Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms
Open accessAbstract
BACKGROUND: The presence of Lewy bodies and Lewy neurites (LN) has been demonstrated in the enteric nervous system (ENS) of Parkinson's disease (PD) patients. The aims of the present research were to use routine colonoscopy biopsies (1) to analyze, in depth, enteric pathology throughout the colonic submucosal plexus (SMP), and (2) to correlate the pathological burden with neurological and gastrointestinal (GI) symptoms. METHODOLOGY/PRINCIPAL FINDINGS: A total of 10 control and 29 PD patients divided into 3 groups according to disease duration were included. PD and GI symptoms were assessed using the Unified Parkinson's Disease Rating Scale part III and the Rome III questionnaire, respectively. Four biopsies were taken from the ascending and descending colon during the course of a total colonoscopy. Immunohistochemical analysis was performed using antibodies against phosphorylated alpha-synuclein, neurofilaments NF 220 kDa (NF) and tyrosine hydroxylase (TH). The density of LN, labeled by anti-phosphorylated alpha-synuclein antibodies, was evaluated using a quantitative rating score. Lewy pathology was apparent in the colonic biopsies from 21 patients and in none of the controls. A decreased number of NF-immunoreactive neurons per ganglion was observed in the SMP of PD patients compared to controls. The amount of LN in the ENS was inversely correlated with neuronal count and positively correlated with levodopa-unresponsive features and constipation. CONCLUSION/SIGNIFICANCE: Analysis of the ENS by routine colonoscopy biopsies is a useful tool for pre-mortem neuropathological diagnosis of PD, and also provides insight into the progression of motor and non-motor symptoms.
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Levodopa-unresponsive features and constipation were positively associated with the amount of Lewy neurites in the enteric nervous system.
“Moreover, it has been shown that levodopa-unresponsive features and constipation were positively associated with the amount of Lewy neurites in the ENS (Lebouvier et al., 2010).”
From The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies (2017) · cites this paper as Lebouvier et al., 2010
Prolonged use of levodopa induces severe side effects such as dyskinesia and motor fluctuation, and as the disease progresses patients might eventually develop levodopa-resistance.
“The prolonged use of levodopa induces severe side effects such as dyskinesia and motor fluctuation (Schrag and Quinn, 2000) and as the disease progresses patients might eventually develop levodopa-resistance (Lebouvier et al., 2010;Lee and Koh, 2015).”
From The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies (2017) · cites this paper as Lebouvier et al., 2010
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Cites
Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.55.3.181 · Cited by 10,378 · see citing works
Spillantini, M. G., Schmidt, M. L., Lee, V. M.-Y., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997) · Nature · doi:10.1038/42166 · Cited by 8,382 · see citing works
Unified Parkinson's Disease Rating Scale
(2012) · Springer eBooks · doi:10.1007/springerreference_184495 · Cited by 3,071 · see citing works
Non-motor symptoms of Parkinson's disease: diagnosis and management
Chaudhuri, K. R., Healy, D. G., & Schapira, A. H. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(06)70373-8 · Cited by 2,807 · see citing works
Recent developments in Parkinson's disease
Fahn, S., Elton, R., MARSDEN, C. D., Calne, D. B., & Goldstein, M. (1986) · Raven Press eBooks · Cited by 2,306 · see citing works
Lees, A. J., Hardy, J., & Revesz, T. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60492-x · Cited by 1,956 · see citing works
α-Synuclein is phosphorylated in synucleinopathy lesions
Fujiwara, H., Hasegawa, M., Dohmae, N., Kawashima, A., Masliah, E., Goldberg, M., Shen, J., Takio, K., & Iwatsubo, T. (2002) · Nature Cell Biology · doi:10.1038/ncb748 · Cited by 1,906 · see citing works
Anderson, J. P., Walker, D., Goldstein, J. M., de Laat, R., Banducci, K., Caccavello, R. J., Barbour, R., Huang, J., Kling, K., Lee, M., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600933200 · Cited by 1,418 · see citing works
Braak, H., de Vos, R. A. I., Bohl, J., & Del Tredici, K. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.11.012 · Cited by 1,354 · see citing works
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 · see citing works
Gastrointestinal Dysfunction in Parkinson’s Disease
Fasano, A., Visanji, N. P., Liu, L. W. C., Lang, A. E., & Pfeiffer, R. F. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00007-1 · Cited by 1,016 · see citing works
Gastrointestinal dysfunction in Parkinson's disease
Pfeiffer, R. F. (2003) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00307-7 · Cited by 925 · see citing works
Arizona Parkinson’s Disease Consortium, Beach, T. G., Adler, C. H., Sue, L. I., Vedders, L., Lue, L., White III, C. L., Akiyama, H., Caviness, J. N., Shill, H. A., et al. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0664-3 · Cited by 911 · see citing works
Pathoanatomy of Parkinson’s disease
Braak, H., & Braak, E. (2000) · Journal of Neurology · doi:10.1007/pl00007758 · Cited by 693 · see citing works
Martínez‐Martín, P., Schapira, A. H. V., Stocchi, F., Sethi, K. D., Odin, P., Macphee, G. J. A., Brown, R. G., Naidu, Y., Clayton, L. M. S., Abe, K., et al. (2007) · Movement Disorders · doi:10.1002/mds.21586 · Cited by 556 · see citing works
Orimo, S., Uchihara, T., Nakamura, A., Mori, F., Kakita, A., Wakabayashi, K., & Takahashi, H. (2007) · Brain · doi:10.1093/brain/awm302 · Cited by 462 · see citing works
Psychometric validation of a constipation symptom assessment questionnaire.
