Gut inflammation and dysbiosis in human motor neuron disease
Open accessAbstract
Amyotrophic lateral sclerosis (ALS) is a systemic disorder that involves dysfunction of multiple organs. Growing evidence has shown that neurodegenerative disorders with gut dysbiosis affect the central nervous system via pro-inflammatory mediators thus impacting gut-brain communications. We have demonstrated dysbiosis and increased intestinal permeability in the SOD1G93A ALS mouse model. In this study, we comprehensively examined the human gut microbiome in stool samples and evaluated infection and markers of intestinal inflammation in five patients with ALS and motor neuron disorders. Five patients we studied all had alteration in their gut microbiome characterized by a low diversity of the microbiome, compared to healthy cohorts with relatively intact abundance. Firmicutes and Bacteroidetes are the two major members of bacteria at the phylum level. Low Ruminococcus spp. occurred in three patients with low Firmicutes/Bacteroidetes (F/B) ratio. A majority of patients had signs of intestinal inflammation. This is the first comprehensive examination of inflammatory markers in the stool of ALS patients. Studies in gut health and microbiome related to the onset and progression of ALS may reveal novel therapeutic targets for disease modulation.
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In ALS patients, gastrointestinal symptoms precede neurological symptoms in all cases.
“Studies have found that, in ALS patients, gastrointestinal symptoms precede neurological symptoms in all cases (33); these include gastroesophageal reflux, chronic constipation, intermittent diarrhea, bloating, and abdominal pain.”
From Modulation of the gut–brain axis via the gut microbiota: a new era in treatment of amyotrophic lateral sclerosis (2023) · cites this paper as [33]
Blood endotoxin levels are elevated in amyotrophic lateral sclerosis patients, possibly as a result of gut inflammation and microbiome changes.
“Blood endotoxin levels are elevated in ALS patients [10], possibly as a result of gut inflammation and microbiome changes [102].”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [102]
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1 retracted
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ResultAberrant enteric neuromuscular system and dysbiosis in amyotrophic lateral sclerosis
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“ALS patients have elevated intestinal inflammation and dysbiosis.(10,11) The ENS and smooth muscle automatism are unable to modulate the motor functions of the digestive tract, which provide an anatomical explanation for these clinical manifestations.”
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“Specific dysbiotic intestinal conditions have been reported in the following neuro inflammatory diseases: Alzheimer’s disease [49–51]; Parkinson’s disease [52–54]; autism spectrum disorders [20,55]; multiple sclerosis [25,56] and amyotrophic lateral sclerosis (ALS) [57].”
BackgroundAmyotrophic lateral sclerosis and intestinal microbiota—toward establishing cause and effect
Gotkine, M., Kviatcovsky, D., & Elinav, E. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1767464 · Cited by 55 · see citing works
“The human form of ALS is a complex condition, and there are many ways in which the disease process itself could impact on the microbiome.(29,30) Addressing these potentially confounding effects in human disease will be a major challenge to establishing causality.”
BackgroundA Gut Feeling in Amyotrophic Lateral Sclerosis: Microbiome of Mice and Men
Martin, S., Battistini, C., & Sun, J. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.839526 · Cited by 54 · see citing works
Self-citationInterplay between immunity and amyotrophic lateral sclerosis: Clinical impact
Marchi, F. D., Munitić, I., Amedei, A., Berry, J. D., Feldman, E. L., Aronica, E., Nardo, G., Weehaeghe, D. V., Niccolai, E., Prtenjača, N., et al. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.027 · Cited by 52 · see citing works
Progression and survival of patients with motor neuron disease relative to their fecal microbiota
Ngo, S. T., Restuadi, R., McRae, A. F., van Eijk, R. P. A., Garton, F. C., Henderson, R. D., Wray, N. R., McCombe, P., & Steyn, F. J. (2020) · Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration · doi:10.1080/21678421.2020.1772825 · Cited by 53 · see citing works
Dynamic Changes in the Gut Microbiome at the Acute Stage of Ischemic Stroke in a Pig Model
Jeon, J. H., Lourenco, J. M., Kaiser, E. E., Waters, E. S., Scheulin, K. M., Fang, X., Kinder, H. A., Platt, S. R., Rothrock, M. J., Callaway, T. R., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.587986 · Cited by 54 · see citing works
Wang, J., Feng, W., Zhang, S., Chen, L., Sheng, Y., Tang, F., He, J., Xu, X., Ao, H., & Peng, C. Y. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.111887 · Cited by 52 · see citing works
The microbiota restrains neurodegenerative microglia in a model of amyotrophic lateral sclerosis
Cox, L. M., Calcagno, N., Gauthier, C., Madore, C., Butovsky, O., & Weiner, H. L. (2022) · Microbiome · doi:10.1186/s40168-022-01232-z · Cited by 53 · see citing works
“Two independent studies have found that butyrate producing bacteria were depleted in ALS [7, 8].”
