/s007020050086 · Cited by 108
Andries, K., & Pensaert, M. B. (1980) · American Journal of Veterinary Research · doi:10.2460/ajvr.1980.41.09.1372 · Cited by 106
Reinacher, M., Bonin, J., Narayan, O., & Scholtissek, C. (1983) · PubMed · Cited by 94
Influenza Virus Antigen in Postencephalitic Parkinsonism Brain
Gamboa, E. T. (1974) · Archives of Neurology · doi:10.1001/archneur.1974.00490400042003 · Cited by 89
Influenza virus infections and immunity: a review of human and animal models.
Kb, R. (1992) · PubMed · Cited by 82
The Pathogenesis of Pseudorabies in Mice following Peripheral Inoculation
Field, H. J., & Hill, T. J. (1974) · Journal of General Virology · doi:10.1099/0022-1317-23-2-145 · Cited by 78
Dickman, M. S. (2001) · Archives of Neurology · doi:10.1001/archneur.58.10.1696 · Cited by 75
Influenza‐associated encephalopathy in Japan: Pathogenesis and treatment
Sugaya, N. (2000) · Pediatrics International · doi:10.1046/j.1442-200x.2000.01200.x · Cited by 73
Influenza virus and neurological diseases
Hayase, Y., & Tobita, K. (1997) · Psychiatry and Clinical Neurosciences · doi:10.1111/j.1440-1819.1997.tb02580.x · Cited by 68
Reovirus serotypes 1 and 3 differ in their in vitro association with microtubules
Babiss, L. E., Luftig, R. B., Weatherbee, J. A., Weihing, R. R., Ray, U. R., & Fields, B. N. (1979) · Journal of Virology · doi:10.1128/jvi.30.3.863-874.1979 · Cited by 67
Shimeld, C., Efstathiou, S., & Hill, T. (2001) · Journal of Virology · doi:10.1128/jvi.75.11.5252-5262.2001 · Cited by 66
Shinya, K., SHIMADA, A., Ito, T., Otsuki, K., MORITA, T., Tanaka, H., Takada, A., Kida, H., & Umemura, T. (2000) · Archives of Virology · doi:10.1007/s007050050016 · Cited by 64
Self-citationOcular pathogenicity of herpes simplex virus
Hill, T. J. (1987) · Current Eye Research · doi:10.3109/02713688709020060 · Cited by 50
Mori, I., Diehl, A. D., Chauhan, A., Ljunggren, H., & Kristensson, K. (1999) · Journal of NeuroVirology · doi:10.3109/13550289909029476 · Cited by 46
Bilateral distribution of vagal motor and sensory nerve fibers in the rat's lungs and airways
Fontán, J. J. P., Diec, C. T., & Velloff, C. R. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.2.r713 · Cited by 38
Parallel mechanisms in neuropathogenesis of enteric virus infections
Morrison, L. A., & Fields, B. N. (1991) · Journal of Virology · doi:10.1128/jvi.65.6.2767-2772.1991 · Cited by 29
The GDVII Strain of Theiler’s Virus Spreads via Axonal Transport
Martinat, C., Jarousse, N., Prévost, M., & Brahic, M. (1999) · Journal of Virology · doi:10.1128/jvi.73.7.6093-6098.1999 · Cited by 27
SILVANO, F. D., Yoshikawa, M., Shimada, A., Otsuki, K., & Umemura, T. (1997) · Journal of Veterinary Medical Science · doi:10.1292/jvms.59.143 · Cited by 27
Self-citationShinya, K., SILVANO, F. D., MORITA, T., Shimada, A., Nakajima, M., Ito, T., Otsuki, K., & Umemura, T. (1998) · Journal of Veterinary Medical Science · doi:10.1292/jvms.60.627 · Cited by 19
Self-citationDavis, L. E., Blisard, K. S., & Kornfeld, M. (1990) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(90)90220-h · Cited by 17
Research works printed but not linked: 5
- Andries K, 1980, Am J Vet Res, 41, 1372
- Reinacher M, 1983, Lab Invest, 49, 686
- Renegar KB, 1992, Lab Anim Sci, 42, 222
- Tyler KL, 1997, Viral Pathogenesis, 837
- Von Economo C, 1917, Wien Klin Weshr, 30, 581
Cited by
Sorted by citations
Li, Y., Bai, W., & Hashikawa, T. (2020) · Journal of Medical Virology · doi:10.1002/jmv.25728 · Cited by 2,266
Desforges, M., Le Coupanec, A., Dubeau, P., Bourgouin, A., Lajoie, L., Dubé, M., & Talbot, P. J. (2019) · Viruses · doi:10.3390/v12010014 · Cited by 1,048
Parkinson's disease: a dual‐hit hypothesis
Hawkes, C. H., Del Tredici, K., & Braak, H. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00874.x · Cited by 1,021
Zubair, A. S., McAlpine, L. S., Gardin, T., Farhadian, S., Kuruvilla, D. E., & Spudich, S. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.2065 · Cited by 923
Neurologic alterations due to respiratory virus infections
Bohmwald, K., Gálvez, N. M. S., Ríos, M., & Kalergis, A. M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00386 · Cited by 636
Metadata
- Authors
- Matsuda, K., Park, C. H., Sunden, Y., Kimura, T., Ochiai, K., Kida, H., & Umemura, T.
- Affiliations
- Hokkaido University (JP)
- Corresponding author
- Umemura, T.
- Venue
- Veterinary Pathology
- Publisher
- SAGE Publications
- Published
- 2004-03
- Volume
- 41
- Issue
- 2
- Pages
- 101-107
- ISSN
- 0300-9858 (ISSN-L)
- 1544-2217
- OpenAlex
- W2105165121
- Cited by
- 189
- References
- 42
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 6 · 2023: 12 · 2022: 18 · 2021: 39 · 2020: 71 · 2019: 3 · 2018: 2 · 2016: 3 · 2015: 2 · 2014: 2 · 2013: 4 · 2012: 5
- FWCI
- 2.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Veterinary Pathology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- influenza A virus, vagus nerve, central nervous system infection, nodose ganglion, peripheral nervous system, viral dissemination, mouse model
- MeSH terms
- Animals, Brain Stem, Immunohistochemistry, Lung, Nodose Ganglion, Orthomyxoviridae Infections, Influenza A virus, Vagus Nerve, In Situ Hybridization, Respiratory Mucosa, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review