Frank, L., Kleinman, L., Farup, C., Taylor, L., & Miner, P. (1999) · Scandinavian Journal of Gastroenterology · doi:10.1080/003655299750025327 · Cited by 459 · see citing works
Changes in motor subtype and risk for incident dementia in Parkinson's disease
Alves, G. W., Larsen, J. P., Emre, M., Wentzel‐Larsen, T., & Aarsland, D. (2006) · Movement Disorders · doi:10.1002/mds.20897 · Cited by 436 · see citing works
Singaram, C., Gaumnitz, E., Torbey, C., Ashraf, W., Quigley, E. M., Sengupta, A., & Pfeiffer, R. F. (1995) · The Lancet · doi:10.1016/s0140-6736(95)92707-7 · Cited by 364 · see citing works
Buhner, S., Li, Q., Vignali, S., Barbara, G., De Giorgio, R., Stanghellini, V., Cremon, C., Zeller, F., Langer, R., Daniel, H., et al. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.07.005 · Cited by 351 · see citing works
Wedel, T., Spiegler, J., Soellner, S., Roblick, U., Schiedeck, T., Bruch, H., & Krammer, H. (2002) · Gastroenterology · doi:10.1053/gast.2002.36600 · Cited by 324 · see citing works
Esophageal Lewy bodies associated with ganglion cell loss in achalasia
Qualman, S. J., Haupt, H. M., Yang, P. H., & Hamilton, S. R. (1984) · Gastroenterology · doi:10.1016/0016-5085(84)90079-9 · Cited by 305 · see citing works
Qualman, S. J., Haupt, H. M., Yang, P. H., & Hamilton, S. R. (1984) · PubMed · Cited by 295 · see citing works
Kuo, Y., Li, Z., Jiao, Y., Gaborit, N., Pani, A. K., Orrison, B. M., Bruneau, B. G., Giasson, B. I., Smeyne, R. J., Gershon, M. D., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq038 · Cited by 288 · see citing works
The Rate of Cognitive Decline in Parkinson Disease
Aarsland, D., Andersen, K., Larsen, J. P., Perry, R., Wentzel‐Larsen, T., Lolk, A., & Kragh-Sørensen, P. (2004) · Archives of Neurology · doi:10.1001/archneur.61.12.1906 · Cited by 284 · see citing works
Innervation of the gastrointestinal tract: Patterns of aging
Phillips, R. J., & Powley, T. L. (2007) · Autonomic Neuroscience · doi:10.1016/j.autneu.2007.04.005 · Cited by 272 · see citing works
Neuropathology of non-motor features of Parkinson disease
Dickson, D. W., Fujishiro, H., Orr, C., DelleDonne, A., Josephs, K. A., Frigerio, R., Burnett, M. S., Parisi, J. E., Klos, K. J., & Ahlskog, J. E. (2009) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(09)70769-2 · Cited by 267 · see citing works
The second brain and Parkinson’s disease
Lebouvier, T., Chaumette, T., Paillusson, S., Duyckaerts, C. J., Varannes, S. B. D., Neunlist, M., & Derkinderen, P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06873.x · Cited by 258 · see citing works
Self-citationOlfactory bulb α-synucleinopathy has high specificity and sensitivity for Lewy body disorders
Beach, T. G., White, C. L., Hladik, C. L., Sabbagh, M. N., Connor, D. J., Shill, H. A., Sue, L. I., Sasse, J., Bachalakuri, J., Henry-Watson, J., et al. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0450-7 · Cited by 236 · see citing works
Pathological lesions in colonic biopsies during Parkinson’s disease
Lebouvier, T., Chaumette, T., Damier, P., Coron, E., Touchefeu, Y., Vrignaud, S., Naveilhan, P., Galmiche, J.-P., Varannes, S. B. D., Derkinderen, P., et al. (2008) · Gut · doi:10.1136/gut.2008.162503 · Cited by 229 · see citing works
Self-citationHuman enteric neuropathies: morphology and molecular pathology
GIORGIO, R. D., & Camilleri, M. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2004.00538.x · Cited by 221 · see citing works
Lewy Body Pathology Involves Cutaneous Nerves
Ikemura, M., Saito, Y., Sengoku, R., Sakiyama, Y., Hatsuta, H., Kanemaru, K., Sawabe, M., Arai, T., Ito, G., Iwatsubo, T., et al. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e318186de48 · Cited by 214 · see citing works
Anlauf, M., Schäfer, M. K.-H., Eiden, L. E., & Weihe, E. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10599 · Cited by 213 · see citing works
Guidelines--Rome III Diagnostic Criteria for Functional Gastrointestinal Disorders.