BackgroundKim, H. S., Son, J. L., Lee, D., Tsai, J., Wang, D., Chocrón, E. S., Jeong, S., Kittrell, P., Murchison, C., Kennedy, R., et al. (2022) · BMC Neurology · doi:10.1186/s12883-022-02586-5 · Cited by 52 · see citing works
Healthy Gut, Healthy Brain: The Gut Microbiome in Neurodegenerative Disorders
Chandra, S., Alam, M. T., Dey, J., Sasidharan, B. C. P., Ray, U., Srivastava, A. K., Gandhi, S., & Tripathi, P. P. (2020) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026620666200413091101 · Cited by 51 · see citing works
Bacteriophages: Uncharacterized and Dynamic Regulators of the Immune System
Sinha, A., & Maurice, C. F. (2019) · Mediators of Inflammation · doi:10.1155/2019/3730519 · Cited by 50 · see citing works
“Consequently, a number of immunological disorders have been associated with shifts in microbial community composition [10, 73, 74].”
BackgroundGut microbiota in ALS: possible role in pathogenesis?
McCombe, P. A., Henderson, R. D., Lee, A., Lee, J. D., Woodruff, T. M., Restuadi, R., McRae, A., Wray, N. R., Ngo, S., & Steyn, F. J. (2019) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2019.1623026 · Cited by 46 · see citing works
“Within existing studies [250,251,253], it is possible that dysphagia contributed to the clear differences in reported outcomes between patients with ALS and controls.”
BackgroundMethodInfluentialHashim, H. M., & Makpol, S. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1007166 · Cited by 46 · see citing works
“healthy cohorts with relatively intact abundance (Rowin et al., 2017).”
Lu, G., Wen, Q., Cui, B., Li, Q., & Zhang, F. (2022) · Journal of Biomedical Research · doi:10.7555/jbr.36.20220088 · Cited by 43 · see citing works
Gubert, C., Love, C. J., Kodikara, S., Mei Liew, J. J., Renoir, T., Lê Cao, K.-A., & Hannan, A. J. (2022) · iScience · doi:10.1016/j.isci.2021.103687 · Cited by 41 · see citing works
Zhang, Y., Xia, Y., & Sun, J. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2363880 · Cited by 42 · see citing works
“3 Microbiome and intestinal homeostasis are known to play essential roles in neurological diseases, such as ALS, 4,5 Alzheimer’s disease , 6–8 and Parkinson’s disease.”
BackgroundSelf-citationMunir, M. U., Ali, S. A., Chung, K. H. K., Käkinen, A., Javed, I., & Davis, T. P. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2422468 · Cited by 44 · see citing works
Gut microbiome and amyotrophic lateral sclerosis: a systematic review of current evidence
Sun, J., Huang, T., Debelius, J. W., & Fang, F. (2021) · Journal of Internal Medicine · doi:10.1111/joim.13336 · Cited by 43 · see citing works
Self-citationButyrate as a potential therapeutic agent for neurodegenerative disorders
Chakraborty, P., Gamage, H. K. A. H., & Laird, A. S. (2024) · Neurochemistry International · doi:10.1016/j.neuint.2024.105745 · Cited by 41 · see citing works
Microbial signatures and therapeutic strategies in neurodegenerative diseases
Rob, M., Yousef, M., Lakshmanan, A. P., Mahboob, A., Terranegra, A., & Châari, A. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.117905 · Cited by 42 · see citing works
Convergent pathways of the gut microbiota–brain axis and neurodegenerative disorders
Gubert, C., Gasparotto, J., & Morais, L. H. (2022) · Gastroenterology report · doi:10.1093/gastro/goac017 · Cited by 40 · see citing works
Chiu, L. S., & Anderton, R. S. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15892 · Cited by 35 · see citing works
“A small case study examined inflammatory markers and stool samples in five MND patients, associating their condition with gut inflammation and dysbiosis (Rowin et al., 2017).”
