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November 14 2024
JAMA Network Open recently published the results of a cohort study that analyzed the associations between sociodemographic and lifestyle factors and 1...
A growing body of evidence suggests that the gut microbiome plays a role in the etiology of neurodegenerative diseases, with indications that in at least some conditions, the very first signs of pathology occur in the GI tract first. Additionally, the “gut-brain axis,” i.e., the bilateral communication that occurs between the central nervous system (CNS) and the gut appears to be a plausible thread between these two systems. As reviewed previously, there are many reasons to suspect that gut dysfunction may precede the more recognizable symptoms of Parkinson’s disease, for example, including constipation which may occur decades in advance.
In one of the most striking examples of how this recent understanding may impact disease prevention and treatment, the results of a randomized and double-blind placebo-controlled phase 2 trial were recently published in EClinicalMedicine (part of the Lancet family of journals). The first of its kind and known as the GUT-PARFECT trial, 47 participants diagnosed with Parkinson’s disease (mild to moderate disease) were randomly allocated to one of two groups, both of which received fecal microbiota transplantation (FMT). The control (placebo group) received a single FMT via nasojejunal administration using their own stool, while the experimental group received a single FMT using stool from a healthy donor. The primary endpoint of this study was the change in the motor section score of the Movement Disorders Society-Unified Parkinson's Disease Rating Scale (MDS-UPDRS), measured in an off-medication state, between baseline and at 12 months. Participants were restricted to people under age 65 whose motor symptoms began after age 50, and multiple safety steps were included in the protocol, including a colonoscopy to screen for contraindications, quarantining and serological testing of fecal samples, etc.
After 12 months, the group receiving healthy donor FMT had a significant improvement in their MDS-UPDRS motor scores (decrease of 5.8) compared to the control group (decrease of 2.7), demonstrating that FMT can improve motor symptoms among people with mild to moderate Parkinson’s disease. The authors point out that in addition to being statistically significant, this degree of improvement is clinically meaningful. A radiopaque pellet test indicated that the healthy donor group also had a slower progression in constipation compared to the control group. No severe adverse events occurred, with only minor GI symptoms in the healthy donor group which resolved within one week. The authors also point out a number of strengths and weaknesses; for example, the small sample size may have prevented the detection of non-motor symptom improvement, it’s possible that multiple doses of FMT would have been more effective (but costly) compared to one, and while technically challenging, nasojejunal administration may have advantages in this population, as it may more effectively target the vagus nerve which does not innervate the entire colon. As pointed out by the authors, the vagus nerve is thought to play a role in Parkinson’s development, as suggested by the protective effect of vagotomy.
It must also be noted that a subsequent randomized and controlled clinical trial published in JAMA Neurology did not find a benefit with FMT among people with Parkinson’s disease. It is difficult to know why significant improvement was observed in the initial study, but not in this more recent one, as there are so many variables that are not well standardized or understood. Among these, the FMT was infused into the cecum rather than the jejunum, but factors related to donor selection, fecal processing, etc. could potentially be decisive.
Parkinson’s is not the only neurodegenerative disease in which the gut-brain axis appears relevant to disease etiology. For example, animal models of Alzheimer’s disease suggest that early disruption of the gut microbiome with antibiotic use may increase susceptibility for CNS dysfunction later in life, in part by enhancing senescent degenerative pathways. The diverse and bioactive compounds created by the microbiota in the gut (and which travel via the vagus nerve, through the circulatory system, etc.) likely modulate brain function. Metabolism of the amino acid tryptophan alone (via the kynurenine pathway, reviewed here) creates a variety of compounds, some of which are thought to be neuroprotective while others are neurotoxic. For instance, quinolinic acid (QUIN) is an NMDA receptor agonist that can cross the blood-brain barrier from the circulation, and in excess amounts, it may generate reactive oxygen species that cause neuronal damage. An imbalance of QUIN metabolites has been associated with multiple neurodegenerative diseases, including Alzheimer’s disease, Parkinson’s disease, multiple sclerosis, amyotrophic lateral sclerosis, and Huntington’s disease. Disruptions in the microbiome, damage to the integrity of the intestinal barrier, and a shift away from the bacterial synthesis of protective compounds (e.g., short chain fatty acids) have all been suggested as contributing factors.
A controlled trial evaluating FMT among patients at risk for Alzheimer’s disease has not yet been conducted, but a very small pilot trial suggests there may be a benefit here, too. In a single-arm trial with only 5 participants, FMT (uncontrolled, taken as capsules) was associated with an improved (or at least maintained) score on a variety of cognitive tests among people with mild cognitive impairment. While this study does not allow for larger conclusions, hopefully it helps to pave the way for larger controlled trials.
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