(2006) · PubMed · Cited by 192 · see citing works
The enteric nervous system: normal functions and enteric neuropathies
Furness, J. (2008) · Neurogastroenterology and Motility · doi:10.1111/j.1365-2982.2008.01094.x · Cited by 188 · see citing works
Complications of diagnostic and therapeutic colonoscopy within a defined population in Sweden
Dafnis, G., Ekbom, A., Påhlman, L., et al. (2001) · Gastrointestinal Endoscopy · doi:10.1067/mge.2001.117545 · Cited by 178 · see citing works
Benarroch, E. E. (2007) · Neurology · doi:10.1212/01.wnl.0000281999.56102.b5 · Cited by 174 · see citing works
Biopsies of olfactory epithelium in patients with Parkinson's disease
Witt, M., Bormann, K., Gudziol, V., Pehlke, K., Barth, K., Minovi, A., Haehner, A., Reichmann, H., & Hummel, T. R. (2009) · Movement Disorders · doi:10.1002/mds.22464 · Cited by 154 · see citing works
Parkinson Disease With Old-Age Onset
Diederich, N. J., Moore, C. G., Leurgans, S. E., Chmura, T. A., & Goetz, C. G. (2003) · Archives of Neurology · doi:10.1001/archneur.60.4.529 · Cited by 147 · see citing works
Excess burden of constipation in Parkinson's disease: a pilot study
Kaye, J., Gage, H., Kimber, A., Storey, L., & Trend, P. (2006) · Movement Disorders · doi:10.1002/mds.20942 · Cited by 128 · see citing works
Neurodegeneration: a key factor in the ageing gut
Wade, P. R., & Cowen, T. (2004) · Neurogastroenterology & Motility · doi:10.1111/j.1743-3150.2004.00469.x · Cited by 126 · see citing works
Clinical availability of skin biopsy in the diagnosis of Parkinson's disease
Miki, Y., Tomiyama, M., Ueno, T., Haga, R., Nishijima, H., Suzuki, C., Mori, F., Kaimori, M., Baba, M., & Wakabayashi, K. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.12.027 · Cited by 113 · see citing works
Enteric neurodegeneration in ageing
Camilleri, M., Cowen, T., & Koch, T. R. (2008) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2007.01072.x · Cited by 109 · see citing works
Mirror movements in parkinsonism: evaluation of a new clinical sign
Espay, A. J. (2005) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.062950 · Cited by 106 · see citing works
Routine colonic biopsies as a new tool to study the enteric nervous system in living patients
Lebouvier, T., Coron, E., Chaumette, T., Paillusson, S., Varannes, S. B. D., Neunlist, M., & Derkinderen, P. (2009) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2009.01368.x · Cited by 86 · see citing works
Self-citationAllcock, L. M., Kenny, R. A., & Burn, D. J. (2006) · Movement Disorders · doi:10.1002/mds.20996 · Cited by 79 · see citing works
Ganns, D., Schroedl, F., Neuhuber, W., et al. (2006) · PubMed · doi:10.14670/hh-21.41 · Cited by 69 · see citing works
Enteric neurodegeneration in ageing
Camilleri, M., Cowen, T., & Koch, T. R. (2008) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2008.01134.x · Cited by 68 · see citing works
Alpha-synuclein immunopositive aggregates in the myenteric plexus of the aging Fischer 344 rat
Phillips, R. J., Walter, G. C., Ringer, B. E., Higgs, K. M., & Powley, T. L. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.07.025 · Cited by 66 · see citing works
Patterns of motor and non-motor features in Parkinson's disease
van Rooden, S. M., Jeukens‐Visser, M., Verbaan, D., Marinus, J., & van Hilten, J. J. (2009) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2008.166629 · Cited by 65 · see citing works
Age-related neuronal loss in the submucosal plexus of the colon of Fischer 344 rats
Phillips, R. J., Pairitz, J. C., & Powley, T. L. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.05.019 · Cited by 55 · see citing works
Long Vasodilator Reflexes Projecting Through the Myenteric Plexus in Guinea‐Pig Ileum
Reed, D. E., & Vanner, S. J. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.053140 · Cited by 46 · see citing works
Biopsable Neural Tissues: Toward New Biomarkers for Parkinson's Disease?