BackgroundHong, D., Zhang, C., Wu, W., Lu, X., & Zhang, L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1133546 · Cited by 38 · see citing works
Chen, S., Cai, X., Lao, L., Wang, Y., Su, H., & Sun, H. (2024) · Aging and Disease · doi:10.14336/ad.2023.0524 · Cited by 38 · see citing works
“…of patients with ALS found that the concentrations of inflammatory markers such as sIgA, calmodulin and eosinophils in the feces of patients increased [116], which indicated that adaptive immune response activated in ALS patients may also pose challenges to the survival of some gut microbiota.”
BackgroundChen, S., Zhang, P., Duan, H., Wang, J., Qiu, Y., Cui, Z., Yin, Y., Wan, D., & Xie, L. (2023) · The Innovation · doi:10.1016/j.xinn.2023.100479 · Cited by 39 · see citing works
“They had higher levels of immunoglobulin A (IgA), calprotectin, and eosinophilic protein X in feces.(61) IL-2 levels were also greater in patients with ALS.”
Zhou, X., Lian, P., Liu, H., Wang, Y., Zhou, M., & Feng, Z. (2023) · Nutrients · doi:10.3390/nu15204445 · Cited by 40 · see citing works
Cryptosporidiosis Modulates the Gut Microbiome and Metabolism in a Murine Infection Model
Karpe, A. V., Hutton, M. L., Mileto, S. J., James, M. L., Evans, C., Shah, R., Ghodke, A. B., Hillyer, K. E., Metcalfe, S. S., Liu, J., et al. (2021) · Metabolites · doi:10.3390/metabo11060380 · Cited by 36 · see citing works
“Synthesis and metabolism of SCFAs by the gut microbiome modulate inflammatory cytokine activity [25], especially by increased butanoate and propionate production in the caecum and colon [24].”
BackgroundAdvancing human disease research with fish evolutionary mutant models
Beck, E. A., Healey, H. M., Small, C. M., Currey, M. C., Desvignes, T., Cresko, W. A., & Postlethwait, J. H. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.07.002 · Cited by 37 · see citing works
Gut microbiota immune cross-talk in amyotrophic lateral sclerosis
Kaul, M., Mukherjee, D., Weiner, H. L., & Cox, L. M. (2024) · Neurotherapeutics · doi:10.1016/j.neurot.2024.e00469 · Cited by 35 · see citing works
Uceda, S., Echeverry‐Alzate, V., Reiriz, M., Miguel, E. M., Pérez-Curiel, A., Gómez-Senent, S., & Beltrán-Velasco, A. I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713294 · Cited by 35 · see citing works
Bhuiyan, P., Chen, Y., Karim, M., Dong, H., & Qian, Y. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.04.010 · Cited by 33 · see citing works
Jiang, H., Li, R., Zhao, M., Peng, X., Sun, M., Liu, C., Liu, G., & Xue, H. (2024) · Aquatic Toxicology · doi:10.1016/j.aquatox.2024.106844 · Cited by 31 · see citing works
Seguella, L., Capuano, R., Sarnelli, G., & Esposito, G. (2019) · Expert Review of Clinical Pharmacology · doi:10.1080/17512433.2019.1612744 · Cited by 31 · see citing works
“with the pathogenesis of such neurological diseases [71,77,78].”
BackgroundWhat the Gut Tells the Brain—Is There a Link between Microbiota and Huntington’s Disease?