Lebouvier, T., Tasselli, M., Paillusson, S., Pouclet, H., Neunlist, M., & Derkinderen, P. (2010) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2010.00128 · Cited by 42 · see citing works
Self-citationPhillips, R. J., Rhodes, B. S., & Powley, T. L. (2006) · Anatomy and Embryology · doi:10.1007/s00429-006-0123-z · Cited by 40 · see citing works
Brain targeting through the autonomous nervous system: lessons from prion diseases
Haı̈k, S. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.01.008 · Cited by 30 · see citing works
Joiner, S., Linehan, J. M., Brandner, S., et al. (2005) · Gut · doi:10.1136/gut.2005.072447 · Cited by 30 · see citing works
Cerebellar degeneration and hearing loss in a patient with idiopathic myenteric ganglionitis
Basilisco, G., Gebbia, C., PERACCHI, M., et al. (2005) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200504000-00010 · Cited by 26 · see citing works
Cardiac sympathetic denervation is correlated with Parkinsonian midline motor symptoms
Kim, J., Lee, K., Song, I., et al. (2008) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2008.02.017 · Cited by 23 · see citing works
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Gut microbiota are related to Parkinson's disease and clinical phenotype
Scheperjans, F., Aho, V., Pereira, P. A. B., Koskinen, K., Paulin, L., Pekkonen, E., Haapaniemi, E., Kaakkola, S., Eerola‐Rautio, J., Pohja, M., et al. (2015) · Movement Disorders · doi:10.1002/mds.26069 · Cited by 1,968 · see citing works
Cattaneo, A., Cattane, N., Galluzzi, S., Provasi, S., Lopizzo, N., Festari, C., Ferrari, C., Guerra, U. P., Paghera, B., Muscio, C., et al. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.08.019 · Cited by 1,382 · see citing works
Gastrointestinal Dysfunction in Parkinson’s Disease
Fasano, A., Visanji, N. P., Liu, L. W. C., Lang, A. E., & Pfeiffer, R. F. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00007-1 · Cited by 1,016 · see citing works
Forsyth, C. B., Shannon, K. M., Kordower, J. H., Voigt, R. M., Shaikh, M., Jaglin, J. A., Estes, J. D., Dodiya, H. B., & Keshavarzian, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028032 · Cited by 974 · see citing works
Bedarf, J. R., Hildebrand, F., Coelho, L. P., Sunagawa, S., Bahram, M., Goeser, F., Bork, P., & Wüllner, U. (2017) · Genome Medicine · doi:10.1186/s13073-017-0428-y · Cited by 642 · see citing works
Colonic inflammation in Parkinson's disease
Devos, D., Lebouvier, T., Lardeux, B., Biraud, M., Rouaud, T., Pouclet, H., Coron, E., Bruley des Varannes, S., Naveilhan, P., Nguyen, J.-M., et al. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.09.007 · Cited by 627 · see citing works
Self-citationThe gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis?
Houser, M. C., & Tansey, M. G. (2017) · npj Parkinson's Disease · doi:10.1038/s41531-016-0002-0 · Cited by 588 · see citing works
Brain-Gut-Microbiota Axis in Parkinson’s Disease
Mulak, A. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i37.10609 · Cited by 583 · see citing works
Alpha-synuclein in colonic submucosa in early untreated Parkinson’s disease
Shannon, K. M., Keshavarzian, A., Mutlu, E., Dodiya, H. B., Daian, D., Jaglin, J. A., & Kordower, J. H. (2012) · Movement Disorders · doi:10.1002/mds.23838 · Cited by 469 · see citing works
Altered gut microbiota and inflammatory cytokine responses in patients with Parkinson's disease
Lin, C.-H., Chen, C.-C., Chiang, H.-L., Liou, J.-M., Chang, C.-M., Lu, T.-P., Chuang, E. Y., Tai, Y.-C., Cheng, C., Lin, H.-Y., et al. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1528-y · Cited by 469 · see citing works
Is alpha-synuclein in the colon a biomarker for premotor Parkinson’s disease? Evidence from 3 cases
Shannon, K. M., Keshavarzian, A., Dodiya, H. B., Jakate, S., & Kordower, J. H. (2012) · Movement Disorders · doi:10.1002/mds.25020 · Cited by 464 · see citing works
Linking Neuroinflammation and Neurodegeneration in Parkinson's Disease
Gelders, G., Baekelandt, V., & Van der Perren, A. (2018) · Journal of Immunology Research · doi:10.1155/2018/4784268 · Cited by 430 · see citing works
Exploring Braak’s hypothesis of Parkinson’s disease
Rietdijk, C. D., Perez-Pardo, P., Garssen, J., van Wezel, R. J. A., & Kraneveld, A. D. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00037 · Cited by 395 · see citing works
Multiple organ involvement by alpha-synuclein pathology in lewy body disorders
Gelpi, E., Navarro‐Otano, J., Tolosa, E., Gaig, C., Compta, Y., Rey, M. J., Martí, M. J., Hernández, I., Valldeoriola, F., Reñé, R., et al. (2014) · Movement Disorders · doi:10.1002/mds.25776 · Cited by 361 · see citing works
Cersosimo, M. G., Raina, G. B., Pecci, C., Pellene, A., Calandra, C. R., Gutiérrez, C., Micheli, F. E., & Benarroch, E. E. (2013) · Journal of Neurology · doi:10.1007/s00415-012-6801-2 · Cited by 314 · see citing works
Kelly, L. P., Carvey, P. M., Keshavarzian, A., Shannon, K. M., Shaikh, M., Bakay, R. A. E., & Kordower, J. H. (2014) · Movement Disorders · doi:10.1002/mds.25736 · Cited by 308 · see citing works
Alpha‐Synuclein as a Biomarker for Parkinson's Disease
Atik, A., Stewart, T., & Zhang, J. (2016) · Brain Pathology · doi:10.1111/bpa.12370 · Cited by 311 · see citing works
Neuroinflammation in Neurodegenerative Disorders-a Review
Schain, M., & Kreisl, W. C. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0733-2 · Cited by 301 · see citing works
The prion hypothesis in Parkinson's disease: braak to the future
Visanji, N. P., Brooks, P. L., Hazrati, L.-N., & Lang, A. E. (2013) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-1-2 · Cited by 278 · see citing works
The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies
Perez-Pardo, P., Kliest, T., Dodiya, H. B., Broersen, L. M., Garssen, J., Keshavarzian, A., & Kraneveld, A. D. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.05.042 · Cited by 203 · see citing works
“Moreover, it has been shown that levodopa-unresponsive features and constipation were positively associated with the amount of Lewy neurites in the ENS (Lebouvier et al., 2010).”