Wronka, D., Karlik, A., Misiorek, J. O., & Przybył, Ł. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054477 · Cited by 30 · see citing works
Trabjerg, M. S., Andersen, D. C., Huntjens, P., Oklinski, K. E., Bolther, L., Hald, J. L., Baisgaard, A. E., Mørk, K., Warming, N., Kullab, U. B., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02034-z · Cited by 29 · see citing works
Fontdevila, L., Povedano, M., Domínguez, R., Boada, J., Serrano, J. C. E., Pamplona, R., Ayala, V., & Portero‐Otín, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-75083-z · Cited by 29 · see citing works
“Nonetheless, our results mainly agree with previous reports 22 23 , mainly showing that fecal SCFA concentrations did not significantly differ between ALS patients and controls, or between patients with different clinical characteristics.”
ResultBoeri, L., Perottoni, S., Izzo, L., Giordano, C., & Albani, D. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202002043 · Cited by 28 · see citing works
Chu, X., Hou, Y., Meng, Q., Croteau, D. L., Wei, Y. Q., De, S., Becker, K. G., & Bohr, V. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.993615 · Cited by 28 · see citing works
“In addition, a low Firmicutes to Bacteroidetes (F/B) ratio is believed to be correlated with inflammation (Rowin et al., 2017).”
BackgroundErber, A. C., Çetin, H., Berry, D., & Schernhammer, E. S. (2019) · International Journal of Neuroscience · doi:10.1080/00207454.2019.1702549 · Cited by 28 · see citing works
“differences in the gut microbiome of ALS patients compared to controls [29,31,32,34,36,37], and four of these studies have been summarized in recent reviews [17,18].”
BackgroundResultCasani-Cubel, J., Benlloch, M., Sanchis-Sanchis, C. E., Marín, R., Lajara-Romance, J. M., & Ortí, J. E. D. L. R. (2021) · Metabolites · doi:10.3390/metabo11020120 · Cited by 29 · see citing works
“…that a decrease in the relation of the Firmicutes/Bacteroidetes phyla has been observed, causing an increase in Bacteroidetes phylum in ALS [55], as also described in the study conducted by Rowin et al. (2017) [56], and associated with a poor quality gut microbiota in babies and the elderly [57].”
BackgroundMinich, D. J., Madden, C. C., Evans, M. V., Ballash, G. A., Barr, D. J., Poulsen, K. P., Dennis, P. M., & Hale, V. L. (2021) · Scientific Reports · doi:10.1038/s41598-021-89896-9 · Cited by 27 · see citing works
Contribution of CNS and extra-CNS infections to neurodegeneration: a narrative review
Kettunen, P., Koıstınaho, J., & Rõlova, T. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03139-y · Cited by 25 · see citing works
Onisiforou, A., & Spyrou, G. M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.843128 · Cited by 25 · see citing works
“(78), but also other diseases such as Chron’s disease (79–81).”
BackgroundDiet-microbiome-gut-brain nexus in acute and chronic brain injury
Krakovski, M., Arora, N., Jain, S., Glover, J., Dombrowski, K. E., Hernandez, B., Yadav, H., & Sarma, A. K. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1002266 · Cited by 27 · see citing works
“Several human studies noted low Firmicutes/Bacteroidetes ratio in ALS patients (Fang et al., 2016; Rowin et al., 2017; Zeng et al., 2020).”
BackgroundGut-Modulating Agents and Amyotrophic Lateral Sclerosis: Current Evidence and Future Perspectives
Eddin, A. N., Alfuwais, M., Eddin, R. N., AlKattan, K. M., & Yaqinuddin, A. (2024) · Nutrients · doi:10.3390/nu16050590 · Cited by 26 · see citing works
“Some studies have reported that ALS patients exhibit significant shifts in the gut microbiome in favor of either Firmicutes [30,32,38] or Bacteroides [28,31,39,40], while others failed to detect any difference in the F/B ratio between ALS patients and controls [41].”
BackgroundGut microbiota links with cognitive impairment in amyotrophic lateral sclerosis: A multi-omics study
Gong, Z., Ba, L., Tang, J., Yang, Y., Li, Z., Liu, M., Yang, C., Ding, F., & Zhang, M. (2022) · Journal of Biomedical Research · doi:10.7555/jbr.36.20220198 · Cited by 25 · see citing works
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Cuffaro, F., Lamminpää, I., Niccolai, E., & Amedei, A. (2024) · Nutrients · doi:10.3390/nu17010102 · Cited by 25 · see citing works
“Emerging evidence suggests that GI symptoms often precede motor symptoms, highlighting a potential link between GM dysbiosis and the disease’s underlying mechanisms [68].”