BackgroundEnteric <scp>GFAP</scp> expression and phosphorylation in Parkinson's disease
Clairembault, T., Kamphuis, W., Leclair‐Visonneau, L., Rolli‐Derkinderen, M., Coron, E., Neunlist, M., Hol, E. M., & Derkinderen, P. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12742 · Cited by 191 · see citing works
Self-citationNeuronal vulnerability, pathogenesis, and Parkinson's disease
Sulzer, D., & Surmeier, D. J. (2013) · Movement Disorders · doi:10.1002/mds.25187 · Cited by 184 · see citing works
Premotor Parkinson’s disease: Concepts and definitions
Siderowf, A., & Lang, A. E. (2012) · Movement Disorders · doi:10.1002/mds.24954 · Cited by 174 · see citing works
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Lubomski, M., Tan, A. H., Lim, S.-Y., Holmes, A. J., Davis, R. L., & Sue, C. M. (2020) · Journal of Neurology · doi:10.1007/s00415-019-09320-1 · Cited by 172 · see citing works
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Yang, D., Zhao, D., Ali Shah, S. Z., Wu, W., Lai, M., Zhang, X., Li, J., Guan, Z., Zhao, H., Li, W., et al. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01155 · Cited by 162 · see citing works
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Self-citationGold, A., Turkalp, Z. T., & Munoz, D. G. (2013) · Movement Disorders · doi:10.1002/mds.25298 · Cited by 132 · see citing works
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Clairembault, T., Leclair‐Visonneau, L., Neunlist, M., & Derkinderen, P. (2015) · Movement Disorders · doi:10.1002/mds.25979 · Cited by 117 · see citing works
Self-citationIn vivo gastric detection of α-synuclein inclusions in Parkinson's disease
Sánchez‐Ferro, Á., Rábano, A., Catalán, M. J., Rodríguez‐Valcárcel, F. C., Díez, S. F., Herreros‐Rodríguez, J., García‐Cobos, E., Álvarez‐Santullano, M. M., López‐Manzanares, L., Mosqueira, A. J., et al. (2015) · Movement Disorders · doi:10.1002/mds.25988 · Cited by 123 · see citing works
Tsao, S.-P., Nurrahma, B. A., Kumar, R., Wu, C.-H., Yeh, T.-H., Chiu, C.-C., Lee, Y.-P., Liao, Y.-C., Huang, C.-H., Yeh, Y.-T., et al. (2021) · Antioxidants · doi:10.3390/antiox10111823 · Cited by 79 · see citing works
The pathology roadmap in Parkinson disease
Surmeier, D. J., & Sulzer, D. (2013) · Prion · doi:10.4161/pri.23582 · Cited by 74 · see citing works
Akhtar, R. S., Licata, J. P., Luk, K. C., Shaw, L. M., Trojanowski, J. Q., & Lee, V. M. ‐. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14330 · Cited by 60 · see citing works
Miyazaki, I., Isooka, N., Wada, K., Kikuoka, R., Kitamura, Y., & Asanuma, M. (2019) · Cells · doi:10.3390/cells8030221 · Cited by 53 · see citing works
Bencsik, A., Muselli, L., Leboidre, M., Lakhdar, L., & Baron, T. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000137 · Cited by 48 · see citing works
Association of Parkinson’s Disease With Microbes and Microbiological Therapy
Chen, Z.-J., Liang, C.-Y., Yang, L.-Q., Ren, S.-M., Xia, Y.-M., Cui, L., Li, X.-F., & Gao, B.-L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.619354 · Cited by 45 · see citing works
Sleep disturbances in Parkinson's disease patients and management options
Claassen, D. (2011) · Nature and Science of Sleep · doi:10.2147/nss.s18897 · Cited by 29 · see citing works
Grathwohl, S., Quansah, E., Maroof, N., Steiner, J. A., Spycher, L., Benmansour, F., Duran-Pacheco, G., Siebourg-Polster, J., Oroszlan-Szovik, K., Remy, H., et al. (2020) · doi:10.21203/rs.3.rs-100199/v1 · Cited by 17 · see citing works
- Authors
- Lebouvier, T., Neunlist, M., Bruley des Varannes, S., Coron, E., Drouard, A., N'Guyen, J.-M., Chaumette, T., Tasselli, M., Paillusson, S., Flamand, M., Galmiche, J.-P., Damier, P., & Derkinderen, P.
- Affiliations
- Inserm (FR)
- Corresponding author
- Lebouvier, Thibaud
- Neunlist, Michel
- Derkinderen, Pascal
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-09-14
- Volume
- 5
- Issue
- 9
- Pages
- e12728
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2939055
- OpenAlex
- W2054107031
- Cited by
- 427
- References
- 58
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 19 · 2023: 22 · 2022: 19 · 2021: 28 · 2020: 26 · 2019: 35 · 2018: 29 · 2017: 35 · 2016: 34 · 2015: 32 · 2014: 33 · 2013: 27 · 2012: 36
- FWCI
- 15.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Michael J. Fox Foundation for Parkinson's Research
- Institut National de la Santé et de la Recherche Médicale
- Association France Parkinson
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- Parkinson's disease, enteric nervous system, Lewy bodies, Lewy neurites, colonic biopsy, submucosal plexus, alpha-synuclein phosphorylation, neurofilaments, tyrosine hydroxylase, constipation, gastrointestinal symptoms, disease progression
- MeSH terms
- Adult, Aged, Biopsy, Colon, Colonoscopy, Female, Humans, Male, Middle Aged, Parkinson Disease, Lewy Bodies, Enteric Nervous System
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