Liu, C., Cheng, Y., Guo, Y., & Qian, H. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.06.009 · Cited by 24 · see citing works
Brain–body mechanisms contribute to sexual dimorphism in amyotrophic lateral sclerosis
Jacob, S. M., Lee, S., Kim, S. H., Sharkey, K. A., Pfeffer, G., & Nguyen, M. D. (2024) · Nature Reviews Neurology · doi:10.1038/s41582-024-00991-7 · Cited by 25 · see citing works
Ayoola, M. B., Pillai, N., Nanduri, B., Rothrock, M. J., & Ramkumar, M. (2023) · Animal Microbiome · doi:10.1186/s42523-023-00260-w · Cited by 24 · see citing works
“Relationships between microbiome dysbiosis and diseases such as ulcerative colitis, obesity and amyotrophic lateral sclerosis in humans has been established [19–21].”
BackgroundOnisiforou, A., & Spyrou, G. M. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab141 · Cited by 23 · see citing works
Gut-Brain Axis Deregulation and Its Possible Contribution to Neurodegenerative Disorders
Villavicencio-Tejo, F., Olesen, M. A., Navarro, L., Calisto, N., Iribarren, C., GARCÍA, K. P., Corsini, G., & Quintanilla, R. A. (2023) · Neurotoxicity Research · doi:10.1007/s12640-023-00681-0 · Cited by 23 · see citing works
“Inflammatory markers have also been found in ALS patients’ fecal sediments, determining a significant increase in fecal secretory IgA, calprotectin, and eosinophilic protein X, which is suggested to accompany ALS progression (Rowin et al. 2017).”
Gut Symptoms, Gut Dysbiosis and Gut-Derived Toxins in ALS
Lee, A., Henderson, R. D., Aylward, J., & McCombe, P. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031871 · Cited by 23 · see citing works
Parobková, E., & Matěj, R. (2021) · Diagnostics · doi:10.3390/diagnostics11030509 · Cited by 22 · see citing works
“Several preliminary studies have analyzed the fecal microbiota in ALS patients, but with no conclusive results [120,121].”
BackgroundFournier, C. N., Houser, M. C., Tansey, M. G., Glass, J. D., & Hertzberg, V. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.10.007 · Cited by 21 · see citing works
A network biology approach to unraveling inherited axonopathies
Bis‐Brewer, D. M., Danzi, M. C., Wuchty, S., & Zuchner, S. L. (2019) · Scientific Reports · doi:10.1038/s41598-018-37119-z · Cited by 19 · see citing works
- Authors
- Rowin, J., Xia, Y., Jung, B., & Sun, J.
- Affiliations
- Wellness and Integrative Neurology; Westchester Illinois
- University of Illinois Chicago (US)
- Corresponding author
- Sun, Jun
- Venue
- Physiological Reports
- Publisher
- Wiley
- Published
- 2017-09
- Volume
- 5
- Issue
- 18
- Pages
- e13443
- ISSN
- 2051-817X (ISSN-L)
- PMC
- PMC5617930
- OpenAlex
- W2759952551
- Cited by
- 224
- References
- 25
- Citations by year
- 2026: 23 · 2025: 21 · 2024: 32 · 2023: 22 · 2022: 29 · 2021: 38 · 2020: 25 · 2019: 20 · 2018: 13 · 2017: 1
- FWCI
- 6.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Physiological Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (R01 DK105118)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- amyotrophic lateral sclerosis, motor neuron disease, gut microbiota, dysbiosis, intestinal inflammation, intestinal permeability, gut-brain axis, Firmicutes/Bacteroidetes ratio, Ruminococcus, microbial diversity, SOD1 G93A mouse model
- MeSH terms
- Gastrointestinal Microbiome, Adult, Aged, Aged, 80 and over, Amyotrophic Lateral Sclerosis, Female, Humans, Male, Middle Aged, Inflammatory Bowel Diseases, Bacteroidetes, Ruminococcus, Dysbiosis
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